Login Register Cart 0
Generic placeholder image

Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

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

Anti-Diabetic Effects of Isolated Lipids from Natural Sources through Modulation of Angiogenesis

Author(s): Soraya Sajadimajd, Mina Khosravifar and Gholamreza Bahrami*

Volume 15, Issue 4, 2022

Published on: 07 January, 2022

Article ID: e020921196076 Pages: 18

DOI: 10.2174/1874467214666210902121337

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Aberrant angiogenesis plays a fateful role in the development of diabetes and diabetic complications. Lipids, as a diverse group of biomacromolecules, are able to relieve diabetes through the modulation of angiogenesis.

Objectives: Owing to the present remarkable anti-diabetic effects with no or few side effects of lipids, the aim of this study was to assess the state-of-the-art research on anti-diabetic effects of lipids via the modulation of angiogenesis.

Methods: To study the effects of lipids in diabetes via modulation of angiogenesis, we have searched the electronic databases including Scopus, PubMed, and Cochrane.

Results: The promising anti-diabetic effects of lipids were reported in several studies. Eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) from fish oil (FO) were reported to significantly induce neovasculogenesis in high glucose (HG)-mediated endothelial progenitor cells (EPCs) with neovasculogenesis dysfunction in type 2 diabetic mice. Linoleic acid, mono-epoxy-tocotrienol- α (MeT3α), and ginsenoside Rg1 facilitate wound closure and vessel formation. N-Palmitoylethanolamine (PEA), α-linolenic acid (ALA), omega-3 (ω3) lipids from flaxseed (FS) oil, ω-3 polyunsaturated fatty acids (PUFA), lipoic acid, taurine, and zeaxanthin (Zx) are effective in diabetic retinopathy via suppression of angiogenesis. Lysophosphatidic acid, alkyl-glycerophosphate, crocin, arjunolic acid, α-lipoic acid, and FS oil are involved in the management of diabetes and its cardiac complications. Furthermore, in two clinical trials, R-(+)-lipoic acid (RLA) in combination with hyperbaric oxygenation therapy (HBOT) for treatment of chronic wound healing in DM patients, as well as supplementation with DHA plus antioxidants along with intravitreal ranibizumab were investigated for its effects on diabetic macular edema.

Conclusion: Proof-of-concept studies presented here seem to well shed light on the anti-diabetic effects of lipids via modulation of angiogenesis.

Keywords: Diabetes, diabetic complications, angiogenesis, isolated lipids, natural sources, modulation.

