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
Mini-Review Article

Newly-onset Autoimmune Diabetes Mellitus Triggered by COVID 19 Infection: A Case-based Review

Author(s): Gamze Akkuş*

Volume 23, Issue 7, 2023

Published on: 17 October, 2022

Page: [887 - 893] Pages: 7

DOI: 10.2174/2666145415666221004111511

Price: $65

Abstract

The devastating global pandemic Coronavirus disease 2019 (COVID 19) isolated in China in January 2020 is responsible for an outbreak of pneumonia and other multisystemic complications. The clinical picture of the infection has extreme variability: it goes from asymptomatic patients or mild forms with fever, cough, fatigue and loss of smell and taste to severe cases ending up in the intensive care unit (ICU). This is due to a possible cytokine storm that may lead to multiorgan failure, septic shock, or thrombosis.

Severe Acute Respiratory Syndrome coronavirus 2 (SARS-CoV -2), which is the virus that causes COVID 19, binds to angiotensin-converting enzyme 2 (ACE2) receptors, which are expressed in key metabolic organs and tissues, including pancreatic beta cells, adipose tissue, the small intestine and the kidneys. Therefore it is possible to state that newly-onset diabetes is triggered by COVID 19 infection.

Although many hypotheses have clarified the potential diabetogenic effect of COVID 19, a few observations were reported during this pandemic. Two male patients admitted to us with devastating hyperglycemia symptoms were diagnosed with type 1/autoimmune diabetes mellitus within 3 months following COVID 19 infection. Autoantibodies and decreased C peptide levels were detected in these patients. We speculated that several mechanisms might trigger autoimmune insulitis and pancreatic beta-cell destruction by COVID 19 infection. We aim to raise awareness of the possible link between SARS-CoV-2 and newly onset type 1 diabetes mellitus. Further studies are needed to determine a more definitive link between the two clinical entities.

Keywords: COVID-19, autoimmune, diabetes mellitus, inflammation, pandemia beta cell, destruction, c-peptide.

