Login Register Cart 0
Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Immunometabolism in the Bladder Cancer Microenvironment

Author(s): Mohammad Javad Fattahi, Mohammad Reza Haghshenas and Abbas Ghaderi*

Volume 22, Issue 12, 2022

Published on: 18 April, 2022

Page: [1201 - 1216] Pages: 16

DOI: 10.2174/1871530322666220104103905

Price: $65

Abstract

The initiation and progression of bladder cancer (BC) are dependent on its tumor microenvironment (TME). On the other hand, cancer cells shape and train TME to support their development, respond to treatment and migration in an organism. Immune cells exert key roles in the BC microenvironment and have complex interactions with BC cells. These complicated interplays result in metabolic competition in the TME, leading to nutrient deprivation, acidosis, hypoxia and metabolite accumulation, which impair immune cell function. Recent studies have demonstrated that immune cells functions are closely correlated with their metabolism. Immunometabolism describes the functional metabolic alterations that take place within immune cells and the role of these cells in directing metabolism and immune response in tissues or diseases such as cancer. Some molecules and their metabolites in the TME, including glucose, fatty acids and amino acids, can regulate the phenotype, function and metabolism of immune cells. Hence, here we describe some recent advances in immunometabolism and relate them to BC progression. A profound understanding of the metabolic reprogramming of BC cells and immune cells in the TME will offer novel opportunities for targeted therapies in future.

Keywords: Immunometabolism, bladder cancer, tumor microenvironment, metabolic reprogramming, immune cell functions, targeted therapies.

« Previous Next »
Graphical Abstract

[1]
Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer, 2015, 136(5), E359-E386.
[http://dx.doi.org/10.1002/ijc.29210] [PMID: 25220842]
[2]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2018. CA Cancer J. Clin., 2018, 68(1), 7-30.
[http://dx.doi.org/10.3322/caac.21442] [PMID: 29313949]
[3]
Sanli, O.; Dobruch, J.; Knowles, M.A.; Burger, M.; Alemozaffar, M.; Nielsen, M.E.; Lotan, Y. Bladder cancer. Nat. Rev. Dis. Primers, 2017, 3, 17022.
[http://dx.doi.org/10.1038/nrdp.2017.22] [PMID: 28406148]
[4]
Knowles, M.A.; Hurst, C.D. Molecular biology of bladder cancer: new insights into pathogenesis and clinical diversity. Nat. Rev. Cancer, 2015, 15(1), 25-41.
[http://dx.doi.org/10.1038/nrc3817] [PMID: 25533674]
[5]
Hayashi, T.; Fujita, K.; Hayashi, Y.; Hatano, K.; Kawashima, A.; McConkey, D.J.; Nonomura, N. Mutational landscape and environmental effects in bladder cancer. Int. J. Mol. Sci., 2020, 21(17), 6072-6086.
[http://dx.doi.org/10.3390/ijms21176072] [PMID: 32842545]
[6]
Yousef, P.G.; Gabril, M.Y. An update on the molecular pathology of urinary bladder tumors. Pathol. Res. Pract., 2018, 214(1), 1-6.
[http://dx.doi.org/10.1016/j.prp.2017.11.003] [PMID: 29254798]
[7]
Afonso, J.; Santos, L.L.; Longatto-Filho, A.; Baltazar, F. Competitive glucose metabolism as a target to boost bladder cancer immunotherapy. Nat. Rev. Urol., 2020, 17(2), 77-106.
[http://dx.doi.org/10.1038/s41585-019-0263-6] [PMID: 31953517]
[8]
Humphrey, P.A.; Moch, H.; Cubilla, A.L.; Ulbright, T.M.; Reuter, V.E. The 2016 WHO classification of tumours of the urinary system and male genital organs-part B: Prostate and bladder tumours. Eur. Urol., 2016, 70(1), 106-119.
[http://dx.doi.org/10.1016/j.eururo.2016.02.028] [PMID: 26996659]
[9]
Casey, S.C.; Amedei, A.; Aquilano, K.; Azmi, A.S.; Benencia, F.; Bhakta, D.; Bilsland, A.E.; Boosani, C.S.; Chen, S.; Ciriolo, M.R. Cancer prevention and therapy through the modulation of the tumor microenvironment. Semin. Cancer Biol., 2015, 35, S199-S223.
[http://dx.doi.org/10.1016/j.semcancer.2015.02.007]
[10]
Zhang, Y.; Ou, D.H.; Zhuang, D.W.; Zheng, Z.F.; Lin, M.E. In silico analysis of the immune microenvironment in bladder cancer. BMC Cancer, 2020, 20(1), 265.
[http://dx.doi.org/10.1186/s12885-020-06740-5] [PMID: 32228629]
[11]
Li, L.; Wang, L.; Li, J.; Fan, Z.; Yang, L.; Zhang, Z.; Zhang, C.; Yue, D.; Qin, G.; Zhang, T.; Li, F.; Chen, X.; Ping, Y.; Wang, D.; Gao, Q.; He, Q.; Huang, L.; Li, H.; Huang, J.; Zhao, X.; Xue, W.; Sun, Z.; Lu, J.; Yu, J.J.; Zhao, J.; Zhang, B.; Zhang, Y. Metformin-induced reduction of CD39 and CD73 blocks myeloid-derived suppressor cell activity in patients with ovarian cancer. Cancer Res., 2018, 78(7), 1779-1791.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2460] [PMID: 29374065]
[12]
Jin, M.Z.; Jin, W.L. The updated landscape of tumor microenvironment and drug repurposing. Signal Transduct. Target. Ther., 2020, 5(1), 166-182.
[http://dx.doi.org/10.1038/s41392-020-00280-x] [PMID: 32843638]
[13]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[14]
Fang, H.; Declerck, Y.A. Targeting the tumor microenvironment: from understanding pathways to effective clinical trials. Cancer Res., 2013, 73(16), 4965-4977.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-0661] [PMID: 23913938]
[15]
Crispen, P.L.; Kusmartsev, S. Mechanisms of immune evasion in bladder cancer. Cancer Immunol. Immunother., 2020, 69(1), 3-14.
[http://dx.doi.org/10.1007/s00262-019-02443-4] [PMID: 31811337]
[16]
Buck, M.D.; Sowell, R.T.; Kaech, S.M.; Pearce, E.L. Metabolic instruction of immunity. Cell, 2017, 169(4), 570-586.
[http://dx.doi.org/10.1016/j.cell.2017.04.004] [PMID: 28475890]
[17]
Pearce, E.L.; Pearce, E.J. Metabolic pathways in immune cell activation and quiescence. Immunity, 2013, 38(4), 633-643.
[http://dx.doi.org/10.1016/j.immuni.2013.04.005] [PMID: 23601682]
[18]
Yaqoob, P. Fatty acids as gatekeepers of immune cell regulation. Trends Immunol., 2003, 24(12), 639-645.
[http://dx.doi.org/10.1016/j.it.2003.10.002] [PMID: 14644137]
[19]
Lawless, S.J.; Kedia-Mehta, N.; Walls, J.F.; McGarrigle, R.; Convery, O.; Sinclair, L.V.; Navarro, M.N.; Murray, J.; Finlay, D.K. Glucose represses dendritic cell-induced T cell responses. Nat. Commun., 2017, 8, 15620.
[http://dx.doi.org/10.1038/ncomms15620] [PMID: 28555668]
[20]
Sikalidis, A.K. Amino acids and immune response: a role for cysteine, glutamine, phenylalanine, tryptophan and arginine in T-cell function and cancer? Pathol. Oncol. Res., 2015, 21(1), 9-17.
[http://dx.doi.org/10.1007/s12253-014-9860-0] [PMID: 25351939]
[21]
Scholtes, M.P.; de Jong, F.C.; Zuiverloon, T.C.M.; Theodorescu, D. Role of bladder cancer metabolic reprogramming in the effectiveness of immunotherapy. Cancers (Basel), 2021, 13(2), 288.
[http://dx.doi.org/10.3390/cancers13020288] [PMID: 33466735]
[22]
Roy, D.G.; Kaymak, I.; Williams, K.S.; Ma, E.H.; Jones, R.G. Immunometabolism in the tumor microenvironment. Annu. Rev. Cancer Biol., 2021, 5, 137-159.
[http://dx.doi.org/10.1146/annurev-cancerbio-030518-055817]
[23]
Marchiq, I.; Pouysségur, J. Hypoxia, cancer metabolism and the therapeutic benefit of targeting lactate/H(+) symporters. J. Mol. Med. (Berl.), 2016, 94(2), 155-171.
[http://dx.doi.org/10.1007/s00109-015-1307-x] [PMID: 26099350]
[24]
Gallo, M.; Sapio, L.; Spina, A.; Naviglio, D.; Calogero, A.; Naviglio, S. Lactic dehydrogenase and cancer: an overview. Front. Biosci., 2015, 20, 1234-1249.
[http://dx.doi.org/10.2741/4368] [PMID: 25961554]
[25]
van de Putte, E.E.F.; Vegt, E.; Mertens, L.S.; Bruining, A.; Hendricksen, K.; van der Heijden, M.S.; Horenblas, S.; van Rhijn, B.W.G. FDG-PET/CT for response evaluation of invasive bladder cancer following neoadjuvant chemotherapy. Int. Urol. Nephrol., 2017, 49(9), 1585-1591.
[http://dx.doi.org/10.1007/s11255-017-1637-4] [PMID: 28674853]
[26]
Yin, Z.; Bai, L.; Li, W.; Zeng, T.; Tian, H.; Cui, J. Targeting T cell metabolism in the tumor microenvironment: an anti-cancer therapeutic strategy. J. Exp. Clin. Cancer Res., 2019, 38(1), 403.
[http://dx.doi.org/10.1186/s13046-019-1409-3] [PMID: 31519198]
[27]
Gatenby, R.A.; Gillies, R.J. Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer, 2004, 4(11), 891-899.
[http://dx.doi.org/10.1038/nrc1478] [PMID: 15516961]
[28]
Pavlova, N.N.; Thompson, C.B. The emerging hallmarks of cancer metabolism. Cell Metab., 2016, 23(1), 27-47.
[http://dx.doi.org/10.1016/j.cmet.2015.12.006] [PMID: 26771115]
[29]
Danhier, P.; Bański, P.; Payen, V.L.; Grasso, D.; Ippolito, L.; Sonveaux, P.; Porporato, P.E. Cancer metabolism in space and time: Beyond the Warburg effect. Biochim. Biophys. Acta Bioenerg., 2017, 1858(8), 556-572.