Graphical Abstract

[1]
Ogurtsova, K.; da Rocha Fernandes, J.D.; Huang, Y.; Linnenkamp, U.; Guariguata, L.; Cho, N.H.; Cavan, D.; Shaw, J.E.; Makaroff, L.E. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res. Clin. Pract., 2017, 128, 40-50.
[http://dx.doi.org/10.1016/j.diabres.2017.03.024] [PMID: 28437734]
[2]
Danaei, G.; Finucane, M.M.; Lu, Y.; Singh, G.M.; Cowan, M.J.; Paciorek, C.J.; Lin, J.K.; Farzadfar, F.; Khang, Y.H.; Stevens, G.A.; Rao, M.; Ali, M.K.; Riley, L.M.; Robinson, C.A.; Ezzati, M. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2·7 million participants. Lancet, 2011, 378(9785), 31-40.
[http://dx.doi.org/10.1016/S0140-6736(11)60679-X] [PMID: 21705069]
[3]
Tuomi, T.; Santoro, N.; Caprio, S.; Cai, M.; Weng, J.; Groop, L. The many faces of diabetes: a disease with increasing heterogeneity. Lancet, 2014, 383(9922), 1084-1094.
[http://dx.doi.org/10.1016/S0140-6736(13)62219-9] [PMID: 24315621]
[4]
Stumvoll, M.; Goldstein, B.J.; van Haeften, T.W. Type 2 diabetes: principles of pathogenesis and therapy. Lancet, 2005, 365(9467), 1333-1346.
[http://dx.doi.org/10.1016/S0140-6736(05)61032-X] [PMID: 15823385]
[5]
Florez, J.C. Clinical review: the genetics of type 2 diabetes: a realistic appraisal in 2008. J. Clin. Endocrinol. Metab., 2008, 93(12), 4633-4642.
[http://dx.doi.org/10.1210/jc.2008-1345] [PMID: 18782870]
[6]
Beck-Nielsen, H.; Groop, L.C. Metabolic and genetic characterization of prediabetic states. Sequence of events leading to non-insulin-dependent diabetes mellitus. J. Clin. Invest., 1994, 94(5), 1714-1721.
[http://dx.doi.org/10.1172/JCI117518] [PMID: 7962519]
[7]
Stettler, C.; Christ, E.; Diem, P. Novelties in diabetes; Karger Medical and Scientific Publishers, 2016.
[http://dx.doi.org/10.1159/isbn.978-3-318-05639-6]
[8]
Røder, M.E.; Kahn, S.E. Suppression of Beta-cell secretion by somatostatin does not fully reverse the disproportionate proinsulinemia of type 2 diabetes. Diabetes, 2004, 53(Suppl. 3), S22-S25.
[http://dx.doi.org/10.2337/diabetes.53.suppl_3.S22] [PMID: 15561914]
[9]
Chatterjee, S.; Khunti, K.; Davies, M.J. Type 2 diabetes. Lancet, 2017, 389(10085), 2239-2251.
[http://dx.doi.org/10.1016/S0140-6736(17)30058-2] [PMID: 28190580]
[10]
de Rekeneire, N.; Peila, R.; Ding, J.; Colbert, L.H.; Visser, M.; Shorr, R.I.; Kritchevsky, S.B.; Kuller, L.H.; Strotmeyer, E.S.; Schwartz, A.V.; Vellas, B.; Harris, T.B. Diabetes, hyperglycemia, and inflammation in older individuals: the health, aging and body composition study. Diabetes Care, 2006, 29(8), 1902-1908.
[http://dx.doi.org/10.2337/dc05-2327] [PMID: 16873800]
[11]
Felisbino, M.B.; Ziemann, M.; Khurana, I.; Okabe, J.; Al-Hasani, K.; Maxwell, S.; Harikrishnan, K.N.; de Oliveira, C.B.M.; Mello, M.L.S.; El-Osta, A. Valproic acid influences the expression of genes implicated with hyperglycaemia-induced complement and coagulation pathways. Sci. Rep., 2021, 11(1), 2163.
[http://dx.doi.org/10.1038/s41598-021-81794-4] [PMID: 33495488]
[12]
Atkinson, M.A.; Eisenbarth, G.S.; Michels, A.W. Type 1 diabetes. Lancet, 2014, 383(9911), 69-82.
[http://dx.doi.org/10.1016/S0140-6736(13)60591-7] [PMID: 23890997]
[13]
Concannon, P.; Rich, S.S.; Nepom, G.T. Genetics of type 1A diabetes. N. Engl. J. Med., 2009, 360(16), 1646-1654.
[http://dx.doi.org/10.1056/NEJMra0808284] [PMID: 19369670]
[14]
Association, A.D. American Diabetes Association 2. Classification and diagnosis of diabetes: standards of medical care in diabetes—2019. Diabetes Care, 2019, 42(Suppl. 1), S13-S28.
[http://dx.doi.org/10.2337/dc19-S002] [PMID: 30559228]
[15]
Atlas, D. IDF Diabetes Atlas, 7th ed; International Diabetes Federation: Brussels, Belgium, 2015. Available from: https://www.diabetesatlas.org/upload/resources/previous/files/7/IDF%20Diabetes%20Atlas%207th.pdf
[16]
Nathan, D.M. Long-term complications of diabetes mellitus. N. Engl. J. Med., 1993, 328(23), 1676-1685.
[http://dx.doi.org/10.1056/NEJM199306103282306] [PMID: 8487827]
[17]
Gerstein, H.C.; Werstuck, G.H. Dysglycaemia, vasculopenia, and the chronic consequences of diabetes. Lancet Diabetes Endocrinol., 2013, 1(1), 71-78.
[http://dx.doi.org/10.1016/S2213-8587(13)70025-1] [PMID: 24622269]
[18]
Aronow, W.S.; McClung, J.A. Translational research in coronary artery disease: pathophysiology to treatment; Academic Press, 2015.
[19]
Martin, A.; Komada, M.R.; Sane, D.C. Abnormal angiogenesis in diabetes mellitus. Med. Res. Rev., 2003, 23(2), 117-145.
[http://dx.doi.org/10.1002/med.10024] [PMID: 12500286]
[20]
