Beta cells under attack: Toward a better understanding of type 1 diabetes immunopathology

Seminars in Immunopathology

Volumn 33, Issue 1, 2011, Pages 1-7

  Coppieters, Ken T ^a   Roep, Bart O ^b   Von Herrath, Matthias G ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INTERLEUKIN 10; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ANTIGEN ANTIBODY COMPLEX; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL REGENERATION; CELL TRANSPLANTATION; CELLULAR IMMUNITY; CLINICAL FEATURE; DIABETOGENESIS; DISEASE MODEL; DOSE RESPONSE; DRUG DOSE REDUCTION; DRUG MECHANISM; ENTEROVIRUS INFECTION; ENVIRONMENTAL FACTOR; EXPERIMENTAL MOUSE; GENE EXPRESSION REGULATION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNOPATHOGENESIS; IMMUNOPATHOLOGY; IMMUNOREGULATION; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; LOW DRUG DOSE; LYMPHOCYTIC INFILTRATION; NONHUMAN; NONMYELOABLATIVE CONDITIONING; NOTE; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REPEATED DRUG DOSE; T LYMPHOCYTE SUBPOPULATION; TREATMENT DURATION; VIRUS CELL INTERACTION; VIRUS PATHOGENESIS;

ANIMALS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; HUMANS; INSULIN-SECRETING CELLS; T-LYMPHOCYTES;

EID: 79251609686     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-010-0236-6     Document Type: Note

References (50)

1. W Gepts 1965 Pathologic anatomy of the pancreas in juvenile diabetes mellitus Diabetes 14 10 619 633 1:STN:280:DyaF28%2FgvF2isQ%3D%3D 5318831
2. R Hilbrands VA Huurman P Gillard JH Velthuis M De Waele C Mathieu, et al. 2009 Differences in baseline lymphocyte counts and autoreactivity are associated with differences in outcome of islet cell transplantation in type 1 diabetic patients Diabetes 58 10 2267 2276 1:CAS:528:DC%2BD1MXht1yku7bO 10.2337/db09-0160 19602536 PMCID: 2750206
3. BO Roep I Stobbe G Duinkerken JJ van Rood A Lernmark B Keymeulen, et al. 1999 Auto- and alloimmune reactivity to human islet allografts transplanted into type 1 diabetic patients Diabetes 48 3 484 490 1:CAS:528:DyaK1MXhsFymsbg%3D 10.2337/diabetes.48.3.484 10078547
4. T Hanafusa A Miyazaki J Miyagawa S Tamura M Inada K Yamada, et al. 1990 Examination of islets in the pancreas biopsy specimens from newly diagnosed type 1 (insulin-dependent) diabetic patients Diabetologia 33 2 105 111 1:STN:280:DyaK3c3ivVKiuw%3D%3D 10.1007/BF00401048 1691724
5. N Itoh T Hanafusa A Miyazaki J Miyagawa K Yamagata K Yamamoto, et al. 1993 Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients J Clin Invest 92 5 2313 2322 1:CAS:528:DyaK2cXivFWqtQ%3D%3D 10.1172/JCI116835 8227346 PMCID: 288412
6. AK Foulis CN Liddle MA Farquharson JA Richmond RS Weir 1986 The histopathology of the pancreas in type 1 (insulin-dependent) diabetes mellitus: a 25-year review of deaths in patients under 20 years of age in the United Kingdom Diabetologia 29 5 267 274 1:STN:280:DyaL283kvVCgtw%3D%3D 10.1007/BF00452061 3522324
7. A Willcox SJ Richardson AJ Bone AK Foulis NG Morgan 2009 Analysis of islet inflammation in human type 1 diabetes Clin Exp Immunol 155 2 173 181 1:STN:280:DC%2BD1M%2FlslKltw%3D%3D 10.1111/j.1365-2249.2008.03860.x 19128359 PMCID: 2675247
8. P In't Veld D Lievens J De Grijse Z Ling B Van der Auwera M Pipeleers-Marichal, et al. 2007 Screening for insulitis in adult autoantibody-positive organ donors Diabetes 56 9 2400 2404 10.2337/db07-0416 17563060 (Pubitemid 47358248)
9. M von Herrath S Sanda K Herold 2007 Type 1 diabetes as a relapsing-remitting disease? Nat Rev Immunol 7 12 988 994 10.1038/nri2192 (Pubitemid 350166057)
10. R Gianani M Campbell-Thompson SA Sarkar C Wasserfall A Pugliese JM Solis, et al. 2010 Dimorphic histopathology of long-standing childhood-onset diabetes Diabetologia 53 4 690 698 1:STN:280:DC%2BC3c7nsF2mtg%3D%3D 10.1007/s00125-009- 1642-y 20062967
11. HA Keenan JK Sun J Levine A Doria LP Aiello G Eisenbarth, et al. 2010 Residual insulin production and pancreatic beta cell turnover after 50 years of diabetes: Joslin Medalist Study Diabetes 59 11 2846 2853 1:CAS:528: DC%2BC3cXhsV2nsb%2FL 10.2337/db10-0676 20699420
12. NA Sherry JA Kushner M Glandt T Kitamura AM Brillantes KC Herold 2006 Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes Diabetes 55 12 3238 3245 1:CAS:528:DC%2BD28XhtlSmsLbK 10.2337/db05-1034 17130466 (Pubitemid 44923579)
13. A Willcox SJ Richardson AJ Bone AK Foulis NG Morgan 2010 Evidence of increased islet cell proliferation in patients with recent-onset type 1 diabetes Diabetologia 53 9 2020 2028 1:CAS:528:DC%2BC3cXpsV2ltb4%3D 10.1007/s00125-010- 1817-6 20532863
14. F Souza N Simpson A Raffo C Saxena A Maffei M Hardy, et al. 2006 Longitudinal noninvasive PET-based beta cell mass estimates in a spontaneous diabetes rat model J Clin Invest 116 6 1506 1513 1:CAS:528:DC%2BD28XlsFWrtLg%3D 10.1172/JCI27645 16710474 PMCID: 1462946
15. SM Lieberman T Takaki B Han P Santamaria DV Serreze TP DiLorenzo 2004 Individual nonobese diabetic mice exhibit unique patterns of CD8+ T cell reactivity to three islet antigens, including the newly identified widely expressed dystrophia myotonica kinase J Immunol 173 11 6727 6734 1:CAS:528:DC%2BD2cXhtVShsb%2FM 15557165
16. M Nakayama N Abiru H Moriyama N Babaya E Liu D Miao, et al. 2005 Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice Nature 435 7039 220 223 1:CAS:528:DC%2BD2MXktVWhtLg%3D 10.1038/nature03523 15889095 PMCID: 1364531 (Pubitemid 40685949)
17. JD Trudeau C Kelly-Smith CB Verchere JF Elliott JP Dutz DT Finegood, et al. 2003 Prediction of spontaneous autoimmune diabetes in NOD mice by quantification of autoreactive T cells in peripheral blood J Clin Invest 111 2 217 223 1:CAS:528:DC%2BD3sXlsVGrug%3D%3D 12531877 PMCID: 151866
18. E Enee E Martinuzzi P Blancou JM Bach R Mallone P van Endert 2008 Equivalent specificity of peripheral blood and islet-infiltrating CD8+ T lymphocytes in spontaneously diabetic HLA-A2 transgenic NOD mice J Immunol 180 8 5430 5438 1:CAS:528:DC%2BD1cXkt1artrw%3D 18390725
19. KC Herold B Brooks-Worrell J Palmer HM Dosch M Peakman P Gottlieb, et al. 2009 Validity and reproducibility of measurement of islet autoreactivity by T-cell assays in subjects with early type 1 diabetes Diabetes 58 11 2588 2595 1:CAS:528:DC%2BD1MXhsVCht77L 10.2337/db09-0249 19675135 PMCID: 2768166
20. JH Velthuis WW Unger JR Abreu G Duinkerken K Franken M Peakman, et al. 2010 Simultaneous detection of circulating autoreactive CD8+ T-cells specific for different islet cell-associated epitopes using combinatorial MHC multimers Diabetes 59 7 1721 1730 1:CAS:528:DC%2BC3cXpsVOls7g%3D 10.2337/db09-1486 20357361 PMCID: 2889772
21. JH Velthuis WW Unger AR van der Slik G Duinkerken M Engelse AF Schaapherder, et al. 2009 Accumulation of autoreactive effector T cells and allo-specific regulatory T cells in the pancreas allograft of a type 1 diabetic recipient Diabetologia 52 3 494 503 1:STN:280:DC%2BD1M7hs1GjsQ%3D%3D 10.1007/s00125-008-1237-z 19104770
22. T Brusko C Wasserfall K McGrail R Schatz HL Viener D Schatz, et al. 2007 No alterations in the frequency of FOXP3+ regulatory T-cells in type 1 diabetes Diabetes 56 3 604 612 1:CAS:528:DC%2BD2sXis12itrg%3D 10.2337/db06-1248 17327427 (Pubitemid 46348451)
23. TI Tree BO Roep M Peakman 2006 A mini meta-analysis of studies on CD4+CD25+ T cells in human type 1 diabetes: report of the Immunology of Diabetes Society T Cell Workshop Ann NY Acad Sci 1079 9 18 10.1196/annals.1375.002 17130526 (Pubitemid 44968695)
24. A Schneider M Rieck S Sanda C Pihoker C Greenbaum JH Buckner 2008 The effector T cells of diabetic subjects are resistant to regulation via CD4+ FOXP3+ regulatory T cells J Immunol 181 10 7350 7355 1:CAS:528: DC%2BD1cXhtlaisrnF 18981158 PMCID: 2597079
25. TI Tree J Lawson H Edwards A Skowera S Arif BO Roep, et al. 2010 Naturally arising human CD4 T-cells that recognize islet autoantigens and secrete interleukin-10 regulate proinflammatory T-cell responses via linked suppression Diabetes 59 6 1451 1460 1:CAS:528:DC%2BC3cXotFGkurg%3D 10.2337/db09-0503 20299476 PMCID: 2874706
26. Y Grinberg-Bleyer A Baeyens S You R Elhage G Fourcade S Gregoire, et al. 2010 IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells J Exp Med 207 9 1871 1878 1:CAS:528: DC%2BC3cXhtFensr3I 10.1084/jem.20100209 20679400
27. Q Tang JY Adams C Penaranda K Melli E Piaggio E Sgouroudis, et al. 2008 Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction Immunity 28 5 687 697 1:CAS:528:DC%2BD1cXmtlagt7s%3D 10.1016/j.immuni.2008.03.016 18468463 PMCID: 2394854
28. X Zhou SL Bailey-Bucktrout LT Jeker C Penaranda M Martinez-Llordella M Ashby, et al. 2009 Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo Nat Immunol 10 9 1000 1007 1:CAS:528:DC%2BD1MXovFylt7g%3D 10.1038/ni.1774 19633673 PMCID: 2729804
29. JC Voltarelli CE Couri AB Stracieri MC Oliveira DA Moraes F Pieroni, et al. 2007 Autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus JAMA 297 14 1568 1576 1:CAS:528:DC%2BD2sXktFeitL0%3D 10.1001/jama.297.14.1568 17426276 (Pubitemid 46588370)
30. S Sanda BO Roep M von Herrath 2008 Islet antigen specific IL-10+ immune responses but not CD4+CD25+FoxP3+ cells at diagnosis predict glycemic control in type 1 diabetes Clin Immunol 127 2 138 143 1:CAS:528:DC%2BD1cXks1alurg%3D 10.1016/j.clim.2007.12.003 18304876
31. A Kaas C Pfleger L Hansen K Buschard NC Schloot BO Roep, et al. 2010 Association of adiponectin, interleukin (IL)-1ra, inducible protein 10, IL-6 and number of islet autoantibodies with progression patterns of type 1 diabetes the first year after diagnosis Clin Exp Immunol 161 3 444 452 1:CAS:528: DC%2BC3cXhtFOkurfF 10.1111/j.1365-2249.2010.04193.x 20529086
32. BO Roep M Peakman 2010 Surrogate end points in the design of immunotherapy trials: emerging lessons from type 1 diabetes Nat Rev Immunol 10 2 145 152 1:CAS:528:DC%2BC3cXpslCqtQ%3D%3D 10.1038/nri2705 20098462
33. S Tanaka Y Nishida K Aida T Maruyama A Shimada M Suzuki, et al. 2009 Enterovirus infection, CXC chemokine ligand 10 (CXCL10), and CXCR3 circuit: a mechanism of accelerated beta-cell failure in fulminant type 1 diabetes Diabetes 58 10 2285 2291 1:CAS:528:DC%2BD1MXht1yku7bJ 10.2337/db09-0091 19641142 PMCID: 2750208
34. CM Filippi MG von Herrath 2008 Viral trigger for type 1 diabetes: pros and cons Diabetes 57 11 2863 2871 1:CAS:528:DC%2BD1MXhslejurY%3D 10.2337/db07-1023 18971433 PMCID: 2570378
35. V Harjutsalo L Sjoberg J Tuomilehto 2008 Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study Lancet 371 9626 1777 1782 10.1016/S0140-6736(08)60765-5 18502302 (Pubitemid 351697953)
36. S Adams 1926 The seasonal variation in the onset of acute diabetes Arch Intern Med 37 861 864
37. AK Foulis MA Farquharson A Meager 1987 Immunoreactive alpha-interferon in insulin-secreting beta cells in type 1 diabetes mellitus Lancet 2 8573 1423 1427 1:STN:280:DyaL1c%2Fptlalug%3D%3D 10.1016/S0140-6736(87)91128-7 2891993
38. F Dotta S Censini AG van Halteren L Marselli M Masini S Dionisi, et al. 2007 Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients Proc Natl Acad Sci USA 104 12 5115 5120 1:CAS:528:DC%2BD2sXjvFChu7o%3D 10.1073/pnas.0700442104 17360338 PMCID: 1829272 (Pubitemid 47186185)
39. SJ Richardson A Willcox AJ Bone AK Foulis NG Morgan 2009 The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes Diabetologia 52 6 1143 1151 1:CAS:528:DC%2BD1MXlt1Gqu70%3D 10.1007/s00125-009-1276-0 19266182
40. DJ Smyth JD Cooper R Bailey S Field O Burren LJ Smink, et al. 2006 A genome-wide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferon-induced helicase (IFIH1) region Nat Genet 38 6 617 619 1:CAS:528:DC%2BD28XltVOhur4%3D 10.1038/ng1800 16699517 (Pubitemid 43927300)
41. S Nejentsev N Walker D Riches M Egholm JA Todd 2009 Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes Science 324 5925 387 389 1:CAS:528:DC%2BD1MXksVOltr8%3D 10.1126/science.1167728 19264985 PMCID: 2707798
42. LC Stene S Oikarinen H Hyöty KJ Barriga JM Norris JC Hutton HA Erlich GSR Eisenbarth M Rewers 2010 Enterovirus infection and progression from islet autoimmunity to type 1 diabetes: The Diabetes and Autoimmunity Study in the Young (DAISY) Diabetes 59 12 3174 3180 1:CAS:528:DC%2BC3MXlsValuw%3D%3D 10.2337/db10-0866 20858685
43. Fauquet MAM CM, Maniloff J, Desselberger U, Ball LA (2005) Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Burlington, MA
44. M Roivainen 2006 Enteroviruses: new findings on the role of enteroviruses in type 1 diabetes Int J Biochem Cell Biol 38 5-6 721 725 1:CAS:528: DC%2BD28Xit1Ohtbs%3D 10.1016/j.biocel.2005.08.019 16226050 (Pubitemid 43363408)
45. CM Filippi EA Estes JE Oldham MG von Herrath 2009 Immunoregulatory mechanisms triggered by viral infections protect from type 1 diabetes in mice J Clin Invest 119 6 1515 1523 1:CAS:528:DC%2BD1MXntVCjt7o%3D 19478458 PMCID: 2689128
46. LK Shoda DL Young S Ramanujan CC Whiting MA Atkinson JA Bluestone, et al. 2005 A comprehensive review of interventions in the NOD mouse and implications for translation Immunity 23 2 115 126 1:CAS:528:DC%2BD2MXpvVCnurg%3D 10.1016/j.immuni.2005.08.002 16111631 (Pubitemid 41169282)
47. F Saravia-Fernandez S Durant A el Hasnaoui M Dardenne F Homo-Delarche 1996 Environmental and experimental procedures leading to variations in the incidence of diabetes in the nonobese diabetic (NOD) mouse Autoimmunity 24 2 113 121 1:STN:280:DyaK2s7jvFOhtg%3D%3D 10.3109/08916939609001952 8986323
48. DV Serreze C Wasserfall EW Ottendorfer M Stalvey MA Pierce C Gauntt, et al. 2005 Diabetes acceleration or prevention by a coxsackievirus B4 infection: critical requirements for both interleukin-4 and gamma interferon J Virol 79 2 1045 1052 1:CAS:528:DC%2BD2MXlt12gug%3D%3D 10.1128/JVI.79.2.1045-1052.2005 15613333 PMCID: 538592 (Pubitemid 40053888)
49. T Takaki MP Marron CE Mathews ST Guttmann R Bottino M Trucco, et al. 2006 HLA-A*0201-restricted T cells from humanized NOD mice recognize autoantigens of potential clinical relevance to type 1 diabetes J Immunol 176 5 3257 3265 1:CAS:528:DC%2BD28Xhs1eqsrY%3D 16493087
50. BO Roep M Atkinson M von Herrath 2004 Satisfaction (not) guaranteed: re-evaluating the use of animal models of type 1 diabetes Nat Rev Immunol 4 12 989 997 1:CAS:528:DC%2BD2cXhtVarsb7L 10.1038/nri1502 15573133 (Pubitemid 39620073)