[http://dx.doi.org/10.1016/j.bbabio.2017.02.001] [PMID: 28167100]
[30]
San-Millán, I.; Brooks, G.A. Reexamining cancer metabolism: lactate production for carcinogenesis could be the purpose and explanation of the Warburg effect. Carcinogenesis, 2017, 38(2), 119-133.
[PMID: 27993896]
[31]
Hurst, C.D.; Alder, O.; Platt, F.M.; Droop, A.; Stead, L.F.; Burns, J.E.; Burghel, G.J.; Jain, S.; Klimczak, L.J.; Lindsay, H.; Roulson, J.A.; Taylor, C.F.; Thygesen, H.; Cameron, A.J.; Ridley, A.J.; Mott, H.R.; Gordenin, D.A.; Knowles, M.A. Genomic subtypes of non-invasive bladder cancer with distinct metabolic profile and female gender bias in KDM6A mutation frequency. Cancer Cell, 2017, 32(5), 701-715.e7.
[http://dx.doi.org/10.1016/j.ccell.2017.08.005] [PMID: 29136510]
[32]
Rochel, N.; Krucker, C.; Coutos-Thévenot, L.; Osz, J.; Zhang, R.; Guyon, E.; Zita, W.; Vanthong, S.; Hernandez, O.A.; Bourguet, M.; Badawy, K.A.; Dufour, F.; Peluso-Iltis, C.; Heckler-Beji, S.; Dejaegere, A.; Kamoun, A.; de Reyniès, A.; Neuzillet, Y.; Rebouissou, S.; Béraud, C.; Lang, H.; Massfelder, T.; Allory, Y.; Cianférani, S.; Stote, R.H.; Radvanyi, F.; Bernard-Pierrot, I. Recurrent activating mutations of PPARγ associated with luminal bladder tumors. Nat. Commun., 2019, 10(1), 253.
[http://dx.doi.org/10.1038/s41467-018-08157-y] [PMID: 30651555]
[33]
Choi, J.W.; Kim, Y.; Lee, J.H.; Kim, Y.S. Prognostic significance of lactate/proton symporters MCT1, MCT4, and their chaperone CD147 expressions in urothelial carcinoma of the bladder. Urology, 2014, 84(1), 245.e9-245.e15.
[http://dx.doi.org/10.1016/j.urology.2014.03.031] [PMID: 24857275]
[34]
Todenhöfer, T.; Seiler, R.; Stewart, C.; Moskalev, I.; Gao, J.; Ladhar, S.; Kamjabi, A.; Al Nakouzi, N.; Hayashi, T.; Choi, S.; Wang, Y.; Frees, S.; Daugaard, M.; Oo, H.Z.; Fisel, P.; Schwab, M.; Schaeffeler, E.; Douglas, J.; Hennenlotter, J.; Bedke, J.; Gibb, E.A.; Fazli, L.; Stenzl, A.; Black, P.C. Selective inhibition of the lactate transporter MCT4 reduces growth of invasive bladder cancer. Mol. Cancer Ther., 2018, 17(12), 2746-2755.
[http://dx.doi.org/10.1158/1535-7163.MCT-18-0107] [PMID: 30262589]
[35]
Angelin, A.; Gil-de-Gómez, L.; Dahiya, S.; Jiao, J.; Guo, L.; Levine, M.H.; Wang, Z.; Quinn, W.J., III; Kopinski, P.K.; Wang, L.; Akimova, T.; Liu, Y.; Bhatti, T.R.; Han, R.; Laskin, B.L.; Baur, J.A.; Blair, I.A.; Wallace, D.C.; Hancock, W.W.; Beier, U.H. Foxp3 reprograms T cell metabolism to function in low-glucose, high-lactate environments. Cell Metab., 2017, 25(6), 1282-1293.e7.
[http://dx.doi.org/10.1016/j.cmet.2016.12.018] [PMID: 28416194]
[36]
Kouidhi, S.; Ben Ayed, F.; Benammar Elgaaied, A. Targeting tumor metabolism: A new challenge to improve immunotherapy. Front. Immunol., 2018, 9, 353.
[http://dx.doi.org/10.3389/fimmu.2018.00353] [PMID: 29527212]
[37]
Koltai, T. Cancer: fundamentals behind pH targeting and the double-edged approach. OncoTargets Ther., 2016, 9, 6343-6360.
[http://dx.doi.org/10.2147/OTT.S115438] [PMID: 27799782]
[38]
Brown, T.P.; Ganapathy, V. Lactate/GPR81 signaling and proton motive force in cancer: Role in angiogenesis, immune escape, nutrition, and Warburg phenomenon. Pharmacol. Ther., 2020, 206, 107451.
[http://dx.doi.org/10.1016/j.pharmthera.2019.107451] [PMID: 31836453]
[39]
DeBerardinis, R.J.; Chandel, N.S. We need to talk about the Warburg effect. Nat. Metab., 2020, 2(2), 127-129.
[http://dx.doi.org/10.1038/s42255-020-0172-2] [PMID: 32694689]
[40]
Romero-Garcia, S.; Moreno-Altamirano, M.M.; Prado-Garcia, H.; Sánchez-García, F.J. Lactate contribution to the tumor microenvironment: mechanisms, effects on immune cells and therapeutic relevance. Front. Immunol., 2016, 7, 52.
[http://dx.doi.org/10.3389/fimmu.2016.00052] [PMID: 26909082]
[41]
Zhang, X.K.; Zhang, Z.L.; Lu, X.; Yang, P.; Cai, M.Y.; Hu, W.M.; Yun, J.P.; Zhou, F.J.; Qian, C.N.; Cao, Y. Prognostic significance of preoperative serum lactate dehydrogenase in upper urinary tract urothelial carcinoma. Clin. Genitourin. Cancer, 2016, 14(4), 341-345.e3.
[http://dx.doi.org/10.1016/j.clgc.2016.01.003] [PMID: 26868330]
[42]
Sahu, D.; Lotan, Y.; Wittmann, B.; Neri, B.; Hansel, D.E. Metabolomics analysis reveals distinct profiles of nonmuscle-invasive and muscle-invasive bladder cancer. Cancer Med., 2017, 6(9), 2106-2120.
[http://dx.doi.org/10.1002/cam4.1109] [PMID: 28766915]
[43]
O’Neill, L.A.; Kishton, R.J.; Rathmell, J. A guide to immunometabolism for immunologists. Nat. Rev. Immunol., 2016, 16(9), 553-565.
[http://dx.doi.org/10.1038/nri.2016.70] [PMID: 27396447]
[44]
Scagliola, A.; Mainini, F.; Cardaci, S. The tricarboxylic acid cycle at the crossroad between cancer and immunity. Antioxid. Redox Signal., 2020, 32(12), 834-852.
[http://dx.doi.org/10.1089/ars.2019.7974] [PMID: 31847530]
[45]
Anderson, N.M.; Mucka, P.; Kern, J.G.; Feng, H. The emerging role and targetability of the TCA cycle in cancer metabolism. Protein Cell, 2018, 9(2), 216-237.
[http://dx.doi.org/10.1007/s13238-017-0451-1] [PMID: 28748451]
[46]
Patra, K.C.; Hay, N. The pentose phosphate pathway and cancer. Trends Biochem. Sci., 2014, 39(8), 347-354.
[http://dx.doi.org/10.1016/j.tibs.2014.06.005] [PMID: 25037503]
[47]
Massari, F.; Ciccarese, C.; Santoni, M.; Iacovelli, R.; Mazzucchelli, R.; Piva, F.; Scarpelli, M.; Berardi, R.; Tortora, G.; Lopez-Beltran, A.; Cheng, L.; Montironi, R. Metabolic phenotype of bladder cancer. Cancer Treat. Rev., 2016, 45, 46-57.
[http://dx.doi.org/10.1016/j.ctrv.2016.03.005] [PMID: 26975021]
[48]
Jiang, L.; Fang, X.; Wang, H.; Li, D.; Wang, X. Ovarian cancer-intrinsic fatty acid synthase prevents anti-tumor immunity by disrupting tumor-infiltrating dendritic cells. Front. Immunol., 2018, 9, 2927.
[http://dx.doi.org/10.3389/fimmu.2018.02927] [PMID: 30619288]
[49]
Kuo, C.Y.; Ann, D.K. When fats commit crimes: fatty acid metabolism, cancer stemness and therapeutic resistance. Cancer Commun., 2018, 38(1), 47.
[http://dx.doi.org/10.1186/s40880-018-0317-9] [PMID: 29996946]
[50]
Jiang, B.; Li, E.H.; Lu, Y.Y.; Jiang, Q.; Cui, D.; Jing, Y.F.; Xia, S.J. Inhibition of fatty-acid synthase suppresses P-AKT and induces apoptosis in bladder cancer. Urology, 2012, 80(2), 484.e9-484.e15.
[http://dx.doi.org/10.1016/j.urology.2012.02.046] [PMID: 22554590]
[51]
Visca, P.; Sebastiani, V.; Pizer, E.S.; Botti, C.; De Carli, P.; Filippi, S.; Monaco, S.; Alo, P.L. Immunohistochemical expression and prognostic significance of FAS and GLUT1 in bladder carcinoma. Anticancer Res., 2003, 23(1A), 335-339.
[PMID: 12680233]
[52]
Sugino, T.; Baba, K.; Hoshi, N.; Aikawa, K.; Yamaguchi, O.; Suzuki, T. Overexpression of fatty acid synthase in human urinary bladder cancer and combined expression of the synthase and Ki-67 as a predictor of prognosis of cancer patients. Med. Mol. Morphol., 2011, 44(3), 146-150.
[http://dx.doi.org/10.1007/s00795-010-0517-0] [PMID: 21922386]
[53]
Gao, P.; Tchernyshyov, I.; Chang, T.C.; Lee, Y.S.; Kita, K.; Ochi, T.; Zeller, K.I.; De Marzo, A.M.; Van Eyk, J.E.; Mendell, J.T.; Dang, C.V. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature, 2009, 458(7239), 762-765.
[http://dx.doi.org/10.1038/nature07823] [PMID: 19219026]
[54]
Wise, D.R.; DeBerardinis, R.J.; Mancuso, A.; Sayed, N.; Zhang, X.Y.; Pfeiffer, H.K.; Nissim, I.; Daikhin, E.; Yudkoff, M.; McMahon, S.B.; Thompson, C.B. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. USA, 2008, 105(48), 18782-18787.
[http://dx.doi.org/10.1073/pnas.0810199105] [PMID: 19033189]
[55]
Wang, L.; Yang, X.; Li, D.; Liang, Z.; Chen, Y.; Ma, G.; Wang, Y.; Li, Y.; Liang, Y.; Niu, H. The elevated glutaminolysis of bladder cancer and T cells in a simulated tumor microenvironment contributes to the up-regulation of PD-L1 expression by interferon-γ. OncoTargets Ther., 2018, 11, 7229-7243.