« Previous Next »
Graphical Abstract

[1]
Huang, C.; Wang, Y.; Li, X.; Ren, L.; Zhao, J.; Hu, Y. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020, 395(10223), 497-506.
[http://dx.doi.org/10.1016/S0140-6736(20)30183-5]
[2]
Vallianou, N.G.; Evangelopoulos, A.; Kounatidis, D.; Stratigou, T.; Christodoulatos, G.S.; Karampela, I.; Dalamaga, M. Diabetes mellitus and SARS-CoV-2 infection: Pathophysiologic mechanisms and implications in management. Curr. Diabetes Rev., 2021, 17(6), e123120189797.
[http://dx.doi.org/10.2174/1573399817666210101110253] [PMID: 33388022]
[3]
Doremalen, N.; Bushmaker, T.; Morris, D.H.; Holbrook, M.G.; Gamble, A.; Williamson, B.N.; Tamin, A.; Harcourt, J.L.; Thornburg, N.J.; Gerber, S.I.; Lloyd, S.J.O.; De Wit, E.; Munster, V.J. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med., 2020, 382(16), 1564-1567.
[http://dx.doi.org/10.1056/NEJMc2004973] [PMID: 32182409]
[4]
Hoffmann, M.; Wever, H.; Kruger, N.; Muller, M.; Drotsten, C. The novel Coronavirus 2019 (2019-nCoV) uses the SARS coronavirus receptor ACE2 and the cellular protease TMPRSS2 for entryin target cells. Cell, 2020, 181(2), 271-280.e8.
[5]
Liu, Y.; Yang, Y.; Zhang, C.; Huang, F.; Wang, F.; Yuan, J.; Wang, Z.; Li, J. Clinical and biochemical indexes from 2019-nCoV infected patients linked to viral loads and lung injury. Sci. China Life Sci., 2020, 63(3), 364-374.
[http://dx.doi.org/10.1007/s11427-020-1643-8] [PMID: 32048163]
[6]
Yang, J.; Zheng, Y.; Gou, X.; Pu, K.; Chen, Z.; Guo, Q.; Ji, R.; Wang, H.; Wang, Y.; Zhou, Y. Prevalence of comorbidities in the novel Wuhan Coronavirus (COVID-19) infection: A systematic review and meta-analysis. Int. J. Infect. Dis., 2020, 9712, 30136.
[7]
Adhikari, S.P.; Meng, S.; Wu, Y.J.; Mao, Y.P.; Ye, R.X.; Wang, Q.Z. Epidemiology, causes, clinical manifestation and diagnosis, prevention and control of Coronavirus Disease (COVID-19) during the early outbreak period: A scoping review. Infect. Dis. Poverty, 2020, 9(1), 29.
[8]
Guo, Y.R.; Cao, Q.D.; Hong, Z.S.; Tan, Y.Y.; Chen, S.D.; Jin, H.J. The origin, transmission and clinical therapies on Coronavirus disease 2019 (COVID-19) outbreak - An update on the status. Mil. Med. Res., 2020, 2020, 7.
[9]
Hussain, A.; Bhowmik, B.; Do Vale Moreira, N.C. COVID-19 and diabetes: Knowledge in progress. Diabetes Res. Clin. Pract., 2020, 162, 108142.
[http://dx.doi.org/10.1016/j.diabres.2020.108142] [PMID: 32278764]
[10]
Haller, M.J.; Schatz, D.A. The DIPP project: 20 years of discovery in type 1 diabetes. Pediatr. Diabetes, 2016, 17(22), 5-7.
[http://dx.doi.org/10.1111/pedi.12398] [PMID: 27411430]
[11]
Tatti, P.; Tonolo, G.; Zanfardino, A.; Iafusco, D. Is it fair to hope that patients with type 1 diabetes (autoimmune) may be spared by the infection of COVID-19? Med. Hypotheses, 2020, 142, 109795.
[http://dx.doi.org/10.1016/j.mehy.2020.109795] [PMID: 32416410]
[12]
Yang, J.K.; Lin, S.S.; Ji, X.J.; Guo, L.M. Binding of SARS coronavirus to its receptor damages islets and causes acute diabetes. Acta Diabetol., 2010, 47(3), 193-199.
[http://dx.doi.org/10.1007/s00592-009-0109-4] [PMID: 19333547]
[13]
Berg, H.; Walter, M.; Mauch, L.; Seissler, J.; Northemann, W. Recombinant human preproinsulin expression, purification and reaction with insulin autoantibodies in sera from patients with insulin-dependent diabetes mellitus. J. Immunol. Methods, 1993, 164(2), 221-231.
[http://dx.doi.org/10.1016/0022-1759(93)90315-X] [PMID: 8370928]
[14]
Cooke, A. Infection and autoimmunity. Blood Cells Mol. Dis., 2009, 42(2), 105-107.
[http://dx.doi.org/10.1016/j.bcmd.2008.10.004] [PMID: 19027331]
[15]
Devendra, D.; Eisenbarth, G.S. Interferon alpha-A potential link in the pathogenesis of viral-induced type 1 diabetes and autoimmunity. Clin. Immunol., 2004, 111(3), 225-233.