Wang, P-C.; Zhao, S.; Yang, B-Y.; Wang, Q-H.; Kuang, H-X. Anti-diabetic polysaccharides from natural sources: A review. Carbohydr. Polym., 2016, 148, 86-97.
[http://dx.doi.org/10.1016/j.carbpol.2016.02.060] [PMID: 27185119]
[21]
Wu, H.; Xu, G.; Liao, Y.; Ren, H.; Fan, J.; Sun, Z.; Zhang, M. Supplementation with antioxidants attenuates transient worsening of retinopathy in diabetes caused by acute intensive insulin therapy. Graefes Arch. Clin. Exp. Ophthalmol., 2012, 250(10), 1453-1458.
[http://dx.doi.org/10.1007/s00417-012-2079-4] [PMID: 22695936]
[22]
Lee, S.G.; Lee, C.G.; Yun, I.H.; Hur, D.Y.; Yang, J.W.; Kim, H.W. Effect of lipoic acid on expression of angiogenic factors in diabetic rat retina. Clin. Exp. Ophthalmol., 2012, 40(1), e47-e57.
[http://dx.doi.org/10.1111/j.1442-9071.2011.02695.x] [PMID: 21902786]
[23]
Pfister, F.; Riedl, E.; Wang, Q.; vom Hagen, F.; Deinzer, M.; Harmsen, M.C.; Molema, G.; Yard, B.; Feng, Y.; Hammes, H.P. Oral carnosine supplementation prevents vascular damage in experimental diabetic retinopathy. Cell. Physiol. Biochem., 2011, 28(1), 125-136.
[http://dx.doi.org/10.1159/000331721] [PMID: 21865855]
[24]
Dátilo, M.N.; Sant’Ana, M.R.; Formigari, G.P.; Rodrigues, P.B.; de Moura, L.P.; da Silva, A.S.R.; Ropelle, E.R.; Pauli, J.R.; Cintra, D.E. Omega-3 from flaxseed oil protects obese mice against diabetic retinopathy through GPR120 receptor. Sci. Rep., 2018, 8(1), 14318.
[http://dx.doi.org/10.1038/s41598-018-32553-5] [PMID: 30254287]
[25]
Human nutrition: Encyclopædia Britannica, inc., Available from: https://www.britannica.com/science/human-nutrition/Lipids#accordion-article-contributorshttps://www.britannica.com/science/human-nutrition
[26]
Chiu, S-C.; Chao, C-Y.; Chiang, E.I.; Syu, J-N.; Rodriguez, R.L.; Tang, F-Y. N-3 polyunsaturated fatty acids alleviate high glucose- mediated dysfunction of endothelial progenitor cells and prevent ischemic injuries both in vitro and in vivo. J. Nutr. Biochem., 2017, 42, 172-181.
[http://dx.doi.org/10.1016/j.jnutbio.2017.01.009] [PMID: 28189115]
[27]
Luo, X.; Jia, R.; Yao, Q.; Xu, Y.; Luo, Z.; Luo, X.; Wang, N. Docosahexaenoic acid attenuates adipose tissue angiogenesis and insulin resistance in high fat diet-fed middle-aged mice via a sirt1-dependent mechanism. Mol. Nutr. Food Res., 2016, 60(4), 871-885.
[http://dx.doi.org/10.1002/mnfr.201500714] [PMID: 26750093]
[28]
Shishtar, E.; Jovanovski, E.; Jenkins, A.; Vuksan, V. Effects of Korean White Ginseng (Panax Ginseng CA Meyer) on vascular and glycemic health in type 2 diabetes: results of a randomized, double blind, placebo-controlled, multiple-crossover, acute dose escalation trial. Clin. Nutr. Res., 2014, 3(2), 89-97.
[http://dx.doi.org/10.7762/cnr.2014.3.2.89] [PMID: 25136536]
[29]
Sen, S.; Chen, S.; Wu, Y.; Feng, B.; Lui, E.K.; Chakrabarti, S. Preventive effects of North American ginseng (Panax quinquefolius) on diabetic retinopathy and cardiomyopathy. Phytother. Res., 2013, 27(2), 290-298.
[http://dx.doi.org/10.1002/ptr.4719] [PMID: 22566158]
[30]
Shi, Y.; Wan, X.; Shao, N.; Ye, R.; Zhang, N.; Zhang, Y. Protective and anti-angiopathy effects of ginsenoside Re against diabetes mellitus via the activation of p38 MAPK, ERK1/2 and JNK signaling. Mol. Med. Rep., 2016, 14(5), 4849-4856.
[http://dx.doi.org/10.3892/mmr.2016.5821] [PMID: 27748921]
[31]
Balwierz, A.; Polus, A.; Razny, U.; Wator, L.; Dyduch, G.; Tomaszewska, R.; Scherneck, S.; Joost, H.; Dembinska-Kiec, A. Angiogenesis in the New Zealand obese mouse model fed with high fat diet. Lipids Health Dis., 2009, 8(1), 13.
[http://dx.doi.org/10.1186/1476-511X-8-13] [PMID: 19344534]
[32]
Nwadozi, E.; Roudier, E.; Rullman, E.; Tharmalingam, S.; Liu, H.Y.; Gustafsson, T.; Haas, T.L. Endothelial FoxO proteins impair insulin sensitivity and restrain muscle angiogenesis in response to a high-fat diet. FASEB J., 2016, 30(9), 3039-3052.
[http://dx.doi.org/10.1096/fj.201600245R] [PMID: 27235148]
[33]
Rodrigues, H.G.; Vinolo, M.A.; Sato, F.T.; Magdalon, J.; Kuhl, C.M.; Yamagata, A.S.; Pessoa, A.F.; Malheiros, G.; Dos Santos, M.F.; Lima, C.; Farsky, S.H.; Camara, N.O.; Williner, M.R.; Bernal, C.A.; Calder, P.C.; Curi, R. Oral administration of linoleic acid induces new vessel formation and improves skin wound healing in diabetic rats. PLoS One, 2016, 11(10), e0165115.
[http://dx.doi.org/10.1371/journal.pone.0165115] [PMID: 27764229]
[34]
Rodrigues, H.G.; Vinolo, M.A.R.; Magdalon, J.; Fujiwara, H.; Cavalcanti, D.M.; Farsky, S.H.; Calder, P.C.; Hatanaka, E.; Curi, R. Dietary free oleic and linoleic acid enhances neutrophil function and modulates the inflammatory response in rats. Lipids, 2010, 45(9), 809-819.
[http://dx.doi.org/10.1007/s11745-010-3461-9] [PMID: 20730605]
[35]
Vessby, B. Dietary fat, fatty acid composition in plasma and the metabolic syndrome. Curr. Opin. Lipidol., 2003, 14(1), 15-19.
[http://dx.doi.org/10.1097/00041433-200302000-00004] [PMID: 12544656]
[36]
Marti, P.; Stein, C.; Blumer, T.; Abraham, Y.; Dill, M.T.; Pikiolek, M.; Orsini, V.; Jurisic, G.; Megel, P.; Makowska, Z.; Agarinis, C.; Tornillo, L.; Bouwmeester, T.; Ruffner, H.; Bauer, A.; Parker, C.N.; Schmelzle, T.; Terracciano, L.M.; Heim, M.H.; Tchorz, J.S. YAP promotes proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma through TEAD transcription factors. Hepatology, 2015, 62(5), 1497-1510.
[http://dx.doi.org/10.1002/hep.27992] [PMID: 26173433]
[37]
Singh, A.; Ramesh, S.; Cibi, D.M.; Yun, L.S.; Li, J.; Li, L.; Manderfield, L.J.; Olson, E.N.; Epstein, J.A.; Singh, M.K. Hippo signaling mediators Yap and Taz are required in the epicardium for coronary vasculature development. Cell Rep., 2016, 15(7), 1384-1393.
[http://dx.doi.org/10.1016/j.celrep.2016.04.027] [PMID: 27160901]
[38]
Moya, I.M.; Halder, G. The Hippo pathway in cellular reprogramming and regeneration of different organs. Curr. Opin. Cell Biol., 2016, 43, 62-68.
[http://dx.doi.org/10.1016/j.ceb.2016.08.004] [PMID: 27592171]
[39]
Yuan, L.; Mao, Y.; Luo, W.; Wu, W.; Xu, H.; Wang, X.L.; Shen, Y.H. Palmitic acid dysregulates the Hippo-YAP pathway and inhibits angiogenesis by inducing mitochondrial damage and activating the cytosolic DNA sensor cGAS-STING-IRF3 signaling mechanism. J. Biol. Chem., 2017, 292(36), 15002-15015.
[http://dx.doi.org/10.1074/jbc.M117.804005] [PMID: 28698384]
[40]
Aggarwal, B.B.; Sundaram, C.; Prasad, S.; Kannappan, R. Tocotrienols, the vitamin E of the 21st century: its potential against cancer and other chronic diseases. Biochem. Pharmacol., 2010, 80(11), 1613-1631.
[http://dx.doi.org/10.1016/j.bcp.2010.07.043] [PMID: 20696139]
[41]
Bentinger, M.; Tekle, M.; Brismar, K.; Chojnacki, T.; Swiezewska, E.; Dallner, G. Polyisoprenoid epoxides stimulate the biosynthesis of coenzyme Q and inhibit cholesterol synthesis. J. Biol. Chem., 2008, 283(21), 14645-14653.
[http://dx.doi.org/10.1074/jbc.M710202200] [PMID: 18353784]
[42]
Turunen, M.; Olsson, J.; Dallner, G. Metabolism and function of coenzyme Q. Biochimica et Biophysica Acta (BBA)-. Biomembranes, 2004, 1660(1-2), 171-199.
[http://dx.doi.org/10.1016/j.bbamem.2003.11.012]
[43]
Xu, C.; Bentinger, M.; Savu, O.; Moshfegh, A.; Sunkari, V.; Dallner, G.; Swiezewska, E.; Catrina, S.B.; Brismar, K.; Tekle, M. Mono-epoxy-tocotrienol-α enhances wound healing in diabetic mice and stimulates in vitro angiogenesis and cell migration. J. Diabetes Complications, 2017, 31(1), 4-12.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.10.010] [PMID: 27839658]
[44]
Yu, H.; Zhen, J.; Yang, Y.; Gu, J.; Wu, S.; Liu, Q. Ginsenoside Rg1 ameliorates diabetic cardiomyopathy by inhibiting endoplasmic reticulum stress-induced apoptosis in a streptozotocin-induced diabetes rat model. J. Cell. Mol. Med., 2016, 20(4), 623-631.
[http://dx.doi.org/10.1111/jcmm.12739] [PMID: 26869403]
[45]
Wang, W.; Zhang, E.; Lin, C. MicroRNAs in tumor angiogenesis. Life Sci., 2015, 136, 28-35.
[http://dx.doi.org/10.1016/j.lfs.2015.06.025] [PMID: 26144623]
[46]
Martin, E.; Nathan, C.; Xie, Q.W. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp. Med., 1994, 180(3), 977-984.
[http://dx.doi.org/10.1084/jem.180.3.977] [PMID: 7520478]
[47]
Cai, H-A.; Huang, L.; Zheng, L-J.; Fu, K.; Wang, J.; Hu, F-D.; Liao, R.Y. Ginsenoside (Rg-1) promoted the wound closure of diabetic foot ulcer through iNOS elevation via miR-23a/IRF-1 axis. Life Sci., 2019, 233, 116525.
[http://dx.doi.org/10.1016/j.lfs.2019.05.081] [PMID: 31158376]
[48]
Stone, J.R.; Collins, T. The role of hydrogen peroxide in endothelial proliferative responses. Endothelium, 2002, 9(4), 231-238.
[http://dx.doi.org/10.1080/10623320214733] [PMID: 12572854]
[49]
Enea, N.A.; Hollis, T.M.; Kern, J.A.; Gardner, T.W. Histamine H1 receptors mediate increased blood-retinal barrier permeability in experimental diabetes. Arch. Ophthalmol., 1989, 107(2), 270-274.
[http://dx.doi.org/10.1001/archopht.1989.01070010276036] [PMID: 2521787]
[50]
Tang, J.; Kern, T.S. Inflammation in diabetic retinopathy. Prog. Retin. Eye Res., 2011, 30(5), 343-358.
[http://dx.doi.org/10.1016/j.preteyeres.2011.05.002] [PMID: 21635964]
[51]
Lu, L.; Seidel, C.P.; Iwase, T.; Stevens, R.K.; Gong, Y.Y.; Wang, X.; Hackett, S.F.; Campochiaro, P.A. Suppression of GLUT1; a new strategy to prevent diabetic complications. J. Cell. Physiol., 2013, 228(2), 251-257.
[http://dx.doi.org/10.1002/jcp.24133] [PMID: 22717959]
[52]
De La Cruz, J.P.; González-Correa, J.A.; Guerrero, A.; de la Cuesta, F.S. Pharmacological approach to diabetic retinopathy. Diabetes Metab. Res. Rev., 2004, 20(2), 91-113.
[http://dx.doi.org/10.1002/dmrr.432] [PMID: 15037985]
[53]
Ciulla, T.A.; Amador, A.G.; Zinman, B. Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care, 2003, 26(9), 2653-2664.
[http://dx.doi.org/10.2337/diacare.26.9.2653] [PMID: 12941734]
[54]
Giacco, F.; Brownlee, M. Oxidative stress and diabetic complications. Circ. Res., 2010, 107(9), 1058-1070.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.223545] [PMID: 21030723]
[55]
Yamagishi, S.; Nakamura, K.; Matsui, T.; Inagaki, Y.; Takenaka, K.; Jinnouchi, Y.; Yoshida, Y.; Matsuura, T.; Narama, I.; Motomiya, Y.; Takeuchi, M.; Inoue, H.; Yoshimura, A.; Bucala, R.; Imaizumi, T. Pigment epithelium-derived factor inhibits advanced glycation end product-induced retinal vascular hyperpermeability by blocking reactive oxygen species-mediated vascular endothelial growth factor expression. J. Biol. Chem., 2006, 281(29), 20213-20220.
[http://dx.doi.org/10.1074/jbc.M602110200] [PMID: 16707486]
[56]
Mancini, J.E.; Ortiz, G.; Croxatto, J.O.; Gallo, J.E. Retinal upregulation of inflammatory and proangiogenic markers in a model of neonatal diabetic rats fed on a high-fat-diet. BMC Ophthalmol., 2013, 13(1), 14.
[http://dx.doi.org/10.1186/1471-2415-13-14] [PMID: 23587252]
[57]
Das, U.N. Metabolic syndrome pathophysiology: the role of essential fatty acids; John Wiley & Sons, 2010.
[http://dx.doi.org/10.1002/9780813820637]
[58]
Das, U.N. Cell Membrane Organization. In: Molecular Basis of Health and Disease; Springer, 2011; pp. 153-173.
[http://dx.doi.org/10.1007/978-94-007-0495-4_5]
[59]
Serhan, C.N.; Clish, C.B.; Brannon, J.; Colgan, S.P.; Chiang, N.; Gronert, K. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J. Exp. Med., 2000, 192(8), 1197-1204.
[http://dx.doi.org/10.1084/jem.192.8.1197] [PMID: 11034610]
[60]
Mukherjee, P.K.; Marcheselli, V.L.; Serhan, C.N.; Bazan, N.G. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl. Acad. Sci. USA, 2004, 101(22), 8491-8496.
[http://dx.doi.org/10.1073/pnas.0402531101] [PMID: 15152078]
[61]
Shen, J.H.; Ma, Q.; Shen, S.R.; Xu, G-T.; Das, U.N. Effect of α-linolenic acid on streptozotocin-induced diabetic retinopathy indices in vivo. Arch. Med. Res., 2013, 44(7), 514-520.
[http://dx.doi.org/10.1016/j.arcmed.2013.09.010] [PMID: 24120388]
[62]
Krabbe, K.S.; Nielsen, A.R.; Krogh-Madsen, R.; Plomgaard, P.; Rasmussen, P.; Erikstrup, C.; Fischer, C.P.; Lindegaard, B.; Petersen, A.M.; Taudorf, S.; Secher, N.H.; Pilegaard, H.; Bruunsgaard, H.; Pedersen, B.K. Brain-derived neurotrophic factor (BDNF) and type 2 diabetes. Diabetologia, 2007, 50(2), 431-438.
[http://dx.doi.org/10.1007/s00125-006-0537-4] [PMID: 17151862]
[63]
Paterniti, I.; Di Paola, R.; Campolo, M.; Siracusa, R.; Cordaro, M.; Bruschetta, G.; Tremolada, G.; Maestroni, A.; Bandello, F.; Esposito, E.; Zerbini, G.; Cuzzocrea, S. Palmitoylethanolamide treatment reduces retinal inflammation in streptozotocin-induced diabetic rats. Eur. J. Pharmacol., 2015, 769, 313-323.
[http://dx.doi.org/10.1016/j.ejphar.2015.11.035] [PMID: 26607470]
[64]
Oliveira, V.; Marinho, R.; Vitorino, D.; Santos, G.A.; Moraes, J.C.; Dragano, N.; Sartori-Cintra, A.; Pereira, L.; Catharino, R.R.; da Silva, A.S.; Ropelle, E.R.; Pauli, J.R.; De Souza, C.T.; Velloso, L.A.; Cintra, D.E. Diets containing α-linolenic (ω3) or oleic (ω9) fatty acids rescues obese mice from insulin resistance. Endocrinology, 2015, 156(11), 4033-4046.
[http://dx.doi.org/10.1210/en.2014-1880] [PMID: 26280128]
[65]
Oh, D.Y.; Talukdar, S.; Bae, E.J.; Imamura, T.; Morinaga, H.; Fan, W.; Li, P.; Lu, W.J.; Watkins, S.M.; Olefsky, J.M. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell, 2010, 142(5), 687-698.
[http://dx.doi.org/10.1016/j.cell.2010.07.041] [PMID: 20813258]
[66]
Cintra, D.E.; Ropelle, E.R.; Moraes, J.C.; Pauli, J.R.; Morari, J.; Souza, C.T.; Grimaldi, R.; Stahl, M.; Carvalheira, J.B.; Saad, M.J.; Velloso, L.A. Unsaturated fatty acids revert diet-induced hypothalamic inflammation in obesity. PLoS One, 2012, 7(1), e30571.
[http://dx.doi.org/10.1371/journal.pone.0030571] [PMID: 22279596]
[67]
Tikhonenko, M.; Lydic, T.A.; Opreanu, M.; Li Calzi, S.; Bozack, S.; McSorley, K.M.; Sochacki, A.L.; Faber, M.S.; Hazra, S.; Duclos, S.; Guberski, D.; Reid, G.E.; Grant, M.B.; Busik, J.V. N-3 polyunsaturated Fatty acids prevent diabetic retinopathy by inhibition of retinal vascular damage and enhanced endothelial progenitor cell reparative function. PLoS One, 2013, 8(1), e55177.
[http://dx.doi.org/10.1371/journal.pone.0055177] [PMID: 23383097]
[68]
Kern, TS Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. J. Diabetes Res., 2007, 2007, 1-14.
[http://dx.doi.org/10.1155/2007/95103]
[69]
Kielczewski, J.L.; Li Calzi, S.; Shaw, L.C.; Cai, J.; Qi, X.; Ruan, Q.; Wu, L.; Liu, L.; Hu, P.; Chan-Ling, T.; Mames, R.N.; Firth, S.; Baxter, R.C.; Turowski, P.; Busik, J.V.; Boulton, M.E.; Grant, M.B. Free insulin-like growth factor binding protein-3 (IGFBP-3) reduces retinal vascular permeability in association with a reduction of acid sphingomyelinase (ASMase). Invest. Ophthalmol. Vis. Sci., 2011, 52(11), 8278-8286.
[http://dx.doi.org/10.1167/iovs.11-8167] [PMID: 21931131]
[70]
Caballero, S.; Sengupta, N.; Afzal, A.; Chang, K-H.; Li Calzi, S.; Guberski, D.L.; Kern, T.S.; Grant, M.B. Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes, 2007, 56(4), 960-967.
[http://dx.doi.org/10.2337/db06-1254] [PMID: 17395742]
[71]
Tikhonenko, M.; Lydic, T.A.; Wang, Y.; Chen, W.; Opreanu, M.; Sochacki, A.; McSorley, K.M.; Renis, R.L.; Kern, T.; Jump, D.B.; Reid, G.E.; Busik, J.V. Remodeling of retinal Fatty acids in an animal model of diabetes: a decrease in long-chain polyunsaturated fatty acids is associated with a decrease in fatty acid elongases Elovl2 and Elovl4. Diabetes, 2010, 59(1), 219-227.
[http://dx.doi.org/10.2337/db09-0728] [PMID: 19875612]
[72]
Chorváthová, V.; Ondreicka, R. The fatty acid composition of the tissues of streptozotocin-diabetic rats. Physiol. Bohemoslov., 1983, 32(5), 466-475.
[PMID: 6647591]
[73]
Chan, J.Y.; Cole, E.; Hanna, A.K. Diabetic nephropathy and proliferative retinopathy with normal glucose tolerance. Diabetes Care, 1985, 8(4), 385-390.
[http://dx.doi.org/10.2337/diacare.8.4.385] [PMID: 4042806]
[74]
Capozzi, M.E.; Giblin, M.J.; Penn, J.S. Palmitic Acid Induces Müller Cell Inflammation that is Potentiated by Co-treatment with Glucose. Sci. Rep., 2018, 8(1), 5459.
[http://dx.doi.org/10.1038/s41598-018-23601-1] [PMID: 29626212]
[75]
Packer, L.; Kraemer, K.; Rimbach, G. Molecular aspects of lipoic acid in the prevention of diabetes complications. Nutrition, 2001, 17(10), 888-895.
[http://dx.doi.org/10.1016/S0899-9007(01)00658-X] [PMID: 11684397]
[76]
Obrosova, I.G.; Minchenko, A.G.; Marinescu, V.; Fathallah, L.; Kennedy, A.; Stockert, C.M.; Frank, R.N.; Stevens, M.J. Antioxidants attenuate early up regulation of retinal vascular endothelial growth factor in streptozotocin-diabetic rats. Diabetologia, 2001, 44(9), 1102-1110.
[http://dx.doi.org/10.1007/s001250100631] [PMID: 11596663]
[77]
Lim, E.; Park, S.; Kim, H. Effect of taurine supplementation on the lipid peroxide formation and the activities of glutathione-related enzymes in the liver and islet of type I and II diabetic model mice. In: Taurine 3; Springer, 1998; pp. 99-103.
[http://dx.doi.org/10.1007/978-1-4899-0117-0_13]
[78]
Raschke, P.; Massoudy, P.; Becker, B.F. Taurine protects the heart from neutrophil-induced reperfusion injury. Free Radic. Biol. Med., 1995, 19(4), 461-471.
[http://dx.doi.org/10.1016/0891-5849(95)00044-X] [PMID: 7590395]
[79]
Sturman, J.A.; Rassin, D.K.; Hayes, K.C.; Gaull, G.E. Taurine deficiency in the kitten: exchange and turnover of [35S] taurine in brain, retina, and other tissues. J. Nutr., 1978, 108(9), 1462-1476.
[http://dx.doi.org/10.1093/jn/108.9.1462] [PMID: 682050]
[80]
Thomson, L.R.; Toyoda, Y.; Langner, A.; Delori, F.C.; Garnett, K.M.; Craft, N.; Nichols, C.R.; Cheng, K.M.; Dorey, C.K. Elevated retinal zeaxanthin and prevention of light-induced photoreceptor cell death in quail. Invest. Ophthalmol. Vis. Sci., 2002, 43(11), 3538-3549.
[PMID: 12407166]
[81]
Stahl, W.; Sies, H. Bioactivity and protective effects of natural carotenoids. Biochimica et Biophysica Acta (BBA)-. Molecular Basis of Disease., 2005, 1740(2), 101-107.
[http://dx.doi.org/10.1016/j.bbadis.2004.12.006]
[82]
Whitehead, A.J.; Mares, J.A.; Danis, R.P. Macular pigment: a review of current knowledge. Arch. Ophthalmol., 2006, 124(7), 1038-1045.
[http://dx.doi.org/10.1001/archopht.124.7.1038] [PMID: 16832030]
[83]
Kowluru, R.A.; Zhong, Q. Beyond AREDS: is there a place for antioxidant therapy in the prevention/treatment of eye disease? Invest. Ophthalmol. Vis. Sci., 2011, 52(12), 8665-8671.
[http://dx.doi.org/10.1167/iovs.10-6768] [PMID: 22065212]
[84]
Coyne, T.; Ibiebele, T.I.; Baade, P.D.; Dobson, A.; McClintock, C.; Dunn, S.; Leonard, D.; Shaw, J. Diabetes mellitus and serum carotenoids: findings of a population-based study in Queensland, Australia. Am. J. Clin. Nutr., 2005, 82(3), 685-693.
[http://dx.doi.org/10.1093/ajcn/82.3.685] [PMID: 16155284]
[85]
Kowluru, R.A.; Menon, B.; Gierhart, D.L. Beneficial effect of zeaxanthin on retinal metabolic abnormalities in diabetic rats. Invest. Ophthalmol. Vis. Sci., 2008, 49(4), 1645-1651.
[http://dx.doi.org/10.1167/iovs.07-0764] [PMID: 18385086]
[86]
Waltenberger, J. New horizons in diabetes therapy: the angiogenesis paradox in diabetes: description of the problem and presentation of a unifying hypothesis. Immunol Endocr Metab Agents Med Chem (Formerly Current Medicinal Chemistry-Immunology, Endocrine and Metabolic Agents), 2007, 7(1), 87-93.
[http://dx.doi.org/10.2174/187152207779802536]
[87]
Kornowski, R.; Mintz, G.S.; Kent, K.M.; Pichard, A.D.; Satler, L.F.; Bucher, T.A.; Hong, M.K.; Popma, J.J.; Leon, M.B. Increased restenosis in diabetes mellitus after coronary interventions is due to exaggerated intimal hyperplasia. A serial intravascular ultrasound study. Circulation, 1997, 95(6), 1366-1369.
[http://dx.doi.org/10.1161/01.CIR.95.6.1366] [PMID: 9118501]
[88]
Abaci, A.; Oğuzhan, A.; Kahraman, S.; Eryol, N.K.; Unal, S.; Arinç, H.; Ergin, A. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation, 1999, 99(17), 2239-2242.
[http://dx.doi.org/10.1161/01.CIR.99.17.2239] [PMID: 10226087]
[89]
Wu, H.; Xia, X.; Jiang, C.; Wu, J.; Zhang, S.; Zheng, Z.; Liu, W.; Zhang, Y.; Ren, H.; Wei, C.; Xu, X. High glucose attenuates insulin-induced VEGF expression in bovine retinal microvascular endothelial cells. Eye (Lond.), 2010, 24(1), 145-151.
[http://dx.doi.org/10.1038/eye.2009.157] [PMID: 19557019]
[90]
Hoshi, S.; Nomoto, K.; Kuromitsu, J.; Tomari, S.; Nagata, M. High glucose induced VEGF expression via PKC and ERK in glomerular podocytes. Biochem. Biophys. Res. Commun., 2002, 290(1), 177-184.
[http://dx.doi.org/10.1006/bbrc.2001.6138] [PMID: 11779150]
[91]
Xia, L.; Wang, H.; Munk, S.; Frecker, H.; Goldberg, H.J.; Fantus, I.G.; Whiteside, C.I. Reactive oxygen species, PKC-β1, and PKC-ζ mediate high-glucose-induced vascular endothelial growth factor expression in mesangial cells. Am. J. Physiol. Endocrinol. Metab., 2007, 293(5), E1280-E1288.
[http://dx.doi.org/10.1152/ajpendo.00223.2007] [PMID: 17711990]
[92]
Doronzo, G.; Viretto, M.; Russo, I.; Mattiello, L.; Anfossi, G.; Trovati, M. Effects of high glucose on vascular endothelial growth factor synthesis and secretion in aortic vascular smooth muscle cells from obese and lean Zucker rats. Int. J. Mol. Sci., 2012, 13(8), 9478-9488.
[http://dx.doi.org/10.3390/ijms13089478] [PMID: 22949809]
[93]
Yilmaz, A.; Kliche, S.; Mayr-Beyrle, U.; Fellbrich, G.; Waltenberger, J. p38 MAPK inhibition is critically involved in VEGFR-2-mediated endothelial cell survival. Biochem. Biophys. Res. Commun., 2003, 306(3), 730-736.
[http://dx.doi.org/10.1016/S0006-291X(03)01064-7] [PMID: 12810080]
[94]
Wardle, E. How does hyperglycaemia predispose to diabetic nephropathy? QJM: monthly J Associ Phys, 1996, 89(12), 943-51.
[http://dx.doi.org/10.1093/qjmed/89.12.943]
[95]
Pernow, J.; Shemyakin, A.; Böhm, F. New perspectives on endothelin-1 in atherosclerosis and diabetes mellitus. Life Sci., 2012, 91(13-14), 507-516.
[http://dx.doi.org/10.1016/j.lfs.2012.03.029] [PMID: 22483688]
[96]
Tigyi, G.; Parrill, A.L. Molecular mechanisms of lysophosphatidic acid action. Prog. Lipid Res., 2003, 42(6), 498-526.
[http://dx.doi.org/10.1016/S0163-7827(03)00035-3] [PMID: 14559069]
[97]
Tsukahara, T.; Tsukahara, R.; Yasuda, S.; Makarova, N.; Valentine, W.J.; Allison, P.; Yuan, H.; Baker, D.L.; Li, Z.; Bittman, R.; Parrill, A.; Tigyi, G. Different residues mediate recognition of 1-O-oleyllysophosphatidic acid and rosiglitazone in the ligand binding domain of peroxisome proliferator-activated receptor γ. J. Biol. Chem., 2006, 281(6), 3398-3407.
[http://dx.doi.org/10.1074/jbc.M510843200] [PMID: 16321982]
[98]
Bishop-Bailey, D. Peroxisome proliferator-activated receptors in the cardiovascular system. Br. J. Pharmacol., 2000, 129(5), 823-834.
[http://dx.doi.org/10.1038/sj.bjp.0703149] [PMID: 10696077]
[99]
Yoshizaki, T.; Motomura, W.; Tanno, S.; Kumei, S.; Yoshizaki, Y.; Tanno, S.; Okumura, T. Thiazolidinediones enhance vascular endothelial growth factor expression and induce cell growth inhibition in non-small-cell lung cancer cells. J. Exp. Clin. Cancer Res., 2010, 29(1), 22.
[http://dx.doi.org/10.1186/1756-9966-29-22] [PMID: 20214829]
[100]
Tsukahara, T.; Tsukahara, R.; Fujiwara, Y.; Yue, J.; Cheng, Y.; Guo, H.; Bolen, A.; Zhang, C.; Balazs, L.; Re, F.; Du, G.; Frohman, M.A.; Baker, D.L.; Parrill, A.L.; Uchiyama, A.; Kobayashi, T.; Murakami- Murofushi, K.; Tigyi, G. Phospholipase D2-dependent inhibition of the nuclear hormone receptor PPARgamma by cyclic phosphatidic acid. Mol. Cell, 2010, 39(3), 421-432.
[http://dx.doi.org/10.1016/j.molcel.2010.07.022] [PMID: 20705243]
[101]
Tsukahara, T.; Tsukahara, R.; Haniu, H.; Matsuda, Y.; Murakami- Murofushi, K. Cyclic phosphatidic acid inhibits the secretion of vascular endothelial growth factor from diabetic human coronary artery endothelial cells through peroxisome proliferator-activated receptor gamma. Mol. Cell. Endocrinol., 2015, 412, 320-329.
[http://dx.doi.org/10.1016/j.mce.2015.05.021] [PMID: 26007326]
[102]
Bie, X.; Chen, Y.; Zheng, X.; Dai, H. The role of crocetin in protection following cerebral contusion and in the enhancement of angiogenesis in rats. Fitoterapia, 2011, 82(7), 997-1002.
[http://dx.doi.org/10.1016/j.fitote.2011.06.001] [PMID: 21741458]
[103]
Lee, S.; Park, Y.; Zhang, C. Exercise training prevents coronary endothelial dysfunction in type 2 diabetic mice. Am. J. Biomed. Sci., 2011, 3(4), 241-252.
[http://dx.doi.org/10.5099/aj110400241] [PMID: 22384308]
[104]
Dariushnejad, H.; Mohammadi, M.; Ghorbanzadeh, V. Crocin and voluntary exercise promote heart angiogenesis through Akt and ERK1/2 signalling in type 2 diabetic rats. Bratisl. Lek Listy, 2018, 119(12), 757-761.
[PMID: 30686014]
[105]
Manna, P.; Sil, P.C. Impaired redox signaling and mitochondrial uncoupling contributes vascular inflammation and cardiac dysfunction in type 1 diabetes: Protective role of arjunolic acid. Biochimie, 2012, 94(3), 786-797.
[http://dx.doi.org/10.1016/j.biochi.2011.11.010] [PMID: 22155371]
[106]
Dworacka, M.; Chukanova, G.; Iskakova, S.; Kurmambayev, Y.; Wesołowska, A.; Frycz, B.A.; Jagodziński, P.P.; Dworacki, G. New arguments for beneficial effects of alpha-lipoic acid on the cardiovascular system in the course of type 2 diabetes. Eur. J. Pharm. Sci., 2018, 117, 41-47.
[http://dx.doi.org/10.1016/j.ejps.2018.02.009] [PMID: 29427700]
[107]
Zeng, H.; Dvorak, H.F.; Mukhopadhyay, D. Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) peceptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem., 2001, 276(29), 26969-26979.
[http://dx.doi.org/10.1074/jbc.M103213200] [PMID: 11350975]
[108]
Vicente, G.C.; Correia-Santos, A.M.; Suzuki, A.; Chagas, M.A.; Boaventura, G.T. Maternal use of a diet rich omega-3 from flaxseed improves aortic remodeling but not the biochemical parameters of female offspring of diabetic rats. Eur. J. Lipid Sci. Technol., 2015, 117(3), 291-299.
[http://dx.doi.org/10.1002/ejlt.201400210]
[109]
Nasole, E.; Nicoletti, C.; Yang, Z.J.; Girelli, A.; Rubini, A.; Giuffreda, F.; Di Tano, A.; Camporesi, E.; Bosco, G. Effects of alpha lipoic acid and its R+ enantiomer supplemented to hyperbaric oxygen therapy on interleukin-6, TNF-α and EGF production in chronic leg wound healing. J. Enzyme Inhib. Med. Chem., 2014, 29(2), 297-302.
[http://dx.doi.org/10.3109/14756366.2012.759951] [PMID: 23360079]
[110]
Lafuente, M.; Ortín, L.; Argente, M.; Guindo, J.L.; López-Bernal, M.D.; López-Román, F.J.; García, M.J.; Domingo, J.C.; Lajara, J. Combined intravitreal ranibizumab and oral supplementation with docosahexaenoic acid and antioxidants for diabetic macular edema: Two-year randomized single-blind controlled trial results. Retina, 2017, 37(7), 1277-1286.
[http://dx.doi.org/10.1097/IAE.0000000000001363] [PMID: 27787443]
[111]
Petrosino, S.; Di Marzo, V. The pharmacology of palmitoylethanolamide and first data on the therapeutic efficacy of some of its new formulations. Br. J. Pharmacol., 2017, 174(11), 1349-1365.
[http://dx.doi.org/10.1111/bph.13580] [PMID: 27539936]
[112]
Yore, M.M.; Syed, I.; Moraes-Vieira, P.M.; Zhang, T.; Herman, M.A.; Homan, E.A.; Patel, R.T.; Lee, J.; Chen, S.; Peroni, O.D.; Dhaneshwar, A.S.; Hammarstedt, A.; Smith, U.; McGraw, T.E.; Saghatelian, A.; Kahn, B.B. Discovery of a class of endogenous mammalian lipids with anti-diabetic and anti-inflammatory effects. Cell, 2014, 159(2), 318-332.
[http://dx.doi.org/10.1016/j.cell.2014.09.035] [PMID: 25303528]

Rights & Permissions Print Cite
Article Metrics
47
1
Wayfinder Image
Open Access Journals Promotions
© 2024 Bentham Science Publishers | Privacy Policy