[http://dx.doi.org/10.2147/OTT.S180505] [PMID: 30425515]
[56]
Li, H.J.; Li, X.; Pang, H.; Pan, J.J.; Xie, X.J.; Chen, W. Long non-coding RNA UCA1 promotes glutamine metabolism by targeting miR-16 in human bladder cancer. Jpn. J. Clin. Oncol., 2015, 45(11), 1055-1063.
[http://dx.doi.org/10.1093/jjco/hyv132] [PMID: 26373319]
[57]
Wu, H.; Gong, J.; Liu, Y. Indoleamine 2, 3-dioxygenase regulation of immune response. (Review). Mol. Med. Rep., 2018, 17(4), 4867-4873.
[http://dx.doi.org/10.3892/mmr.2018.8537] [PMID: 29393500]
[58]
Zhang, W.; Zhang, J.; Zhang, Z.; Guo, Y.; Wu, Y.; Wang, R.; Wang, L.; Mao, S.; Yao, X. Overexpression of Indoleamine 2,3-Dioxygenase 1 Promotes epithelial-mesenchymal transition by activation of the IL-6/STAT3/PD-L1 pathway in bladder cancer. Transl. Oncol., 2019, 12(3), 485-492.
[http://dx.doi.org/10.1016/j.tranon.2018.11.012] [PMID: 30594037]
[59]
Bader, J.E.; Voss, K.; Rathmell, J.C. Targeting metabolism to improve the tumor microenvironment for cancer immunotherapy. Mol. Cell, 2020, 78(6), 1019-1033.
[http://dx.doi.org/10.1016/j.molcel.2020.05.034] [PMID: 32559423]
[60]
Yen, M.C.; Lin, C.C.; Chen, Y.L.; Huang, S.S.; Yang, H.J.; Chang, C.P.; Lei, H.Y.; Lai, M.D. A novel cancer therapy by skin delivery of indoleamine 2,3-dioxygenase siRNA. Clin. Cancer Res., 2009, 15(2), 641-649.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1988] [PMID: 19147770]
[61]
Bessede, A.; Gargaro, M.; Pallotta, M.T.; Matino, D.; Servillo, G.; Brunacci, C.; Bicciato, S.; Mazza, E.M.; Macchiarulo, A.; Vacca, C.; Iannitti, R.; Tissi, L.; Volpi, C.; Belladonna, M.L.; Orabona, C.; Bianchi, R.; Lanz, T.V.; Platten, M.; Della Fazia, M.A.; Piobbico, D.; Zelante, T.; Funakoshi, H.; Nakamura, T.; Gilot, D.; Denison, M.S.; Guillemin, G.J.; DuHadaway, J.B.; Prendergast, G.C.; Metz, R.; Geffard, M.; Boon, L.; Pirro, M.; Iorio, A.; Veyret, B.; Romani, L.; Grohmann, U.; Fallarino, F.; Puccetti, P. Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature, 2014, 511(7508), 184-190.
[http://dx.doi.org/10.1038/nature13323] [PMID: 24930766]
[62]
Platten, M.; Nollen, E.A.A.; Röhrig, U.F.; Fallarino, F.; Opitz, C.A. Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond. Nat. Rev. Drug Discov., 2019, 18(5), 379-401.
[http://dx.doi.org/10.1038/s41573-019-0016-5] [PMID: 30760888]
[63]
Lee, S.H.; Mahendran, R.; Tham, S.M.; Thamboo, T.P.; Chionh, B.J.; Lim, Y.X.; Tsang, W.C.; Wu, Q.H.; Chia, J.Y.; Tay, M.H.W.; Goh, B.Y.S.; Chen, K.W.; Mallari, J.Z.; Periaswami, R.; Raman, L.; Choo, S.N.; Kioh, D.Y.Q.; Chiong, E.; Esuvaranathan, K.; Chan, E.C.Y. Tryptophan-kynurenine ratio as a biomarker of bladder cancer. BJU Int., 2021, 127(4), 445-453.
[http://dx.doi.org/10.1111/bju.15205] [PMID: 32794357]
[64]
Allard, B.; Turcotte, M.; Stagg, J. CD73-generated adenosine: orchestrating the tumor-stroma interplay to promote cancer growth. J. Biomed. Biotechnol., 2012, 2012, 485156.
[http://dx.doi.org/10.1155/2012/485156] [PMID: 23125525]
[65]
Chambers, A.M.; Matosevic, S. Immunometabolic dysfunction of natural killer cells mediated by the Hypoxia-CD73 axis in solid tumors. Front. Mol. Biosci., 2019, 6, 60.
[http://dx.doi.org/10.3389/fmolb.2019.00060] [PMID: 31396523]
[66]
Ghiringhelli, F.; Bruchard, M.; Chalmin, F.; Rébé, C. Production of adenosine by ectonucleotidases: a key factor in tumor immunoescape. J. Biomed. Biotechnol., 2012, 2012, 473712.
[http://dx.doi.org/10.1155/2012/473712] [PMID: 23133312]
[67]
Allard, B.; Pommey, S.; Smyth, M.J.; Stagg, J. Targeting CD73 enhances the antitumor activity of anti-PD-1 and anti-CTLA-4 mAbs. Clin. Cancer Res., 2013, 19(20), 5626-5635.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-0545] [PMID: 23983257]
[68]
Giannone, G.; Ghisoni, E.; Genta, S.; Scotto, G.; Tuninetti, V.; Turinetto, M.; Valabrega, G. Immuno-metabolism and microenvironment in cancer: key players for immunotherapy. Int. J. Mol. Sci., 2020, 21(12), 4414.
[http://dx.doi.org/10.3390/ijms21124414] [PMID: 32575899]
[69]
Young, A.; Mittal, D.; Stagg, J.; Smyth, M.J. Targeting cancer-derived adenosine: new therapeutic approaches. Cancer Discov., 2014, 4(8), 879-888.
[http://dx.doi.org/10.1158/2159-8290.CD-14-0341] [PMID: 25035124]
[70]
Wu, J.; Abraham, S.N. The roles of T cells in bladder pathologies. Trends Immunol., 2021, 42(3), 248-260.
[http://dx.doi.org/10.1016/j.it.2021.01.003] [PMID: 33536141]
[71]
Beier, U.H.; Angelin, A.; Akimova, T.; Wang, L.; Liu, Y.; Xiao, H.; Koike, M.A.; Hancock, S.A.; Bhatti, T.R.; Han, R.; Jiao, J.; Veasey, S.C.; Sims, C.A.; Baur, J.A.; Wallace, D.C.; Hancock, W.W. Essential role of mitochondrial energy metabolism in Foxp3⁺ T-regulatory cell function and allograft survival. FASEB J., 2015, 29(6), 2315-2326.
[http://dx.doi.org/10.1096/fj.14-268409] [PMID: 25681462]
[72]
Gerriets, V.A.; Kishton, R.J.; Nichols, A.G.; Macintyre, A.N.; Inoue, M.; Ilkayeva, O.; Winter, P.S.; Liu, X.; Priyadharshini, B.; Slawinska, M.E.J.T.J.i.; Haeberli, L.; Huck, C.; Turka, L.A.; Wood, K.C.; Hale, L.P.; Smith, P.A.; Schneider, M.A.; MacIver, N.J.; Locasale, J.W.; Newgard, C.B.; Shinohara, M.L.; Rathmell, J.C. Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. J. Clin. Invest., 2015, 125(1), 194-207.
[http://dx.doi.org/10.1172/JCI76012] [PMID: 25437876]
[73]
Michalek, R.D.; Gerriets, V.A.; Jacobs, S.R.; Macintyre, A.N.; MacIver, N.J.; Mason, E.F.; Sullivan, S.A.; Nichols, A.G.; Rathmell, J.C. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol., 2011, 186(6), 3299-3303.
[http://dx.doi.org/10.4049/jimmunol.1003613] [PMID: 21317389]
[74]
Olenchock, B.A.; Rathmell, J.C.; Vander Heiden, M.G. Biochemical underpinnings of Immune cell metabolic phenotypes. Immunity, 2017, 46(5), 703-713.
[http://dx.doi.org/10.1016/j.immuni.2017.04.013] [PMID: 28514672]
[75]
Wang, R.; Dillon, C.P.; Shi, L.Z.; Milasta, S.; Carter, R.; Finkelstein, D.; McCormick, L.L.; Fitzgerald, P.; Chi, H.; Munger, J.; Green, D.R. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity, 2011, 35(6), 871-882.
[http://dx.doi.org/10.1016/j.immuni.2011.09.021] [PMID: 22195744]
[76]
van der Windt, G.J.; Everts, B.; Chang, C.H.; Curtis, J.D.; Freitas, T.C.; Amiel, E.; Pearce, E.J.; Pearce, E.L. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity, 2012, 36(1), 68-78.
[http://dx.doi.org/10.1016/j.immuni.2011.12.007] [PMID: 22206904]
[77]
Ho, P-C.; Liu, P.S. Metabolic communication in tumors: a new layer of immunoregulation for immune evasion. J. Immunother. Cancer, 2016, 4(1), 4.
[http://dx.doi.org/10.1186/s40425-016-0109-1] [PMID: 26885366]
[78]
Wawman, R.E.; Bartlett, H.; Oo, Y.H.; Regulatory, T. Regulatory T cell metabolism in the hepatic microenvironment. Front. Immunol., 2018, 8, 1889.
[http://dx.doi.org/10.3389/fimmu.2017.01889] [PMID: 29358934]
[79]
Gerriets, V.A.; Kishton, R.J.; Johnson, M.O.; Cohen, S.; Siska, P.J.; Nichols, A.G.; Warmoes, M.O.; de Cubas, A.A.; MacIver, N.J.; Locasale, J.W.; Turka, L.A.; Wells, A.D.; Rathmell, J.C. Foxp3 and Toll-like receptor signaling balance Treg cell anabolic metabolism for suppression. Nat. Immunol., 2016, 17(12), 1459-1466.
[http://dx.doi.org/10.1038/ni.3577] [PMID: 27695003]
[80]
Kempkes, R.W.M.; Joosten, I.; Koenen, H.J.P.M.; He, X. Metabolic pathways involved in Regulatory T cell functionality. Front. Immunol., 2019, 10, 2839.