[http://dx.doi.org/10.1016/j.clim.2004.01.008] [PMID: 15183143]
[16]
Dotta, F.; Censini, S.; Van Halteren, A.G.S.; Marselli, L.; Masini, M.; Dionisi, S.; Mosca, F.; Boggi, U.; Muda, A.O.; Prato, S.D.; Elliott, J.F.; Covacci, A.; Rappuoli, R.; Roep, B.O.; Marchetti, P. Coxsackie B4 virus infection of β cells and natural killer cell insulitis in recentonset type 1 diabetic patients. Proc. Natl. Acad. Sci. USA, 2007, 104(12), 5115-5120.
[http://dx.doi.org/10.1073/pnas.0700442104] [PMID: 17360338]
[17]
Ebekozien, O.A.; Noor, N.; Gallagher, M.P.; Alonso, G.T. Type 1 diabetes and COVID-19: Preliminary findings from a multicenter surveillance study in the U.S. Diabetes Care, 2020, 43(8), e83-e85.
[http://dx.doi.org/10.2337/dc20-1088] [PMID: 32503837]
[18]
Zhu, L.; She, Z.G.; Cheng, X.; Qin, J.J.; Zhang, X.J.; Cai, J.; Lei, F.; Wang, H.; Xie, J.; Wang, W.; Li, H.; Zhang, P.; Song, X.; Chen, X.; Xiang, M.; Zhang, C.; Bai, L.; Xiang, D.; Chen, M.M.; Liu, Y.; Yan, Y.; Liu, M.; Mao, W.; Zou, J.; Liu, L.; Chen, G.; Luo, P.; Xiao, B.; Zhang, C.; Zhang, Z.; Lu, Z.; Wang, J.; Lu, H.; Xia, X.; Wang, D.; Liao, X.; Peng, G.; Ye, P.; Yang, J.; Yuan, Y.; Huang, X.; Guo, J.; Zhang, B.H.; Li, H. Association of blood glucose control and outcomes in patients with COVID-19 and pre-existing type 2 diabetes. Cell Metab., 2020, 31(6), 1068-1077.
[http://dx.doi.org/10.1016/j.cmet.2020.04.021] [PMID: 32369736]
[19]
Caruso, P.; Longo, M.; Esposito, K.; Maiorino, M.I. Type 1 diabetes triggered by COVID-19 pandemic: A potential outbreak? Diabetes Res. Clin. Pract., 2020, 164, 108219.
[http://dx.doi.org/10.1016/j.diabres.2020.108219] [PMID: 32442555]
[20]
Ehrenfeld, M.; Tincani, A.; Andreoli, L.; Cattalini, M.; Greenbaum, A.; Kanduc, D.; Alijotas, R.J.; Zinserling, V.; Semenova, N.; Amital, H.; Shoenfeld, Y. COVID-19 and autoimmunity. Autoimmun. Rev., 2020, 19(8), 102597.
[http://dx.doi.org/10.1016/j.autrev.2020.102597] [PMID: 32535093]
[21]
Wang, J.; Jiang, M.; Chen, X.; Montaner, L.J. Cytokine storm and leukocyte changes in mild versus severe SARS-CoV-2 infection: Review of 3939 COVID-19 patients in China and emerging pathogenesis and therapy concepts. J. Leukoc. Biol., 2020, 108(1), 17-41.
[http://dx.doi.org/10.1002/JLB.3COVR0520-272R] [PMID: 32534467]
[22]
Rodríguez, Y.; Novelli, L.; Rojas, M.; De Santis, M.; Acosta, A.Y.; Monsalve, D.M.; Ramírez, S.C.; Costanzo, A.; Ridgway, W.M.; Ansari, A.A.; Gershwin, M.E.; Selmi, C.; Anaya, J.M. Autoinflammatory and autoimmune conditions at the crossroad of COVID-19. J. Autoimmun., 2020, 114, 102506.
[http://dx.doi.org/10.1016/j.jaut.2020.102506] [PMID: 32563547]
[23]
Mehta, P.; McAuley, D.F.; Brown, M.; Sanchez, E.; Tattersall, R.S.; Manson, J.J. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet, 2020, 395(10229), 1033-1034.
[http://dx.doi.org/10.1016/S0140-6736(20)30628-0] [PMID: 32192578]
[24]
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]
[25]
Barrett, J.C.; Clayton, D.G.; Concannon, P.; Akolkar, B.; Cooper, J.D.; Erlich, H.A.; Julier, C.; Morahan, G.; Nerup, J.; Nierras, C.; Plagnol, V.; Pociot, F.; Schuilenburg, H.; Smyth, D.J.; Stevens, H.; Todd, J.A.; Walker, N.M.; Rich, S.S. Genome-wide association study and metaanalysis find that over 40 loci affect risk of type 1 diabetes. Nat. Genet., 2009, 41(6), 703-707.
[http://dx.doi.org/10.1038/ng.381] [PMID: 19430480]
[26]
Mahaffy, J.M.; Edelstein, K.L. Modeling cyclic waves of circulating T cells in autoimmune diabetes. SIAM J. Appl. Math., 2007, 67(4), 915-937.
[http://dx.doi.org/10.1137/060661144]
[27]
Rabin, D.U.; Pleasic, S.M.; Shapiro, J.A.; Yoo, W.H.; Oles, J.; Hicks, J.M.; Goldstein, D.E.; Rae, P.M. Islet cell antigen 512 is a diabetesspecific islet autoantigen related to protein tyrosine phosphatases. J. Immunol., 1994, 152(6), 3183-3188.
[PMID: 8144912]
[28]
Månsson, L.; Törn, C.; Landin, O.M. Islet cell antibodies represent autoimmune response against several antigens. Int. J. Exp. Diabetes Res., 2001, 2(2), 85-90.
[http://dx.doi.org/10.1155/EDR.2001.85] [PMID: 12369720]
[29]
Eisenbarth, G.; Moriyama, H.; Robles, D.T.; Liu, E.; Yu, L.; Babu, S.; Redondo, M.J.; Gottlieb, P.; Wegmann, D.; Rewers, M. Insulin autoimmunity: Prediction/precipitation/prevention type 1A diabetes. Autoimmun. Rev., 2002, 1(3), 139-145.
[http://dx.doi.org/10.1016/S1568-9972(02)00035-6] [PMID: 12849007]
[30]
Hanifi, M.P.; Schloot, N.C.; Kappler, S. Seiβler, J.; Kolb, H. An association of autoantibody status and serum cytokine levels in type 1 diabetes. Diabetes, 2003, 52(5), 1137-1142.
[http://dx.doi.org/10.2337/diabetes.52.5.1137] [PMID: 12716743]
[31]
Nelson, P.; Smith, N.; Ciupe, S.; Zou, W.; Omenn, G.S.; Pietropaolo, M. Modeling dynamic changes in type 1 diabetes progression: Quantifying β-cell variation after the appearance of islet-specific autoimmune responses. Math. Biosci. Eng., 2009, 6(4), 753-778.
[http://dx.doi.org/10.3934/mbe.2009.6.753] [PMID: 19835428]
[32]
Pietropaolo, M.; Surhigh, J.M.; Nelson, P.W.; Eisenbarth, G.S. Primer: Immunity and autoimmunity. Diabetes, 2008, 57(11), 2872-2882.
[http://dx.doi.org/10.2337/db07-1691] [PMID: 18971434]
[33]
Yamamoto, A.M.; Deschamps, I.; Garchon, H.J.; Roussely, H.; Moreau, N.; Beaurain, G.; Robert, J.J.; Bach, J.F. Young age and HLA markers enhance the risk of progression to type 1 diabetes in antibodypositive siblings of diabetic children. J. Autoimmun., 1998, 11(6), 643-650.
[http://dx.doi.org/10.1006/jaut.1998.0244] [PMID: 9878086]
[34]
Brusko, T.M.; Putnam, A.L.; Bluestone, J.A. Human regulatory T cells: Role in autoimmune disease and therapeutic opportunities. Immunol. Rev., 2008, 223(1), 371-390.
[http://dx.doi.org/10.1111/j.1600-065X.2008.00637.x] [PMID: 18613848]
[35]
Martin, S.; Wolf, E.D.; Duinkerken, G.; Scherbaum, W.A.; Kolb, H.; Noordzij, J.G.; Roep, B.O. Development of type 1 diabetes despite severe hereditary B-cell deficiency. N. Engl. J. Med., 2001, 345(14), 1036-1040.
[http://dx.doi.org/10.1056/NEJMoa010465] [PMID: 11586956]
[36]
Redondo, M.J.; Eisenbarth, G.S. Genetic control of autoimmunity in type I diabetes and associated disorders. Diabetologia, 2002, 45(5), 605-622.
[http://dx.doi.org/10.1007/s00125-002-0781-1] [PMID: 12107741]
[37]
Pietropaolo, M.; Becker, D.J.; LaPorte, R.E.; Dorman, J.S.; Riboni, S.; Rudert, W.A.; Mazumdar, S.; Trucco, M. Progression to insulin-requiring diabetes in seronegative prediabetic subjects: The role of two HLA-DQ high-risk haplotypes. Diabetologia, 2002, 45(1), 66-76.
[http://dx.doi.org/10.1007/s125-002-8246-5] [PMID: 11845225]
[38]
Khadra, A.; Santamaria, P.; Edelstein, K.L. The role of low avidity T cells in the protection against type 1 diabetes: A modeling investigation. J. Theor. Biol., 2009, 256(1), 126-141.
[http://dx.doi.org/10.1016/j.jtbi.2008.09.019] [PMID: 18950644]
[39]
Pescovitz, M.D.; Greenbaum, C.J.; Krause, S.H.; Becker, D.J.; Gitelman, S.E.; Goland, R.; Gottlieb, P.A.; Marks, J.B.; McGee, P.F.; Moran, A.M.; Raskin, P.; Rodriguez, H.; Schatz, D.A.; Wherrett, D.; Wilson, D.M.; Lachin, J.M.; Skyler, J.S. Rituximab, B-lymphocyte depletion,and preservation of β-cell function. N. Engl. J. Med., 2009, 361(22), 2143-2152.
[http://dx.doi.org/10.1056/NEJMoa0904452] [PMID: 19940299]
[40]
Millet, J.K.; Whittaker, G.R. Host cell proteases: Critical determinants of coronavirus tropism and pathogenesis. Virus Res., 2015, 202, 120-134.
[http://dx.doi.org/10.1016/j.virusres.2014.11.021] [PMID: 25445340]
[41]
Baum, A.; Fulton, B.O.; Wloga, E.; Copin, R.; Pascal, K.E.; Russo, V.; Giordano, S.; Lanza, K.; Negron, N.; Ni, M.; Wei, Y.; Atwal, G.S.; Murphy, A.J.; Stahl, N.; Yancopoulos, G.D.; Kyratsous, C.A. Antibody cocktail to SARS-CoV-2 spike protein prevents rapid mutational escape seen with individual antibodies. Science, 2020, 369(6506), 1014-1018.
[http://dx.doi.org/10.1126/science.abd0831] [PMID: 32540904]
[42]
Hoffmann, M.; Kleine, W.H.; Pöhlmann, S. A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells. Cell, 2020, 78(4), 779-784.e5.
[PMID: 32362314]
[43]
Lam, T.T.Y.; Jia, N.; Zhang, Y.W.; Shum, M.H.H.; Jiang, J.F.; Zhu, H.C.; Tong, Y.G.; Shi, Y.X.; Ni, X.B.; Liao, Y.S.; Li, W.J.; Jiang, B.G.; Wei, W.; Yuan, T.T.; Zheng, K.; Cui, X.M.; Li, J.; Pei, G.Q.; Qiang, X.; Cheung, W.Y.M.; Li, L.F.; Sun, F.F.; Qin, S.; Huang, J.C.; Leung, G.M.; Holmes, E.C.; Hu, Y.L.; Guan, Y.; Cao, W.C. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature, 2020, 583(7815), 282-285.
[http://dx.doi.org/10.1038/s41586-020-2169-0] [PMID: 32218527]
[44]
Lu, R.; Zhao, X.; Li, J.; Niu, P.; Yang, B.; Wu, H.; Wang, W.; Song, H.; Huang, B.; Zhu, N.; Bi, Y.; Ma, X.; Zhan, F.; Wang, L.; Hu, T.; Zhou, H.; Hu, Z.; Zhou, W.; Zhao, L.; Chen, J.; Meng, Y.; Wang, J.; Lin, Y.; Yuan, J.; Xie, Z.; Ma, J.; Liu, W.J.; Wang, D.; Xu, W.; Holmes, E.C.; Gao, G.F.; Wu, G.; Chen, W.; Shi, W.; Tan, W. Genomic characterisation and epidemiology of 2019 novel coronavirus: Implications for virus origins and receptor binding. Lancet, 2020, 395(10224), 565-574.
[http://dx.doi.org/10.1016/S0140-6736(20)30251-8] [PMID: 32007145]
[45]
McNamara, R.P. High-density amplicon sequencing identifies community spread and ongoing evolution of SARS-CoV-2 in the Southern United States. bioRxiv, 2020, 33(5), 108352.
[46]
Pallesen, J.; Wang, N.; Corbett, K.S.; Wrapp, D.; Kirchdoerfer, R.N.; Turner, H.L.; Cottrell, C.A.; Becker, M.M.; Wang, L.; Shi, W.; Kong, W.P.; Andres, E.L.; Kettenbach, A.N.; Denison, M.R.; Chappell, J.D.; Graham, B.S.; Ward, A.B.; McLellan, J.S. Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. Proc. Natl. Acad. Sci. USA, 2017, 114(35), E7348-E7357.
[http://dx.doi.org/10.1073/pnas.1707304114] [PMID: 28807998]
[47]
Shang, J.; Ye, G.; Shi, K.; Wan, Y.; Luo, C.; Aihara, H.; Geng, Q.; Auerbach, A. Structural basis of receptor recognition by SARS-CoV-2. Nature, 2020, 581, 221-224.
[48]
Pan, Y.; Zhang, D.; Yang, P.; Poon, L.L.M.; Wang, Q. Viral load of SARS-CoV-2 in clinical samples. Lancet Infect. Dis., 2020, 20(4), 411-412.
[http://dx.doi.org/10.1016/S1473-3099(20)30113-4] [PMID: 32105638]
[49]
Zheng, S.; Fan, J.; Yu, F.; Feng, B.; Lou, B.; Zou, Q.; Xie, G.; Lin, S.; Wang, R.; Yang, X.; Chen, W.; Wang, Q.; Zhang, D.; Liu, Y.; Gong, R.; Ma, Z.; Lu, S.; Xiao, Y.; Gu, Y.; Zhang, J.; Yao, H.; Xu, K.; Lu, X.; Wei, G.; Zhou, J.; Fang, Q.; Cai, H.; Qiu, Y.; Sheng, J.; Chen, Y.; Liang, T. Viral load dynamics and disease severity in patients infected with SARS-CoV-2 in Zhejiang province, China, January-March 2020: Retrospective cohort study. BMJ, 2020, 369, m1443.
[http://dx.doi.org/10.1136/bmj.m1443] [PMID: 32317267]
[50]
Yu, F.; Yan, L.; Wang, N.; Yang, S.; Wang, L.; Tang, Y.; Gao, G.; Wang, S.; Ma, C.; Xie, R.; Wang, F.; Tan, C.; Zhu, L.; Guo, Y.; Zhang, F. Quantitative detection and viral load analysis of SARS-CoV-2 in infected patients. Clin. Infect. Dis., 2020, 71(15), 793-798.
[http://dx.doi.org/10.1093/cid/ciaa345] [PMID: 32221523]
[51]
Lan, J.; Ge, J.; Yu, J.; Shan, S.; Zhou, H.; Fan, S.; Zhang, Q.; Shi, X.; Wang, Q.; Zhang, L. Crystal structure of the 2019-nCoV spike receptor-binding domain bound with the ACE2 receptor. Nature, 2020, 581(7807), 215-220.
[http://dx.doi.org/10.1038/s41586-020-2180-5] [PMID: 32225176]
[52]
Shao, S.; Xu, Q.; Yu, X.; Pan, R.; Chen, Y. Dipeptidyl peptidase 4 inhibitors and their potential immune modulatory functions. Pharmacol. Ther., 2020, 209, 107503.
[http://dx.doi.org/10.1016/j.pharmthera.2020.107503] [PMID: 32061923]
[53]
Song, W.; Wang, Y.; Wang, N.; Wang, D.; Guo, J.; Fu, L.; Shi, X. Identification of residues on human receptor DPP4 critical for MERSCoV binding and entry. Virology, 2014, 471-473, 49-53.
[http://dx.doi.org/10.1016/j.virol.2014.10.006] [PMID: 25461530]
[54]
Wang, N.; Shi, X.; Jiang, L.; Zhang, S.; Wang, D.; Tong, P.; Guo, D.; Fu, L.; Cui, Y.; Liu, X.; Arledge, K.C.; Chen, Y.H.; Zhang, L.; Wang, X. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res., 2013, 23(8), 986-993.
[http://dx.doi.org/10.1038/cr.2013.92] [PMID: 23835475]
[55]
Rubino, F.; Amiel, S.A.; Zimmet, P.; Alberti, G.; Bornstein, S.; Eckel, R.H.; Mingrone, G.; Boehm, B.; Cooper, M.E.; Chai, Z.; Del Prato, S.; Ji, L.; Hopkins, D.; Herman, W.H.; Khunti, K.; Mbanya, J.C.; Renard, E. New-onset diabetes in COVID-19. N. Engl. J. Med., 2020, 383(8), 789-790.
[http://dx.doi.org/10.1056/NEJMc2018688] [PMID: 32530585]
[56]
De Beeck, O.A.; Eizirik, D.L. Viral infections in type 1 diabetes mellitus — Why the β cells? Nat. Rev. Endocrinol., 2016, 12(5), 263-273.
[http://dx.doi.org/10.1038/nrendo.2016.30] [PMID: 27020257]
[57]
Yang, L.; Han, Y.; Nilsson, P.B.E.; Gupta, V.; Wang, P.; Duan, X.; Tang, X.; Zhu, J.; Zhao, Z.; Jaffré, F.; Zhang, T.; Kim, T.W.; Harschnitz, O.; Redmond, D.; Houghton, S.; Liu, C.; Naji, A.; Ciceri, G.; Guttikonda, S.; Bram, Y.; Nguyen, D.H.T.; Cioffi, M.; Chandar, V.; Hoagland, D.A.; Huang, Y.; Xiang, J.; Wang, H.; Lyden, D.; Borczuk, A.; Chen, H.J.; Studer, L.; Pan, F.C.; Ho, D.D.; TenOever, B.R.; Evans, T.; Schwartz, R.E.; Chen, S. A human pluripotent stem cellbased platform to study SARS-CoV-2 tropism and model virus infection in human cells and organoids. Cell Stem Cell, 2020, 27(1), 125-136.e7.
[http://dx.doi.org/10.1016/j.stem.2020.06.015] [PMID: 32579880]
[58]
Tymecka, D.; Puszko, A.K. Lipiński, P.F.J.; Fedorczyk, B.; Wilenska,B.; Sura, K.; Perret, G.Y.; Misicka, A. Branched pentapeptides as potent inhibitors of the vascular endothelial growth factor 165 binding to Neuropilin-1: Design, synthesis and biological activity. Eur. J. Med. Chem., 2018, 158, 453-462.
[http://dx.doi.org/10.1016/j.ejmech.2018.08.083] [PMID: 30241012]
[59]
Mota, F.; Yelland, T.; Hutton, J.A.; Parker, J.; Patsiarika, A.; Chan, A.W.E.; O’Leary, A.; Fotinou, C.; Martin, J.F.; Zachary, I.C.; Djordjevic, S.; Frankel, P.; Selwood, D.L. Peptides derived from vascular endothelial growth factor B show potent binding to neuropilin‐1. Chem. Bio. Chem., 2022, 23(1), e202100463.
[http://dx.doi.org/10.1002/cbic.202100463] [PMID: 34647407]
[60]
Domingues, A.; Fantin, A. Neuropilin 1 regulation of vascular permeability signaling. Biomolecules, 2021, 11(5), 666.
[http://dx.doi.org/10.3390/biom11050666] [PMID: 33947161]
[61]
Hoffmann, M.; Arora, P.; Groß, R.; Seidel, A.; Hörnich, B.F.; Hahn, A.S.; Krüger, N.; Graichen, L.; Hofmann-Winkler, H.; Kempf, A.; Winkler, M.S.; Schulz, S.; Jäck, H.M.; Jahrsdörfer, B.; Schrezenmeier, H.; Müller, M.; Kleger, A.; Münch, J.; Pöhlmann, S. SARS-CoV-2 variants B.1.351 and P.1 escape from neutralizing antibodies. Cell, 2021, 184(9), 2384-2393.
[http://dx.doi.org/10.1016/j.cell.2021.03.036] [PMID: 33794143]
[62]
Keicchiro, M. SARS-CoV-2 infection and pancreatic β cell failure. Biology, 2021, 11(1), 22.
[63]
Gupta, A.; Madhavan, M.V.; Sehgal, K.; Nair, N.; Mahajan, S.; Sehrawat, T.S.; Bikdeli, B.; Ahluwalia, N.; Ausiello, J.C.; Wan, E.Y.; Freedberg, D.E.; Kirtane, A.J.; Parikh, S.A.; Maurer, M.S.; Nordvig, A.S.; Accili, D.; Bathon, J.M.; Mohan, S.; Bauer, K.A.; Leon, M.B.; Krumholz, H.M.; Uriel, N.; Mehra, M.R.; Elkind, M.S.V.; Stone, G.W.; Schwartz, A.; Ho, D.D.; Bilezikian, J.P.; Landry, D.W. Extrapulmonary manifestations of COVID-19. Nat. Med., 2020, 26(7), 1017-1032.
[http://dx.doi.org/10.1038/s41591-020-0968-3] [PMID: 32651579]
[64]
Wolff, D.; Nee, S.; Hickey, N.S.; Marschollek, M. Risk factors for COVID-19 severity and fatality: A structured literature review. Infection, 2021, 49(1), 15-28.
[http://dx.doi.org/10.1007/s15010-020-01509-1] [PMID: 32860214]
[65]
Azushima, K.; Morisawa, N.; Tamura, K.; Nishiyama, A. Recent research advances in renin angiotensin aldosterone system receptors. Curr. Hypertens. Rep., 2020, 22(3), 22.
[http://dx.doi.org/10.1007/s11906-020-1028-6] [PMID: 32114685]
[66]
Coutard, B.; Valle, C.; De Lamballerie, X.; Canard, B.; Seidah, N.G.; Decroly, E. The spike glycoprotein of the new coronavirus 2019-nCoV contains a furin-like cleavage site absent in CoV of the same clade. Antiviral Res., 2020, 176, 104742.
[http://dx.doi.org/10.1016/j.antiviral.2020.104742] [PMID: 32057769]
[67]
Kustmerseva, I.; Wu, W.; Syed, F.; Der Heide, V.; Jorgensen, M.; Joseph, P. Expression of SARS-CoV-2 entry factors in the pancreas of normal organ donors and individuals with COVID-19. Cell Metab., 2020, 32(6), 1028-1040.
[PMID: 33207245]
[68]
Chang, T.T.; Chen, J.W. Emerging role of chemokine CC motif ligand 4 related mechanisms in diabetes mellitus and cardiovascular disease: Friends or foes? Cardiovasc. Diabetol., 2016, 15(1), 117.
[http://dx.doi.org/10.1186/s12933-016-0439-9] [PMID: 27553774]
[69]
Chen, Y.L.; Qiao, Y.C.; Pan, Y.H.; Xu, Y.; Huang, Y.C.; Wang, Y.H.; Geng, L.J.; Zhao, H.L.; Zhang, X.X. Correlation between serum interleukin-6 level and type 1 diabetes mellitus: A systematic review and meta-analysis. Cytokine, 2017, 94, 14-20.
[http://dx.doi.org/10.1016/j.cyto.2017.01.002] [PMID: 28283222]
[70]
Pan, X.; Kaminga, A.C.; Kinra, S.; Wen, S.W.; Liu, H.; Tan, X.; Liu, A. Chemokines in type 1 diabetes mellitus. Front. Immunol., 2022, 12, 690082.
[http://dx.doi.org/10.3389/fimmu.2021.690082] [PMID: 35242125]
[71]
Thomas, N.J.; Jones, S.E.; Weedon, M.N.; Shields, B.M.; Oram, R.A.; Hattersley, A.T. Frequency and phenotype of type 1 diabetes in the first six decades of life: A cross-sectional, genetically stratified survival analysis from UK Biobank. Lancet Diabetes Endocrinol., 2018, 6(2), 122-129.
[http://dx.doi.org/10.1016/S2213-8587(17)30362-5] [PMID: 29199115]
[72]
Schulte, B.M.; Bakkers, J.; Lanke, K.H.W.; Melchers, W.J.G.; Westerlaken, C.; Allebes, W.; Aanstoot, H.J.; Bruining, G.J.; Adema, G.J.; Van Kuppeveld, F.J.M.; Galama, J.M.D. Detection of enterovirus RNA in peripheral blood mononuclear cells of type 1 diabetic patients beyond the stage of acute infection. Viral Immunol., 2010, 23(1), 99-104.
[http://dx.doi.org/10.1089/vim.2009.0072] [PMID: 20121407]
[73]
Ifie, E.; Russell, M.A.; Dhayal, S.; Leete, P.; Sebastiani, G.; Nigi, L.; Dotta, F.; Marjomäki, V.; Eizirik, D.L.; Morgan, N.G.; Richardson, S.J. Unexpected subcellular distribution of a specific isoform of the coxsackie and adenovirus receptor, CAR-SIV, in human pancreatic β-cells. Diabetologia, 2018, 61(11), 2344-2355.
[http://dx.doi.org/10.1007/s00125-018-4704-1] [PMID: 30074059]
[74]
Vehik, K.; Lynch, K.F.; Wong, M.C.; Tian, X.; Ross, M.C.; Gibbs, R.A.; Ajami, N.J.; Petrosino, J.F.; Rewers, M.; Toppari, J.; Ziegler, A.G.; She, J.X.; Lernmark, A.; Akolkar, B.; Hagopian, W.A.; Schatz, D.A.; Krischer, J.P.; Hyöty, H.; Lloyd, R.E. Prospective virome analyses in young children at increased genetic risk for type 1 diabetes. Nat. Med., 2019, 25(12), 1865-1872.
[http://dx.doi.org/10.1038/s41591-019-0667-0] [PMID: 31792456]
[75]
Richardson, S.J.; Willcox, A.; Bone, A.J.; Foulis, A.K.; Morgan, N.G. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia, 2009, 52(6), 1143-1151.
[http://dx.doi.org/10.1007/s00125-009-1276-0] [PMID: 19266182]
[76]
Patterson, C.C.; Harjutsalo, V.; Rosenbauer, J.; Neu, A.; Cinek, O.; Skrivarhaug, T.; Rami, M.B.; Soltesz, G.; Svensson, J.; Parslow, R.C.; Castell, C.; Schoenle, E.J.; Bingley, P.J.; Dahlquist, G.; Jarosz, C.P.K. Marčiulionytė, D.; Roche, E.F.; Rothe, U.; Bratina, N.; Ionescu, T.C.; Weets, I.; Kocova, M.; Cherubini, V.; Rojnic, P.N.; deBeaufort, C.E.; Samardzic, M.; Green, A. Trends and cyclical variation in the incidence of childhood type 1 diabetes in 26 European centres in the 25 year period 1989–2013: A multicentre prospective registration study. Diabetologia, 2019, 62(3), 408-417.
[http://dx.doi.org/10.1007/s00125-018-4763-3] [PMID: 30483858]
[77]
Lamb, M.M.; Miller, M.; Seifert, J.A.; Frederiksen, B.; Kroehl, M.; Rewers, M.; Norris, J.M. The effect of childhood cow’s milk intake and HLA-DR genotype on risk of islet autoimmunity and type 1 diabetes: The diabetes autoimmunity study in the young. Pediatr. Diabetes, 2015, 16(1), 31-38.
[http://dx.doi.org/10.1111/pedi.12115] [PMID: 24444005]
[78]
Koivusaari, K.; Syrjälä, E.; Niinistö, S.; Takkinen, H.M.; Ahonen, S.; Åkerlund, M.; Korhonen, T.E.; Toppari, J.; Ilonen, J.; Peltonen, J.; Nevalainen, J.; Knip, M.; Alatossava, T.; Veijola, R.; Virtanen, S.M. Consumption of differently processed milk products in infancy and early childhood and the risk of islet autoimmunity. Br. J. Nutr., 2020, 124(2), 173-180.
[http://dx.doi.org/10.1017/S0007114520000744] [PMID: 32102698]
[79]
Steenblock, C.; Schwarz, P.E.H.; Ludwig, B.; Linkermann, A.; Zimmet, P.; Kulebyakin, K.; Tkachuk, V.A.; Markov, A.G.; Lehnert, H.; De Angelis, M.H.; Rietzsch, H.; Rodionov, R.N.; Khunti, K.; Hopkins, D.; Birkenfeld, A.L.; Boehm, B.; Holt, R.I.G.; Skyler, J.S.; DeVries, J.H.; Renard, E.; Eckel, R.H.; Alberti, K.G.M.M.; Geloneze, B.; Chan, J.C.; Mbanya, J.C.; Onyegbutulem, H.C.; Ramachandran, A.; Basit, A.; Hassanein, M.; Bewick, G.; Spinas, G.A.; Beuschlein, F.; Landgraf, R.; Rubino, F.; Mingrone, G.; Bornstein, S.R. COVID-19 and metabolic disease: Mechanisms and clinical management. Lancet Diabetes Endocrinol., 2021, 9(11), 786-798.
[http://dx.doi.org/10.1016/S2213-8587(21)00244-8] [PMID: 34619105]
[80]
Fignani, D.; Licata, G.; Brusco, N.; Nigi, L.; Grieco, G.E.; Marselli, L.; Overbergh, L.; Gysemans, C.; Colli, M.L.; Marchetti, P.; Mathieu, C.; Eizirik, D.L.; Sebastiani, G.; Dotta, F. SARS-CoV-2 receptor Angiotensin I-Converting Enzyme Type 2 (ACE2) is expressed in human pancreatic β-cells and in the human pancreas microvasculature. Front. Endocrinol., 2020, 11, 596898.
[http://dx.doi.org/10.3389/fendo.2020.596898] [PMID: 33281748]
[81]
Liu, F.; Long, X.; Zhang, B.; Zhang, W.; Chen, X.; Zhang, Z. ACE2 expression in pancreas may cause pancreatic damage after SARSCoV-2 infection. Clin. Gastroenterol. Hepatol., 2020, 18(9), 2128-2130.e2.
[http://dx.doi.org/10.1016/j.cgh.2020.04.040] [PMID: 32334082]
[82]
Kumar, A.; Faiq, M.A.; Pareek, V.; Raza, K.; Narayan, R.K.; Prasoon, P.; Kumar, P.; Kulandhasamy, M.; Kumari, C.; Kant, K.; Singh, H.N.; Qadri, R.; Pandey, S.N.; Kumar, S. Relevance of SARS-CoV-2 related factors ACE2 and TMPRSS2 expressions in gastrointestinal tissue with pathogenesis of digestive symptoms, diabetes-associated mortality, and disease recurrence in COVID-19 patients. Med. Hypotheses, 2020, 144, 110271.
[http://dx.doi.org/10.1016/j.mehy.2020.110271] [PMID: 33254575]
[83]
Esguerra, J.L.S.; Ofori, J.K.; Nagao, M.; Shuto, Y.; Karagiannopoulos, A.; Fadista, J.; Sugihara, H.; Groop, L.; Eliasson, L. Glucocorticoid induces human beta cell dysfunction by involving riborepressor GAS5 LincRNA. Mol. Metab., 2020, 32, 160-167.
[http://dx.doi.org/10.1016/j.molmet.2019.12.012] [PMID: 32029226]
[84]
Lei, C.; Qian, K.; Li, T.; Zhang, S.; Fu, W.; Ding, M.; Hu, S. Neutralization of SARS-CoV-2 spike pseudotyped virus by recombinant ACE2-Ig. Nat. Commun., 2020, 11(1), 2070.
[http://dx.doi.org/10.1038/s41467-020-16048-4] [PMID: 32332765]

Rights & Permissions Print Cite
Article Metrics
32
2
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy