Enteroviruses and the pathogenesis of type 1 diabetes revisited: Cross-reactivity of enterovirus capsid protein (VP1) antibodies with human mitochondrial proteins

Journal of Pathology

Volumn 229, Issue 5, 2013, Pages 719-728

  Hansson, Sara F ^a   Korsgren, Stella ^b   Pontén, Fredrik ^b   Korsgren, Olle ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

ATP synthase beta subunit; creatine kinase B type; enterovirus; immunohistochemistry; proteomics; type 1 diabetes; viral peptide 1

Indexed keywords

CREATINE KINASE; MITOCHONDRIAL ENZYME; MITOCHONDRIAL PROTEIN; PROTEIN VP1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AMINO ACID SEQUENCE; ARTICLE; CONNECTIVE TISSUE; CROSS REACTION; ENTEROVIRUS; EPITHELIUM CELL; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LIVER CELL; MASS SPECTROMETRY; MITOCHONDRION; ONCOCYTOMA; PATHOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SALIVARY GLAND TUMOR; SKELETAL MUSCLE; TWO DIMENSIONAL GEL ELECTROPHORESIS; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ANTIBODIES; ARTIFACTS; BLOTTING, WESTERN; CAPSID PROTEINS; CREATINE KINASE; CROSS REACTIONS; DIABETES MELLITUS, TYPE 1; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; ISLETS OF LANGERHANS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; PROTEOMICS; REPRODUCIBILITY OF RESULTS; TANDEM MASS SPECTROMETRY; TISSUE CULTURE TECHNIQUES;

EID: 84875040157     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4166     Document Type: Article

References (49)

1. Patterson CC, Dahlquist GG, Gyurus E, et al,. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet 2009; 373: 2027-2033.
2. Yoon JW, Austin M, Onodera T, et al,. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N Engl J Med 1979; 300: 1173-1179.
3. King ML, Shaikh A, Bidwell D, et al,. Coxsackie-B-virus-specific IgM responses in children with insulin-dependent (juvenile-onset; type I) diabetes mellitus. Lancet 1983; 1: 1397-1399.
4. Foulis AK, McGill M, Farquharson MA, et al,. A search for evidence of viral infection in pancreases of newly diagnosed patients with IDDM. Diabetologia 1997; 40: 53-61.
5. Ylipaasto P, Klingel K, Lindberg AM, et al,. Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 2004; 47: 225-239.
6. Green J, Casabonne D, Newton R,. Coxsackie B virus serology and type 1 diabetes mellitus: a systematic review of published case-control studies. Diabet Med 2004; 21: 507-514.
7. Dotta F, Censini S, van Halteren AG, et al,. Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci U S A 2007; 104: 5115-5120.
8. Stene LC, Oikarinen S, Hyoty H, et al,. Enterovirus infection and progression from islet autoimmunity to type 1 diabetes: the Diabetes and Autoimmunity Study in the Young (DAISY). Diabetes 2010; 59: 3174-3180.
9. Oikarinen S, Martiskainen M, Tauriainen S, et al,. Enterovirus RNA in blood is linked to the development of type 1 diabetes. Diabetes 2011; 60: 276-279.
10. Oikarinen M, Tauriainen S, Oikarinen S, et al,. Type 1 diabetes is associated with enterovirus infection in gut mucosa. Diabetes 2012; 61: 687-691.
11. Simonen-Tikka ML, Pflueger M, Klemola P, et al,. Human enterovirus infections in children at increased risk for type 1 diabetes: the Babydiet study. Diabetologia 2011; 54: 2995-3002.
12. Tracy S, Drescher KM, Chapman NM,. Enteroviruses and type 1 diabetes. Diabetes Metab Res Rev 2011; 27: 820-823.
13. Yeung WC, Rawlinson WD, Craig ME,. Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 2011; 342: d35.
14. Yousef GE, Brown IN, Mowbray JF,. Derivation and biochemical characterization of an enterovirus group-specific monoclonal antibody. Intervirology 1987; 28: 163-170.
15. Oberste MS, Maher K, Kilpatrick DR, et al,. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 1999; 73: 1941-1948.
16. Roivainen M, Klingel K,. Role of enteroviruses in the pathogenesis of type 1 diabetes. Diabetologia 2009; 52: 995-996.
17. Samuelson A, Forsgren M, Sallberg M,. Characterization of the recognition site and diagnostic potential of an enterovirus group-reactive monoclonal antibody. Clin Diagn Lab Immunol 1995; 2: 385-386.
18. Flodstrom M, Maday A, Balakrishna D, et al,. Target cell defense prevents the development of diabetes after viral infection. Nature Immunol 2002; 3: 373-382.
19. Flodstrom-Tullberg M, Hultcrantz M, Stotland A, et al,. RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection. J Immunol 2005; 174: 1171-1177.
20. Aida K, Nishida Y, Tanaka S, et al,. RIG-I- and MDA5-initiated innate immunity linked with adaptive immunity accelerates beta-cell death in fulminant type 1 diabetes. Diabetes 2011; 60: 884-889.
21. Drescher KM, Kono K, Bopegamage S, et al,. Coxsackievirus B3 infection and type 1 diabetes development in NOD mice: insulitis determines susceptibility of pancreatic islets to virus infection. Virology 2004; 329: 381-394.
22. Kobayashi T, Nishida Y, Tanaka S, et al,. Pathological changes in the pancreas of fulminant type 1 diabetes and slowly progressive insulin-dependent diabetes mellitus (SPIDDM): innate immunity in fulminant type 1 diabetes and SPIDDM. Diabetes Metab Res Rev 2011; 27: 965-970.
23. Bopegamage S, Kovacova J, Vargova A, et al,. Coxsackie B virus infection of mice: inoculation by the oral route protects the pancreas from damage, but not from infection. J Gen Virol 2005; 86: 3271-3280.
24. Richardson SJ, Willcox A, Bone AJ, et al,. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 2009; 52: 1143-1151.
25. Willcox A, Richardson SJ, Bone AJ, et al,. Immunohistochemical analysis of the relationship between islet cell proliferation and the production of the enteroviral capsid protein, VP1, in the islets of patients with recent-onset type 1 diabetes. Diabetologia 2011; 54: 2417-2420.
26. Richardson SJ, Leete P, Bone AJ, et al,. Expression of the enteroviral capsid protein VP1 in the islet cells of patients with type 1 diabetes is associated with induction of protein kinase R and downregulation of Mcl-1. Diabetologia 2013; 56: 185-193.
27. Oikarinen M, Tauriainen S, Honkanen T, et al,. Analysis of pancreas tissue in a child positive for islet cell antibodies. Diabetologia 2008; 51: 1796-1802.
28. Horwitz MS, Ilic A, Fine C, et al,. Coxsackieviral-mediated diabetes: induction requires antigen-presenting cells and is accompanied by phagocytosis of beta cells. Clin Immunol 2004; 110: 134-144.
29. Tanaka S, Nishida Y, Aida K, et al,. Enterovirus infection, CXC chemokine ligand 10 (CXCL10), and CXCR3 circuit: a mechanism of accelerated beta-cell failure in fulminant type 1 diabetes. Diabetes 2009; 58: 2285-2291.
30. Goto M, Eich TM, Felldin M, et al,. Refinement of the automated method for human islet isolation and presentation of a closed system for in vitro islet culture. Transplantation 2004; 78: 1367-1375.
31. Friberg AS, Brandhorst H, Buchwald P, et al,. Quantification of the islet product: presentation of a standardized current good manufacturing practices compliant system with minimal variability. Transplantation 2011; 91: 677-683.
32. Bordier C., Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 1981; 256: 1604-1607.
33. Shevchenko A, Wilm M, Vorm O, et al,. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996; 68: 850-858.
34. Carlsohn E, Nystrom J, Karlsson H, et al. Characterization of the outer membrane protein profile from disease-related Helicobacter pylori isolates by subcellular fractionation and nano-LC FT-ICR MS analysis. J Proteome Res 2006; 5: 3197-3204.
35. Moell A, Skog O, Ahlin E, et al,. Antiviral effect of nicotinamide on enterovirus-infected human islets in vitro: effect on virus replication and chemokine secretion. J Med Virol 2009; 81: 1082-1087.
36. Izquierdo JM,. Control of the ATP synthase beta subunit expression by RNA-binding proteins TIA-1, TIAR, and HuR. Biochem Biophys Res Commun 2006; 348: 703-711.
37. Kohnke R, Mei J, Park M, et al,. Fatty acids and glucose in high concentration down-regulates ATP synthase beta-subunit protein expression in INS-1 cells. Nutr Neurosci 2007; 10: 273-278.
38. Bessman SP, Carpenter CL,. The creatine-creatine phosphate energy shuttle. Annu Rev Biochem 1985; 54: 831-862.
39. Bong SM, Moon JH, Jang EH, et al,. Overexpression, purification, and preliminary X-ray crystallographic analysis of human brain-type creatine kinase. J Microbiol Biotechnol 2008; 18: 295-298.
40. Wallimann T, Wyss M, Brdiczka D, et al,. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem J 1992; 281: 21-40.
41. Harkonen T, Lankinen H, Davydova B, et al,. Enterovirus infection can induce immune responses that cross-react with beta-cell autoantigen tyrosine phosphatase IA-2/IAR. J Med Virol 2002; 66: 340-350.
42. Harkonen T, Puolakkainen M, Sarvas M, et al,. Picornavirus proteins share antigenic determinants with heat shock proteins 60/65. J Med Virol 2000; 62: 383-391.
43. Hjelm B, Fernandez CD, Lofblom J, et al,. Exploring epitopes of antibodies toward the human tryptophanyl-tRNA synthetase. N Biotechnol 2010; 27: 129-137.
44. Higa M, Zhou YT, Ravazzola M, et al,. Troglitazone prevents mitochondrial alterations, beta cell destruction, and diabetes in obese prediabetic rats. Proc Natl Acad Sci U S A 1999; 96: 11513-11518.
45. Lu H, Koshkin V, Allister EM, et al,. Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes 2010; 59: 448-459.
46. Dlaskova A, Spacek T, Santorova J, et al,. 4Pi microscopy reveals an impaired three-dimensional mitochondrial network of pancreatic islet beta-cells, an experimental model of type-2 diabetes. Biochim Biophys Acta 2010; 1797: 1327-1341.
47. Molina AJ, Wikstrom JD, Stiles L, et al,. Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 2009; 58: 2303-2315.
48. Andreoletti L, Bourlet T, Moukassa D, et al,. Enteroviruses can persist with or without active viral replication in cardiac tissue of patients with end-stage ischemic or dilated cardiomyopathy. J Infect Dis 2000; 182: 1222-1227.
49. Triantafyllopoulou A, Tapinos N, Moutsopoulos HM,. Evidence for coxsackievirus infection in primary Sjögren's syndrome. Arthritis Rheum 2004; 50: 2897-2902.