[http://dx.doi.org/10.3389/fimmu.2019.02839] [PMID: 31849995]
[81]
Weinberg, S.E.; Singer, B.D.; Steinert, E.M.; Martinez, C.A.; Mehta, M.M.; Martínez-Reyes, I.; Gao, P.; Helmin, K.A.; Abdala-Valencia, H.; Sena, L.A.; Schumacker, P.T.; Turka, L.A.; Chandel, N.S. Mitochondrial complex III is essential for suppressive function of regulatory T cells. Nature, 2019, 565(7740), 495-499.
[http://dx.doi.org/10.1038/s41586-018-0846-z] [PMID: 30626970]
[82]
Brand, A.; Singer, K.; Koehl, G.E.; Kolitzus, M.; Schoenhammer, G.; Thiel, A.; Matos, C.; Bruss, C.; Klobuch, S.; Peter, K.; Kastenberger, M.; Bogdan, C.; Schleicher, U.; Mackensen, A.; Ullrich, E.; Fichtner-Feigl, S.; Kesselring, R.; Mack, M.; Ritter, U.; Schmid, M.; Blank, C.; Dettmer, K.; Oefner, P.J.; Hoffmann, P.; Walenta, S.; Geissler, E.K.; Pouyssegur, J.; Villunger, A.; Steven, A.; Seliger, B.; Schreml, S.; Haferkamp, S.; Kohl, E.; Karrer, S.; Berneburg, M.; Herr, W.; Mueller-Klieser, W.; Renner, K.; Kreutz, M. LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells. Cell Metab., 2016, 24(5), 657-671.
[http://dx.doi.org/10.1016/j.cmet.2016.08.011] [PMID: 27641098]
[83]
Phan, A.T.; Goldrath, A.W.; Glass, C.K. Metabolic and epigenetic coordination of T cell and macrophage immunity. Immunity, 2017, 46(5), 714-729.
[http://dx.doi.org/10.1016/j.immuni.2017.04.016] [PMID: 28514673]
[84]
Michalek, R.D.; Rathmell, J.C. The metabolic life and times of a T-cell. Immunol. Rev., 2010, 236(1), 190-202.
[http://dx.doi.org/10.1111/j.1600-065X.2010.00911.x] [PMID: 20636818]
[85]
Lau, A.N.; Vander Heiden, M.G. Metabolism in the tumor microenvironment. Annu. Rev. Cancer Biol., 2020, 4, 17-40.
[http://dx.doi.org/10.1146/annurev-cancerbio-030419-033333]
[86]
Voss, K.; Luthers, C.R.; Pohida, K.; Snow, A.L. Fatty acid synthase contributes to restimulation-induced cell death of human CD4 T cells. Front. Mol. Biosci., 2019, 6, 106.
[http://dx.doi.org/10.3389/fmolb.2019.00106] [PMID: 31681794]
[87]
Sinclair, L.V.; Rolf, J.; Emslie, E.; Shi, Y.B.; Taylor, P.M.; Cantrell, D.A. Control of amino-acid transport by antigen receptors coordinates the metabolic reprogramming essential for T cell differentiation. Nat. Immunol., 2013, 14(5), 500-508.
[http://dx.doi.org/10.1038/ni.2556] [PMID: 23525088]
[88]
Geiger, R.; Rieckmann, J.C.; Wolf, T.; Basso, C.; Feng, Y.; Fuhrer, T.; Kogadeeva, M.; Picotti, P.; Meissner, F.; Mann, M.; Zamboni, N.; Sallusto, F.; Lanzavecchia, A. L-Arginine modulates T cell metabolism and enhances survival and anti-tumor activity. Cell, 2016, 167(3), 829-842.e13.
[http://dx.doi.org/10.1016/j.cell.2016.09.031] [PMID: 27745970]
[89]
Nakaya, M.; Xiao, Y.; Zhou, X.; Chang, J.H.; Chang, M.; Cheng, X.; Blonska, M.; Lin, X.; Sun, S.C. Inflammatory T cell responses rely on amino acid transporter ASCT2 facilitation of glutamine uptake and mTORC1 kinase activation. Immunity, 2014, 40(5), 692-705.
[http://dx.doi.org/10.1016/j.immuni.2014.04.007] [PMID: 24792914]
[90]
Munn, D.H.; Sharma, M.D.; Baban, B.; Harding, H.P.; Zhang, Y.; Ron, D.; Mellor, A.L. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity, 2005, 22(5), 633-642.
[http://dx.doi.org/10.1016/j.immuni.2005.03.013] [PMID: 15894280]
[91]
Bengsch, B.; Johnson, A.L.; Kurachi, M.; Odorizzi, P.M.; Pauken, K.E.; Attanasio, J.; Stelekati, E.; McLane, L.M.; Paley, M.A.; Delgoffe, G.M.; Wherry, E.J. Bioenergetic insufficiencies due to metabolic alterations regulated by the inhibitory receptor PD-1 are an early driver of CD8(+) T cell exhaustion. Immunity, 2016, 45(2), 358-373.
[http://dx.doi.org/10.1016/j.immuni.2016.07.008] [PMID: 27496729]
[92]
Siska, P.J.; van der Windt, G.J.; Kishton, R.J.; Cohen, S.; Eisner, W.; MacIver, N.J.; Kater, A.P.; Weinberg, J.B.; Rathmell, J.C. Suppression of Glut1 and glucose metabolism by decreased Akt/mTORC1 signaling drives T cell impairment in B cell leukemia. J. Immunol., 2016, 197(6), 2532-2540.
[http://dx.doi.org/10.4049/jimmunol.1502464] [PMID: 27511728]
[93]
Patsoukis, N.; Weaver, J.D.; Strauss, L.; Herbel, C.; Seth, P.; Boussiotis, V.A. Immunometabolic regulations mediated by coinhibitory receptors and their impact on T cell immune responses. Front. Immunol., 2017, 8, 330.
[http://dx.doi.org/10.3389/fimmu.2017.00330] [PMID: 28443090]
[94]
Guerra, L.; Bonetti, L.; Brenner, D. Metabolic modulation of immunity: a new concept in cancer immunotherapy. Cell Rep., 2020, 32(1), 107848.
[http://dx.doi.org/10.1016/j.celrep.2020.107848] [PMID: 32640218]
[95]
Kamphorst, A.O.; Wieland, A.; Nasti, T.; Yang, S.; Zhang, R.; Barber, D.L.; Konieczny, B.T.; Daugherty, C.Z.; Koenig, L.; Yu, K.; Sica, G.L.; Sharpe, A.H.; Freeman, G.J.; Blazar, B.R.; Turka, L.A.; Owonikoko, T.K.; Pillai, R.N.; Ramalingam, S.S.; Araki, K.; Ahmed, R. Rescue of exhausted CD8 T cells by PD-1-targeted therapies is CD28-dependent. Science, 2017, 355(6332), 1423-1427.
[http://dx.doi.org/10.1126/science.aaf0683] [PMID: 28280249]
[96]
Song, D.; Powles, T.; Shi, L.; Zhang, L.; Ingersoll, M.A.; Lu, Y.J. Bladder cancer, a unique model to understand cancer immunity and develop immunotherapy approaches. J. Pathol., 2019, 249(2), 151-165.
[http://dx.doi.org/10.1002/path.5306] [PMID: 31102277]
[97]
Weng, C.Y.; Kao, C.X.; Chang, T.S.; Huang, Y.H. Immuno-metabolism: the role of cancer niche in immune checkpoint inhibitor resistance. Int. J. Mol. Sci., 2021, 22(3), 1258.
[http://dx.doi.org/10.3390/ijms22031258] [PMID: 33514004]
[98]
Cuyàs, E.; Verdura, S.; Martin-Castillo, B.; Alarcón, T.; Lupu, R.; Bosch-Barrera, J.; Menendez, J.A. Tumor cell-intrinsic immunometabolism and precision nutrition in cancer immunotherapy. Cancers (Basel), 2020, 12(7), 1757.
[http://dx.doi.org/10.3390/cancers12071757] [PMID: 32630618]
[99]
Ou, Z.; Wang, Y.; Liu, L.; Li, L.; Yeh, S.; Qi, L.; Chang, C. Tumor microenvironment B cells increase bladder cancer metastasis via modulation of the IL-8/androgen receptor (AR)/MMPs signals. Oncotarget, 2015, 6(28), 26065-26078.
[http://dx.doi.org/10.18632/oncotarget.4569] [PMID: 26305549]
[100]
Zirakzadeh, A.A.; Sherif, A.; Rosenblatt, R.; Ahlén Bergman, E.; Winerdal, M.; Yang, D.; Cederwall, J.; Jakobsson, V.; Hyllienmark, M.; Winqvist, O.; Marits, P. Tumour-associated B cells in urothelial urinary bladder cancer. Scand. J. Immunol., 2020, 91(2), e12830.
[http://dx.doi.org/10.1111/sji.12830] [PMID: 31823416]
[101]
Franchina, D.G.; Grusdat, M.; Brenner, D. B-Cell metabolic remodeling and cancer. Trends Cancer, 2018, 4(2), 138-150.
[http://dx.doi.org/10.1016/j.trecan.2017.12.006] [PMID: 29458963]
[102]
Kojima, H.; Gu, H.; Nomura, S.; Caldwell, C.C.; Kobata, T.; Carmeliet, P.; Semenza, G.L.; Sitkovsky, M.V. Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1alpha -deficient chimeric mice. Proc. Natl. Acad. Sci. USA, 2002, 99(4), 2170-2174.
[http://dx.doi.org/10.1073/pnas.052706699] [PMID: 11854513]
[103]
Kojima, H.; Kobayashi, A.; Sakurai, D.; Kanno, Y.; Hase, H.; Takahashi, R.; Totsuka, Y.; Semenza, G.L.; Sitkovsky, M.V.; Kobata, T. Differentiation stage-specific requirement in hypoxia-inducible factor-1alpha-regulated glycolytic pathway during murine B cell development in bone marrow. J. Immunol., 2010, 184(1), 154-163.
[http://dx.doi.org/10.4049/jimmunol.0800167] [PMID: 19949104]
[104]
Chan, L.N.; Chen, Z.; Braas, D.; Lee, J.W.; Xiao, G.; Geng, H.; Cosgun, K.N.; Hurtz, C.; Shojaee, S.; Cazzaniga, V.; Schjerven, H.; Ernst, T.; Hochhaus, A.; Kornblau, S.M.; Konopleva, M.; Pufall, M.A.; Cazzaniga, G.; Liu, G.J.; Milne, T.A.; Koeffler, H.P.; Ross, T.S.; Sánchez-García, I.; Borkhardt, A.; Yamamoto, K.R.; Dickins, R.A.; Graeber, T.G.; Müschen, M. Metabolic gatekeeper function of B-lymphoid transcription factors. Nature, 2017, 542(7642), 479-483.
[http://dx.doi.org/10.1038/nature21076] [PMID: 28192788]
[105]
Caro-Maldonado, A.; Wang, R.; Nichols, A.G.; Kuraoka, M.; Milasta, S.; Sun, L.D.; Gavin, A.L.; Abel, E.D.; Kelsoe, G.; Green, D.R.; Rathmell, J.C. Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J. Immunol., 2014, 192(8), 3626-3636.
[http://dx.doi.org/10.4049/jimmunol.1302062] [PMID: 24616478]
[106]
Allman, D.; Pillai, S. Peripheral B cell subsets. Curr. Opin. Immunol., 2008, 20(2), 149-157.
[http://dx.doi.org/10.1016/j.coi.2008.03.014] [PMID: 18434123]
[107]
Wilson, C.S.; Moore, D.J. B cell metabolism: an understudied opportunity to improve immune therapy in autoimmune type 1 diabetes. Immunometabolism, 2020, 2(2), e200016.
[108]
Farmer, J.R.; Allard-Chamard, H.; Sun, N.; Ahmad, M.; Bertocchi, A.; Mahajan, V.S.; Aicher, T.; Arnold, J.; Benson, M.D.; Morningstar, J.; Barmettler, S.; Yuen, G.; Murphy, S.J.H.; Walter, J.E.; Ghebremichael, M.; Shalek, A.K.; Batista, F.; Gerszten, R.; Pillai, S. Induction of metabolic quiescence defines the transitional to follicular B cell switch. Sci. Signal., 2019, 12(604), eaaw5573.
[http://dx.doi.org/10.1126/scisignal.aaw5573] [PMID: 31641080]
[109]
Pillai, S.; Cariappa, A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol., 2009, 9(11), 767-777.
[http://dx.doi.org/10.1038/nri2656] [PMID: 19855403]
[110]
Sintes, J.; Gentile, M.; Zhang, S.; Garcia-Carmona, Y.; Magri, G.; Cassis, L.; Segura-Garzón, D.; Ciociola, A.; Grasset, E.K.; Bascones, S.; Comerma, L.; Pybus, M.; Lligé, D.; Puga, I.; Gutzeit, C.; He, B.; DuBois, W.; Crespo, M.; Pascual, J.; Mensa, A.; Aróstegui, J.I.; Juan, M.; Yagüe, J.; Serrano, S.; Lloreta, J.; Meffre, E.; Hahne, M.; Cunningham-Rundles, C.; Mock, B.A.; Cerutti, A. mTOR intersects antibody-inducing signals from TACI in marginal zone B cells. Nat. Commun., 2017, 8(1), 1462.
[http://dx.doi.org/10.1038/s41467-017-01602-4] [PMID: 29133782]
[111]
Jellusova, J.; Cato, M.H.; Apgar, J.R.; Ramezani-Rad, P.; Leung, C.R.; Chen, C.; Richardson, A.D.; Conner, E.M.; Benschop, R.J.; Woodgett, J.R.; Rickert, R.C. Gsk3 is a metabolic checkpoint regulator in B cells. Nat. Immunol., 2017, 18(3), 303-312.
[http://dx.doi.org/10.1038/ni.3664] [PMID: 28114292]
[112]
Shah, A.M.; Wang, Z.; Ma, J. Glutamine metabolism and its role in immunity, a Comprehensive review. Animals (Basel), 2020, 10(2), 326.
[http://dx.doi.org/10.3390/ani10020326] [PMID: 32092847]
[113]
Navarro, F.; Bacurau, A.V.; Vanzelli, A.; Meneguello-Coutinho, M.; Uchida, M.C.; Moraes, M.R.; Almeida, S.S.; Wasinski, F.; Barros, C.C.; Würtele, M.; Araújo, R.C.; Costa Rosa, L.F.; Bacurau, R.F. Changes in glucose and glutamine lymphocyte metabolisms induced by type I interferon α. Mediators Inflamm., 2010, 2010, 364290.
[http://dx.doi.org/10.1155/2010/364290] [PMID: 21234393]
[114]
van Beek, A.A.; Hugenholtz, F.; Meijer, B.; Sovran, B.; Perdijk, O.; Vermeij, W.P.; Brandt, R.M.; Barnhoorn, S.; Hoeijmakers, J.H.; de Vos, P.; Leenen, P.J.; Hendriks, R.W.; Savelkoul, H.F. Frontline Science: Tryptophan restriction arrests B cell development and enhances microbial diversity in WT and prematurely aging Ercc1-/Δ7 mice. J. Leukoc. Biol., 2017, 101(4), 811-821.
[http://dx.doi.org/10.1189/jlb.1HI0216-062RR] [PMID: 27418353]
[115]
Martínez, V.G.; Rubio, C.; Martínez-Fernández, M.; Segovia, C.; López-Calderón, F.; Garín, M.I.; Teijeira, A.; Munera-Maravilla, E.; Varas, A.; Sacedón, R.; Guerrero, F.; Villacampa, F.; de la Rosa, F.; Castellano, D.; López-Collazo, E.; Paramio, J.M.; Vicente, Á.; Dueñas, M. BMP4 induces M2 macrophage polarization and favors tumor progression in bladder cancer. Clin. Cancer Res., 2017, 23(23), 7388-7399.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-1004] [PMID: 28928159]
[116]
Miyake, M.; Tatsumi, Y.; Gotoh, D.; Ohnishi, S.; Owari, T.; Iida, K.; Ohnishi, K.; Hori, S.; Morizawa, Y.; Itami, Y.; Nakai, Y.; Inoue, T.; Anai, S.; Torimoto, K.; Aoki, K.; Shimada, K.; Konishi, N.; Tanaka, N.; Fujimoto, K.; Regulatory, T. Regulatory T cells and tumor-associated macrophages in the tumor microenvironment in non-muscle invasive bladder cancer treated with intravesical bacille calmette-guérin: a long-term follow-up study of a Japanese cohort. Int. J. Mol. Sci., 2017, 18(10), 2186.
[http://dx.doi.org/10.3390/ijms18102186] [PMID: 29048388]
[117]
Fujimura, T.; Kambayashi, Y.; Fujisawa, Y.; Hidaka, T.; Aiba, S. Tumor-associated macrophages: therapeutic targets for skin Cancer. Front. Oncol., 2018, 8, 3.
[http://dx.doi.org/10.3389/fonc.2018.00003] [PMID: 29410946]
[118]
Casazza, A.; Laoui, D.; Wenes, M.; Rizzolio, S.; Bassani, N.; Mambretti, M.; Deschoemaeker, S.; Van Ginderachter, J.A.; Tamagnone, L.; Mazzone, M. Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity. Cancer Cell, 2013, 24(6), 695-709.
[http://dx.doi.org/10.1016/j.ccr.2013.11.007] [PMID: 24332039]
[119]
Netea-Maier, R.T.; Smit, J.W.A.; Netea, M.G. Metabolic changes in tumor cells and tumor-associated macrophages: A mutual relationship. Cancer Lett., 2018, 413, 102-109.
[http://dx.doi.org/10.1016/j.canlet.2017.10.037] [PMID: 29111350]
[120]
Colegio, O.R.; Chu, N.Q.; Szabo, A.L.; Chu, T.; Rhebergen, A.M.; Jairam, V.; Cyrus, N.; Brokowski, C.E.; Eisenbarth, S.C.; Phillips, G.M.; Cline, G.W.; Phillips, A.J.; Medzhitov, R. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature, 2014, 513(7519), 559-563.
[http://dx.doi.org/10.1038/nature13490] [PMID: 25043024]
[121]
Zhao, Y.; Wang, D.; Xu, T.; Liu, P.; Cao, Y.; Wang, Y.; Yang, X.; Xu, X.; Wang, X.; Niu, H. Bladder cancer cells re-educate TAMs through lactate shuttling in the microfluidic cancer microenvironment. Oncotarget, 2015, 6(36), 39196-39210.
[http://dx.doi.org/10.18632/oncotarget.5538] [PMID: 26474279]
[122]
Zhang, Y.; Sun, Y.; Rao, E.; Yan, F.; Li, Q.; Zhang, Y.; Silverstein, K.A.; Liu, S.; Sauter, E.; Cleary, M.P.; Li, B. Fatty acid-binding protein E-FABP restricts tumor growth by promoting IFN-β responses in tumor-associated macrophages. Cancer Res., 2014, 74(11), 2986-2998.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-2689] [PMID: 24713431]
[123]
Daurkin, I.; Eruslanov, E.; Stoffs, T.; Perrin, G.Q.; Algood, C.; Gilbert, S.M.; Rosser, C.J.; Su, L.M.; Vieweg, J.; Kusmartsev, S. Tumor-associated macrophages mediate immunosuppression in the renal cancer microenvironment by activating the 15-lipoxygenase-2 pathway. Cancer Res., 2011, 71(20), 6400-6409.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-1261] [PMID: 21900394]
[124]
Rath, M.; Müller, I.; Kropf, P.; Closs, E.I.; Munder, M. Metabolism via Arginase or Nitric Oxide Synthase: Two Competing Arginine Pathways in Macrophages. Front. Immunol., 2014, 5, 532.
[http://dx.doi.org/10.3389/fimmu.2014.00532] [PMID: 25386178]
[125]
MacMicking, J.D.; Nathan, C.; Hom, G.; Chartrain, N.; Fletcher, D.S.; Trumbauer, M.; Stevens, K.; Xie, Q.W.; Sokol, K.; Hutchinson, N. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell, 1995, 81(4), 641-650.
[http://dx.doi.org/10.1016/0092-8674(95)90085-3] [PMID: 7538909]
[126]
Liu, Y.; Xu, R.; Gu, H.; Zhang, E.; Qu, J.; Cao, W.; Huang, X.; Yan, H.; He, J.; Cai, Z. Metabolic reprogramming in macrophage responses. Biomark. Res., 2021, 9(1), 1.
[http://dx.doi.org/10.1186/s40364-020-00251-y] [PMID: 33407885]
[127]
Chang, C.I.; Liao, J.C.; Kuo, L. Macrophage arginase promotes tumor cell growth and suppresses nitric oxide-mediated tumor cytotoxicity. Cancer Res., 2001, 61(3), 1100-1106.
[PMID: 11221839]
[128]
Schnoor, M.; Cullen, P.; Lorkowski, J.; Stolle, K.; Robenek, H.; Troyer, D.; Rauterberg, J.; Lorkowski, S. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J. Immunol., 2008, 180(8), 5707-5719.
[http://dx.doi.org/10.4049/jimmunol.180.8.5707] [PMID: 18390756]
[129]
Rodriguez, P.C.; Quiceno, D.G.; Zabaleta, J.; Ortiz, B.; Zea, A.H.; Piazuelo, M.B.; Delgado, A.; Correa, P.; Brayer, J.; Sotomayor, E.M.; Antonia, S.; Ochoa, J.B.; Ochoa, A.C. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res., 2004, 64(16), 5839-5849.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-0465] [PMID: 15313928]
[130]
Choi, J.; Stradmann-Bellinghausen, B.; Yakubov, E.; Savaskan, N.E.; Régnier-Vigouroux, A. Glioblastoma cells induce differential glutamatergic gene expressions in human tumor-associated microglia/macrophages and monocyte-derived macrophages. Cancer Biol. Ther., 2015, 16(8), 1205-1213.
[http://dx.doi.org/10.1080/15384047.2015.1056406] [PMID: 26047211]
[131]
Zhao, Q.; Kuang, D.M.; Wu, Y.; Xiao, X.; Li, X.F.; Li, T.J.; Zheng, L. Activated CD69+ T cells foster immune privilege by regulating IDO expression in tumor-associated macrophages. J. Immunol., 2012, 188(3), 1117-1124.
[http://dx.doi.org/10.4049/jimmunol.1100164] [PMID: 22184722]
[132]
Halbrook, C.J.; Pontious, C.; Kovalenko, I.; Lapienyte, L.; Dreyer, S.; Lee, H.J.; Thurston, G.; Zhang, Y.; Lazarus, J.; Sajjakulnukit, P.; Hong, H.S.; Kremer, D.M.; Nelson, B.S.; Kemp, S.; Zhang, L.; Chang, D.; Biankin, A.; Shi, J.; Frankel, T.L.; Crawford, H.C.; Morton, J.P.; Pasca di Magliano, M.; Lyssiotis, C.A. Macrophage-released pyrimidines inhibit gemcitabine therapy in pancreatic cancer. Cell Metab., 2019, 29(6), 1390-1399.e6.
[http://dx.doi.org/10.1016/j.cmet.2019.02.001] [PMID: 30827862]
[133]
Murphy, T.L.; Grajales-Reyes, G.E.; Wu, X.; Tussiwand, R.; Briseño, C.G.; Iwata, A.; Kretzer, N.M.; Durai, V.; Murphy, K.M. Transcriptional control of dendritic cell development. Annu. Rev. Immunol., 2016, 34, 93-119.
[http://dx.doi.org/10.1146/annurev-immunol-032713-120204] [PMID: 26735697]
[134]
Du, X.; Chapman, N.M.; Chi, H. Emerging roles of cellular metabolism in regulating dendritic cell subsets and function. Front. Cell Dev. Biol., 2018, 6, 152.
[http://dx.doi.org/10.3389/fcell.2018.00152] [PMID: 30483503]
[135]
Ayari, C.; LaRue, H.; Hovington, H.; Caron, A.; Bergeron, A.; Têtu, B.; Fradet, V.; Fradet, Y. High level of mature tumor-infiltrating dendritic cells predicts progression to muscle invasion in bladder cancer. Hum. Pathol., 2013, 44(8), 1630-1637.
[http://dx.doi.org/10.1016/j.humpath.2013.01.014] [PMID: 23574787]
[136]
Troy, A.J.; Davidson, P.J.; Atkinson, C.H.; Hart, D.N. CD1a dendritic cells predominate in transitional cell carcinoma of bladder and kidney but are minimally activated. J. Urol., 1999, 161(6), 1962-1967.
[http://dx.doi.org/10.1016/S0022-5347(05)68864-7] [PMID: 10332481]
[137]
Carrascal, M.A.; Severino, P.F.; Guadalupe Cabral, M.; Silva, M.; Ferreira, J.A.; Calais, F.; Quinto, H.; Pen, C.; Ligeiro, D.; Santos, L.L.; Dall’Olio, F.; Videira, P.A. Sialyl Tn-expressing bladder cancer cells induce a tolerogenic phenotype in innate and adaptive immune cells. Mol. Oncol., 2014, 8(3), 753-765.
[http://dx.doi.org/10.1016/j.molonc.2014.02.008] [PMID: 24656965]
[138]
Naoe, M.; Ogawa, Y.; Takeshita, K.; Morita, J.; Iwamoto, S.; Miyazaki, A.; Yoshida, H. Bacillus Calmette-Guérin-pulsed dendritic cells stimulate natural killer T cells and gammadeltaT cells. Int. J. Urol., 2007, 14(6), 532-538.
[http://dx.doi.org/10.1111/j.1442-2042.2006.01697.x] [PMID: 17593099]
[139]
Snyder, J.P.; Amiel, E. Regulation of dendritic cell immune function and metabolism by cellular nutrient sensor mammalian target of rapamycin (mTOR). Front. Immunol., 2019, 9, 3145.
[http://dx.doi.org/10.3389/fimmu.2018.03145] [PMID: 30692999]
[140]
Everts, B.; Amiel, E.; Huang, S.C-C.; Smith, A.M.; Chang, C-H.; Lam, W.Y.; Redmann, V.; Freitas, T.C.; Blagih, J.; van der Windt, G.J.; Artyomov, M.N.; Jones, R.G.; Pearce, E.L.; Pearce, E.J. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKɛ supports the anabolic demands of dendritic cell activation. Nat. Immunol., 2014, 15(4), 323-332.
[http://dx.doi.org/10.1038/ni.2833] [PMID: 24562310]
[141]
Giovanelli, P.; Sandoval, T.A.; Cubillos-Ruiz, J.R. Dendritic cell metabolism and function in tumors. Trends Immunol., 2019, 40(8), 699-718.
[http://dx.doi.org/10.1016/j.it.2019.06.004] [PMID: 31301952]
[142]
Gottfried, E.; Kunz-Schughart, L.A.; Ebner, S.; Mueller-Klieser, W.; Hoves, S.; Andreesen, R.; Mackensen, A.; Kreutz, M. Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood, 2006, 107(5), 2013-2021.
[http://dx.doi.org/10.1182/blood-2005-05-1795] [PMID: 16278308]
[143]
Herber, D.L.; Cao, W.; Nefedova, Y.; Novitskiy, S.V.; Nagaraj, S.; Tyurin, V.A.; Corzo, A.; Cho, H.I.; Celis, E.; Lennox, B.; Knight, S.C.; Padhya, T.; McCaffrey, T.V.; McCaffrey, J.C.; Antonia, S.; Fishman, M.; Ferris, R.L.; Kagan, V.E.; Gabrilovich, D.I. Lipid accumulation and dendritic cell dysfunction in cancer. Nat. Med., 2010, 16(8), 880-886.
[http://dx.doi.org/10.1038/nm.2172] [PMID: 20622859]
[144]
Veglia, F.; Tyurin, V.A.; Mohammadyani, D.; Blasi, M.; Duperret, E.K.; Donthireddy, L.; Hashimoto, A.; Kapralov, A.; Amoscato, A.; Angelini, R.; Patel, S.; Alicea-Torres, K.; Weiner, D.; Murphy, M.E.; Klein-Seetharaman, J.; Celis, E.; Kagan, V.E.; Gabrilovich, D.I. Lipid bodies containing oxidatively truncated lipids block antigen cross-presentation by dendritic cells in cancer. Nat. Commun., 2017, 8(1), 2122.
[http://dx.doi.org/10.1038/s41467-017-02186-9] [PMID: 29242535]
[145]
Grohmann, U.; Volpi, C.; Fallarino, F.; Bozza, S.; Bianchi, R.; Vacca, C.; Orabona, C.; Belladonna, M.L.; Ayroldi, E.; Nocentini, G.; Boon, L.; Bistoni, F.; Fioretti, M.C.; Romani, L.; Riccardi, C.; Puccetti, P. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat. Med., 2007, 13(5), 579-586.
[http://dx.doi.org/10.1038/nm1563] [PMID: 17417651]
[146]
Ohmatsu, H.; Humme, D.; Gonzalez, J.; Gulati, N.; Möbs, M.; Sterry, W.; Krueger, J.G. IL-32 induces indoleamine 2,3-dioxygenase+CD1c+ dendritic cells and indoleamine 2,3-dioxygenase+CD163+ macrophages: Relevance to mycosis fungoides progression. OncoImmunology, 2016, 6(2), e1181237.
[http://dx.doi.org/10.1080/2162402X.2016.1181237] [PMID: 28344860]
[147]
Malinarich, F.; Duan, K.; Hamid, R.A.; Bijin, A.; Lin, W.X.; Poidinger, M.; Fairhurst, A.M.; Connolly, J.E. High mitochondrial respiration and glycolytic capacity represent a metabolic phenotype of human tolerogenic dendritic cells. J. Immunol., 2015, 194(11), 5174-5186.
[http://dx.doi.org/10.4049/jimmunol.1303316] [PMID: 25917094]
[148]
Wculek, S.K.; Khouili, S.C.; Priego, E.; Heras-Murillo, I.; Sancho, D. Metabolic control of dendritic cell functions: digesting information. Front. Immunol., 2019, 10, 775.
[http://dx.doi.org/10.3389/fimmu.2019.00775] [PMID: 31073300]
[149]
Munder, M.; Eichmann, K.; Morán, J.M.; Centeno, F.; Soler, G.; Modolell, M. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol., 1999, 163(7), 3771-3777.
[PMID: 10490974]
[150]
Mondanelli, G.; Bianchi, R.; Pallotta, M.T.; Orabona, C.; Albini, E.; Iacono, A.; Belladonna, M.L.; Vacca, C.; Fallarino, F.; Macchiarulo, A.; Ugel, S.; Bronte, V.; Gevi, F.; Zolla, L.; Verhaar, A.; Peppelenbosch, M.; Mazza, E.M.C.; Bicciato, S.; Laouar, Y.; Santambrogio, L.; Puccetti, P.; Volpi, C.; Grohmann, U. A relay pathway between arginine and tryptophan metabolism confers immunosuppressive properties on dendritic cells. Immunity, 2017, 46(2), 233-244.
[http://dx.doi.org/10.1016/j.immuni.2017.01.005] [PMID: 28214225]
[151]
Rosales, C. Neutrophil: A cell with many roles in inflammation or several cell types? Front. Physiol., 2018, 9, 113.
[http://dx.doi.org/10.3389/fphys.2018.00113] [PMID: 29515456]
[152]
Shaul, M.E.; Fridlender, Z.G. Cancer-related circulating and tumor-associated neutrophils - subtypes, sources and function. FEBS J., 2018, 285(23), 4316-4342.
[http://dx.doi.org/10.1111/febs.14524] [PMID: 29851227]
[153]
Marchioni, M.; Primiceri, G.; Ingrosso, M.; Filograna, R.; Castellan, P.; De Francesco, P.; Schips, L. The clinical use of the Neutrophil to Lymphocyte Ratio (NLR) in urothelial cancer: a systematic review. Clin. Genitourin. Cancer, 2016, 14(6), 473-484.
[http://dx.doi.org/10.1016/j.clgc.2016.04.008] [PMID: 27209348]
[154]
Sheryka, E.; Wheeler, M.A.; Hausladen, D.A.; Weiss, R.M. Urinary interleukin-8 levels are elevated in subjects with transitional cell carcinoma. Urology, 2003, 62(1), 162-166.
[http://dx.doi.org/10.1016/S0090-4295(03)00134-1] [PMID: 12837459]
[155]
Joseph, M.; Enting, D. Immune responses in bladder cancer-role of immune cell populations, prognostic factors and therapeutic implications. Front. Oncol., 2019, 9, 1270.
[http://dx.doi.org/10.3389/fonc.2019.01270] [PMID: 31824850]
[156]
Suttmann, H.; Riemensberger, J.; Bentien, G.; Schmaltz, D.; Stöckle, M.; Jocham, D.; Böhle, A.; Brandau, S. Neutrophil granulocytes are required for effective Bacillus Calmette-Guérin immunotherapy of bladder cancer and orchestrate local immune responses. Cancer Res., 2006, 66(16), 8250-8257.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1416] [PMID: 16912205]
[157]
Galdiero, M.R.; Bonavita, E.; Barajon, I.; Garlanda, C.; Mantovani, A.; Jaillon, S. Tumor associated macrophages and neutrophils in cancer. Immunobiology, 2013, 218(11), 1402-1410.
[http://dx.doi.org/10.1016/j.imbio.2013.06.003] [PMID: 23891329]
[158]
Jablonska, J.; Leschner, S.; Westphal, K.; Lienenklaus, S.; Weiss, S. Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J. Clin. Invest., 2010, 120(4), 1151-1164.
[http://dx.doi.org/10.1172/JCI37223] [PMID: 20237412]
[159]
Pelletier, M.; Billingham, L.K.; Ramaswamy, M.; Siegel, R.M. Extracellular flux analysis to monitor glycolytic rates and mitochondrial oxygen consumption. Methods Enzymol., 2014, 542, 125-149.
[http://dx.doi.org/10.1016/B978-0-12-416618-9.00007-8] [PMID: 24862264]
[160]
Jun, H.S.; Weinstein, D.A.; Lee, Y.M.; Mansfield, B.C.; Chou, J.Y. Molecular mechanisms of neutrophil dysfunction in glycogen storage disease type Ib. Blood, 2014, 123(18), 2843-2853.
[http://dx.doi.org/10.1182/blood-2013-05-502435] [PMID: 24565827]
[161]
Sieow, J.L.; Gun, S.Y.; Wong, S.C. The sweet surrender: how myeloid cell metabolic plasticity shapes the tumor microenvironment. Front. Cell Dev. Biol., 2018, 6, 168.
[http://dx.doi.org/10.3389/fcell.2018.00168] [PMID: 30619850]
[162]
Azevedo, E.P.; Rochael, N.C.; Guimarães-Costa, A.B.; de Souza-Vieira, T.S.; Ganilho, J.; Saraiva, E.M.; Palhano, F.L.; Foguel, D. A Metabolic shift toward pentose phosphate pathway is necessary for amyloid fibril- and phorbol 12-myristate 13-acetate-induced neutrophil extracellulartrap (NET) formation. J. Biol. Chem., 2015, 290(36), 22174-22183.
[http://dx.doi.org/10.1074/jbc.M115.640094] [PMID: 26198639]
[163]
Martins de Lima, T.; Gorjão, R.; Hatanaka, E.; Cury-Boaventura, M.F.; Portioli Silva, E.P.; Procopio, J.; Curi, R. Mechanisms by which fatty acids regulate leucocyte function. Clin. Sci. (Lond.), 2007, 113(2), 65-77.
[http://dx.doi.org/10.1042/CS20070006] [PMID: 17555405]
[164]
Curi, R.; Levada-Pires, A.C.; Silva, E.B.D.; Poma, S.O.; Zambonatto, R.F.; Domenech, P.; Almeida, M.M.; Gritte, R.B.; Souza-Siqueira, T.; Gorjão, R.; Newsholme, P.; Pithon-Curi, T.C. The critical role of cell metabolism for essential neutrophil functions. cell. Physiol. Biochem., 2020, 54(4), 629-647.
[http://dx.doi.org/10.33594/000000245] [PMID: 32589830]
[165]
Riffelmacher, T.; Clarke, A.; Richter, F.C.; Stranks, A.; Pandey, S.; Danielli, S.; Hublitz, P.; Yu, Z.; Johnson, E.; Schwerd, T. Autophagy-dependent generation of free fatty acids is critical for normal neutrophil differentiation. Immunity, 2017, 47(3), 466-480.
[http://dx.doi.org/10.1016/j.immuni.2017.08.005]
[166]
Newsholme, P. Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? J. Nutr., 2001, 131(9)(Suppl.), 2515S-2522S.
[http://dx.doi.org/10.1093/jn/131.9.2515S] [PMID: 11533304]
[167]
Fan, J.; Kamphorst, J.J.; Mathew, R.; Chung, M.K.; White, E.; Shlomi, T.; Rabinowitz, J.D. Glutamine-driven oxidative phosphorylation is a major ATP source in transformed mammalian cells in both normoxia and hypoxia. Mol. Syst. Biol., 2013, 9(1), 712.
[http://dx.doi.org/10.1038/msb.2013.65] [PMID: 24301801]
[168]
Mukherjee, N.; Ji, N.; Hurez, V.; Curiel, T.J.; Montgomery, M.O.; Braun, A.J.; Nicolas, M.; Aguilera, M.; Kaushik, D.; Liu, Q.; Ruan, J.; Kendrick, K.A.; Svatek, R.S. Intratumoral CD56bright natural killer cells are associated with improved survival in bladder cancer. Oncotarget, 2018, 9(92), 36492-36502.
[http://dx.doi.org/10.18632/oncotarget.26362] [PMID: 30559932]
[169]
Brandau, S.; Riemensberger, J.; Jacobsen, M.; Kemp, D.; Zhao, W.; Zhao, X.; Jocham, D.; Ratliff, T.L.; Böhle, A. NK cells are essential for effective BCG immunotherapy. Int. J. Cancer, 2001, 92(5), 697-702.
[http://dx.doi.org/10.1002/1097-0215(20010601)92:5<697::AID-IJC1245>3.0.CO;2-Z] [PMID: 11340575]
[170]
Bisiaux, A.; Thiounn, N.; Timsit, M.O.; Eladaoui, A.; Chang, H.H.; Mapes, J.; Mogenet, A.; Bresson, J.L.; Prié, D.; Béchet, S.; Baron, C.; Sadorge, C.; Thomas, S.; Albert, E.B.; Albert, P.S.; Albert, M.L. Molecular analyte profiling of the early events and tissue conditioning following intravesical Bacillus Calmette-Guerin therapy in patients with superficial bladder cancer. J. Urol., 2009, 181(4), 1571-1580.
[http://dx.doi.org/10.1016/j.juro.2008.11.124] [PMID: 19230924]
[171]
Vivier, E.; Raulet, D.H.; Moretta, A.; Caligiuri, M.A.; Zitvogel, L.; Lanier, L.L.; Yokoyama, W.M.; Ugolini, S. Innate or adaptive immunity? The example of natural killer cells. Science, 2011, 331(6013), 44-49.
[http://dx.doi.org/10.1126/science.1198687] [PMID: 21212348]
[172]
Stojanovic, A.; Correia, M.P.; Cerwenka, A. Shaping of NK cell responses by the tumor microenvironment. Cancer Microenviron., 2013, 6(2), 135-146.
[http://dx.doi.org/10.1007/s12307-012-0125-8] [PMID: 23242671]
[173]
Keppel, M.P.; Saucier, N.; Mah, A.Y.; Vogel, T.P.; Cooper, M.A. Activation-specific metabolic requirements for NK cell IFN-γ production. J. Immunol., 2015, 194(4), 1954-1962.
[http://dx.doi.org/10.4049/jimmunol.1402099] [PMID: 25595780]
[174]
Marçais, A.; Cherfils-Vicini, J.; Viant, C.; Degouve, S.; Viel, S.; Fenis, A.; Rabilloud, J.; Mayol, K.; Tavares, A.; Bienvenu, J.; Gangloff, Y.G.; Gilson, E.; Vivier, E.; Walzer, T. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol., 2014, 15(8), 749-757.
[http://dx.doi.org/10.1038/ni.2936] [PMID: 24973821]
[175]
Maratou, E.; Dimitriadis, G.; Kollias, A.; Boutati, E.; Lambadiari, V.; Mitrou, P.; Raptis, S.A. Glucose transporter expression on the plasma membrane of resting and activated white blood cells. Eur. J. Clin. Invest., 2007, 37(4), 282-290.
[http://dx.doi.org/10.1111/j.1365-2362.2007.01786.x] [PMID: 17373964]
[176]
Shimano, H.; Sato, R. SREBP-regulated lipid metabolism: convergent physiology - divergent pathophysiology. Nat. Rev. Endocrinol., 2017, 13(12), 710-730.
[http://dx.doi.org/10.1038/nrendo.2017.91] [PMID: 28849786]
[177]
Qin, W.H.; Yang, Z.S.; Li, M.; Chen, Y.; Zhao, X.F.; Qin, Y.Y.; Song, J.Q.; Wang, B.B.; Yuan, B.; Cui, X.L.; Shen, F.; He, J.; Bi, Y.F.; Ning, G.; Fu, J.; Wang, H.Y. High serum levels of cholesterol increase antitumor functions of nature killer cells and reduce growth of liver tumors in mice. Gastroenterology, 2020, 158(6), 1713-1727.
[http://dx.doi.org/10.1053/j.gastro.2020.01.028] [PMID: 31972238]
[178]
Yamauchi, T.; Kamon, J.; Ito, Y.; Tsuchida, A.; Yokomizo, T.; Kita, S.; Sugiyama, T.; Miyagishi, M.; Hara, K.; Tsunoda, M.; Murakami, K.; Ohteki, T.; Uchida, S.; Takekawa, S.; Waki, H.; Tsuno, N.H.; Shibata, Y.; Terauchi, Y.; Froguel, P.; Tobe, K.; Koyasu, S.; Taira, K.; Kitamura, T.; Shimizu, T.; Nagai, R.; Kadowaki, T. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature, 2003, 423(6941), 762-769.
[http://dx.doi.org/10.1038/nature01705] [PMID: 12802337]
[179]
Loftus, R.M.; Assmann, N.; Kedia-Mehta, N.; O’Brien, K.L.; Garcia, A.; Gillespie, C.; Hukelmann, J.L.; Oefner, P.J.; Lamond, A.I.; Gardiner, C.M.; Dettmer, K.; Cantrell, D.A.; Sinclair, L.V.; Finlay, D.K. Amino acid-dependent cMyc expression is essential for NK cell metabolic and functional responses in mice. Nat. Commun., 2018, 9(1), 2341.
[http://dx.doi.org/10.1038/s41467-018-04719-2] [PMID: 29904050]
[180]
Shi, R.; Tang, Y.Q.; Miao, H. Metabolism in tumor microenvironment: Implications for cancer immunotherapy. MedComm, 2020, 1(1), 47-68.
[http://dx.doi.org/10.1002/mco2.6]
[181]
Li, W.; Tanikawa, T.; Kryczek, I.; Xia, H.; Li, G.; Wu, K.; Wei, S.; Zhao, L.; Vatan, L.; Wen, B.; Shu, P.; Sun, D.; Kleer, C.; Wicha, M.; Sabel, M.; Tao, K.; Wang, G.; Zou, W. Aerobic glycolysis controls myeloid-derived suppressor cells and tumor immunity via a specific CEBPB isoform intriple-negative breast cancer. Cell Metab., 2018, 28(1), 87-103.e6.
[http://dx.doi.org/10.1016/j.cmet.2018.04.022] [PMID: 29805099]
[182]
Eruslanov, E.; Neuberger, M.; Daurkin, I.; Perrin, G.Q.; Algood, C.; Dahm, P.; Rosser, C.; Vieweg, J.; Gilbert, S.M.; Kusmartsev, S. Circulating and tumor-infiltrating myeloid cell subsets in patients with bladder cancer. Int. J. Cancer, 2012, 130(5), 1109-1119.
[http://dx.doi.org/10.1002/ijc.26123] [PMID: 21480223]
[183]
Yang, G.; Shen, W.; Zhang, Y.; Liu, M.; Zhang, L.; Liu, Q.; Lu, H.H.; Bo, J. Accumulation of myeloid-derived suppressor cells (MDSCs) induced by low levels of IL-6 correlates with poor prognosis in bladder cancer. Oncotarget, 2017, 8(24), 38378-38388.
[http://dx.doi.org/10.18632/oncotarget.16386] [PMID: 28418913]
[184]
Ornstein, M.C.; Diaz-Montero, C.M.; Rayman, P.; Elson, P.; Haywood, S.; Finke, J.H.; Kim, J.S.; Pavicic, P.G., Jr; Lamenza, M.; Devonshire, S.; Dann, P.; Schach, K.; Stephenson, A.; Campbell, S.; Emamekhoo, H.; Ernstoff, M.S.; Hoimes, C.J.; Gilligan, T.D.; Rini, B.I.; Garcia, J.A.; Grivas, P. Myeloid-derived suppressors cells (MDSC) correlate with clinicopathologic factors and pathologic complete response (pCR) in patients with urothelial carcinoma (UC) undergoing cystectomy. Urol. Oncol., 2018, 36(9), 405-412.
[http://dx.doi.org/10.1016/j.urolonc.2018.02.018] [PMID: 29606341]
[185]
Wu, K.; Tan, M.Y.; Jiang, J.T.; Mu, X.Y.; Wang, J.R.; Zhou, W.J.; Wang, X.; Li, M.Q.; He, Y.Y.; Liu, Z.H. Cisplatin inhibits the progression of bladder cancer by selectively depleting G-MDSCs: A novel chemoimmunomodulating strategy. Clin. Immunol., 2018, 193, 60-69.
[http://dx.doi.org/10.1016/j.clim.2018.01.012] [PMID: 29410331]
[186]
Chevalier, M.F.; Trabanelli, S.; Racle, J.; Salomé, B.; Cesson, V.; Gharbi, D.; Bohner, P.; Domingos-Pereira, S.; Dartiguenave, F.; Fritschi, A.S.; Speiser, D.E.; Rentsch, C.A.; Gfeller, D.; Jichlinski, P.; Nardelli-Haefliger, D.; Jandus, C.; Derré, L. ILC2-modulated T cell-to-MDSC balance is associated with bladder cancer recurrence. J. Clin. Invest., 2017, 127(8), 2916-2929.
[http://dx.doi.org/10.1172/JCI89717] [PMID: 28650339]
[187]
Husain, Z.; Seth, P.; Sukhatme, V.P. Tumor-derived lactate and myeloid-derived suppressor cells: Linking metabolism to cancer immunology. OncoImmunology, 2013, 2(11), e26383.
[http://dx.doi.org/10.4161/onci.26383] [PMID: 24404426]
[188]
Srivastava, M.K.; Sinha, P.; Clements, V.K.; Rodriguez, P.; Ostrand-Rosenberg, S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res., 2010, 70(1), 68-77.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-2587] [PMID: 20028852]
[189]
Hossain, F.; Al-Khami, A.A.; Wyczechowska, D.; Hernandez, C.; Zheng, L.; Reiss, K.; Valle, L.D.; Trillo-Tinoco, J.; Maj, T.; Zou, W.; Rodriguez, P.C.; Ochoa, A.C. Inhibition of fatty acid oxidation modulates immunosuppressive functions of myeloid-derived suppressor cells and enhances cancer therapies. Cancer Immunol. Res., 2015, 3(11), 1236-1247.
[http://dx.doi.org/10.1158/2326-6066.CIR-15-0036] [PMID: 26025381]
[190]
Hanson, E.M.; Clements, V.K.; Sinha, P.; Ilkovitch, D.; Ostrand-Rosenberg, S. Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J. Immunol., 2009, 183(2), 937-944.
[http://dx.doi.org/10.4049/jimmunol.0804253] [PMID: 19553533]
[191]
Baumann, T.; Dunkel, A.; Schmid, C.; Schmitt, S.; Hiltensperger, M.; Lohr, K.; Laketa, V.; Donakonda, S.; Ahting, U.; Lorenz-Depiereux, B.; Heil, J.E.; Schredelseker, J.; Simeoni, L.; Fecher, C.; Körber, N.; Bauer, T.; Hüser, N.; Hartmann, D.; Laschinger, M.; Eyerich, K.; Eyerich, S.; Anton, M.; Streeter, M.; Wang, T.; Schraven, B.; Spiegel, D.; Assaad, F.; Misgeld, T.; Zischka, H.; Murray, P.J.; Heine, A.; Heikenwälder, M.; Korn, T.; Dawid, C.; Hofmann, T.; Knolle, P.A.; Höchst, B. Regulatory myeloid cells paralyze T cells through cell-cell transfer of the metabolite methylglyoxal. Nat. Immunol., 2020, 21(5), 555-566.
[http://dx.doi.org/10.1038/s41590-020-0666-9] [PMID: 32327756]
[192]
Ramesh, V.; Locasale, J.W. A reactive metabolite as an immune suppressant. Nat. Immunol., 2020, 21(5), 497-498.
[http://dx.doi.org/10.1038/s41590-020-0664-y] [PMID: 32327751]
[193]
Corzo, C.A.; Condamine, T.; Lu, L.; Cotter, M.J.; Youn, J.I.; Cheng, P.; Cho, H.I.; Celis, E.; Quiceno, D.G.; Padhya, T.; McCaffrey, T.V.; McCaffrey, J.C.; Gabrilovich, D.I. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med., 2010, 207(11), 2439-2453.
[http://dx.doi.org/10.1084/jem.20100587] [PMID: 20876310]
[194]
Movahedi, K.; Guilliams, M.; Van den Bossche, J.; Van den Bergh, R.; Gysemans, C.; Beschin, A.; De Baetselier, P.; Van Ginderachter, J.A. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood, 2008, 111(8), 4233-4244.
[http://dx.doi.org/10.1182/blood-2007-07-099226] [PMID: 18272812]
[195]
Kaidi, A.; Qualtrough, D.; Williams, A.C.; Paraskeva, C. Direct transcriptional up-regulation of cyclooxygenase-2 by hypoxia-inducible factor (HIF)-1 promotes colorectal tumor cell survival and enhances HIF-1 transcriptional activity during hypoxia. Cancer Res., 2006, 66(13), 6683-6691.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0425] [PMID: 16818642]
[196]
Obermajer, N.; Muthuswamy, R.; Odunsi, K.; Edwards, R.P.; Kalinski, P. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res., 2011, 71(24), 7463-7470.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-2449] [PMID: 22025564]
[197]
Braun, D.; Longman, R.S.; Albert, M.L. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood, 2005, 106(7), 2375-2381.
[http://dx.doi.org/10.1182/blood-2005-03-0979] [PMID: 15947091]
[198]
Rodriguez, P.C.; Hernandez, C.P.; Quiceno, D.; Dubinett, S.M.; Zabaleta, J.; Ochoa, J.B.; Gilbert, J.; Ochoa, A.C. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J. Exp. Med., 2005, 202(7), 931-939.
[http://dx.doi.org/10.1084/jem.20050715] [PMID: 16186186]
[199]
Renner, K.; Singer, K.; Koehl, G.E.; Geissler, E.K.; Peter, K.; Siska, P.J.; Kreutz, M. Metabolic hallmarks of tumor and immune cells in the tumor microenvironment. Front. Immunol., 2017, 8, 248.
[http://dx.doi.org/10.3389/fimmu.2017.00248] [PMID: 28337200]
[200]
Long, Y.C.; Zierath, J.R. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest., 2006, 116(7), 1776-1783.
[http://dx.doi.org/10.1172/JCI29044] [PMID: 16823475]
[201]
Trikha, P.; Plews, R.L.; Stiff, A.; Gautam, S.; Hsu, V.; Abood, D.; Wesolowski, R.; Landi, I.; Mo, X.; Phay, J.; Chen, C.S.; Byrd, J.; Caligiuri, M.; Tridandapani, S.; Carson, W. Targeting myeloid-derived suppressor cells using a novel adenosine monophosphate-activated protein kinase (AMPK) activator. OncoImmunology, 2016, 5(9), e1214787.
[http://dx.doi.org/10.1080/2162402X.2016.1214787] [PMID: 27757311]

Rights & Permissions Print Cite
Article Metrics
29
2
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy