On the etiology of type 1 diabetes: A new animal model signifying a decisive role for bacteria eliciting an adverse innate immunity response

American Journal of Pathology

Volumn 181, Issue 5, 2012, Pages 1735-1748

  Korsgren, Stella ^a   Molin, Ylva ^b   Salmela, Kaija ^c   Lundgren, Torbjörn ^d   Melhus, Åsa ^b   Korsgren, Olle ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF HELSINKI   (Finland)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BLEEDING; CELL DESTRUCTION; CELL INFILTRATION; CYTOKINE RELEASE; CYTOPLASM; DUODENUM; DYING; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPATHOLOGY; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MALE; MONOCYTE; NEUTROPHIL; NONHUMAN; PANCREAS DUCT; PANCREAS ISLET BETA CELL; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; RAT; STAPHYLOCOCCUS AUREUS;

ADULT; ANIMALS; BACTERIA; CYTOKINES; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; FATAL OUTCOME; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; ISLETS OF LANGERHANS; MALE; MODELS, BIOLOGICAL; RATS; RATS, WISTAR;

EID: 84868130672     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.07.022     Document Type: Article

References (65)

1. B.O. Roep, M. Atkinson, M. von Herrath Satisfaction (not) guaranteed: re-evaluating the use of animal models of type 1 diabetes Nat Rev Immunol 4 2004 989 997 (Pubitemid 39620073)
2. A.K. Foulis, N.D. Francis, M.A. Farquharson, A. Boylston Massive synchronous B-cell necrosis causing type 1 (insulin-dependent) diabetes-a unique histopathological case report Diabetologia 31 1988 46 50 (Pubitemid 18077572)
3. A.K. Foulis, C.N. Liddle, M.A. Farquharson, J.A. Richmond, R.S. Weir 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 1986 267 274 (Pubitemid 16080921)
4. W. Gepts Pathologic anatomy of the pancreas in juvenile diabetes mellitus Diabetes 14 1965 619 633
5. P.M. Lecompte Insulitis in early juvenile diabetes AMA Arch Pathol 66 1958 450 457
6. P. In't Veld Insulitis in human type 1 diabetes: the quest for an elusive lesion Islets 3 2011 131 138
7. A.L. Notkins, A. Lernmark Autoimmune type 1 diabetes: resolved and unresolved issues J Clin Invest 108 2001 1247 1252 (Pubitemid 33107747)
8. T. Staeva-Vieira, M. Peakman, M. von Herrath Translational mini-review series on type 1 diabetes: immune-based therapeutic approaches for type 1 diabetes Clin Exp Immunol 148 2007 17 31 (Pubitemid 46364996)
9. M.D. Pescovitz, C.J. Greenbaum, H. Krause-Steinrauf, D.J. Becker, S.E. Gitelman, R. Goland, P.A. Gottlieb, J.B. Marks, P.F. McGee, A.M. Moran, P. Raskin, H. Rodriguez, D.A. Schatz, D. Wherrett, D.M. Wilson, J.M. Lachin, J.S. Skyler Rituximab B-lymphocyte depletion, and preservation of beta-cell function N Engl J Med 361 2009 2143 2152
10. B. Keymeulen, M. Walter, C. Mathieu, L. Kaufman, F. Gorus, R. Hilbrands, E. Vandemeulebroucke, U. Van de Velde, L. Crenier, C. De Block, S. Candon, H. Waldmann, A.G. Ziegler, L. Chatenoud, D. Pipeleers Four-year metabolic outcome of a randomised controlled CD3-antibody trial in recent-onset type 1 diabetic patients depends on their age and baseline residual beta cell mass Diabetologia 53 2010 614 623
11. K.C. Herold, S. Gitelman, C. Greenbaum, J. Puck, W. Hagopian, P. Gottlieb, P. Sayre, P. Bianchine, E. Wong, V. Seyfert-Margolis, K. Bourcier, J.A. Bluestone Treatment of patients with new onset Type 1 diabetes with a single course of anti-CD3 mAb Teplizumab preserves insulin production for up to 5 years Clin Immunol 132 2009 166 173
12. D.K. Wherrett, B. Bundy, D.J. Becker, L.A. DiMeglio, S.E. Gitelman, R. Goland, P.A. Gottlieb, C.J. Greenbaum, K.C. Herold, J.B. Marks, R. Monzavi, A. Moran, T. Orban, J.P. Palmer, P. Raskin, H. Rodriguez, D. Schatz, D.M. Wilson, J.P. Krischer, J.S. Skyler Antigen-based therapy with glutamic acid decarboxylase (GAD) vaccine in patients with recent-onset type 1 diabetes: a randomised double-blind trial Lancet 378 2011 319 327
13. J.S. Skyler, J.P. Krischer, J. Wolfsdorf, C. Cowie, J.P. Palmer, C. Greenbaum, D. Cuthbertson, L.E. Rafkin-Mervis, H.P. Chase, E. Leschek Effects of oral insulin in relatives of patients with type 1 diabetes: the Diabetes Prevention Trial-Type 1 Diabetes Care 28 2005 1068 1076 (Pubitemid 40616615)
14. K. Nanto-Salonen, A. Kupila, S. Simell, H. Siljander, T. Salonsaari, A. Hekkala, S. Korhonen, R. Erkkola, J.I. Sipila, L. Haavisto, M. Siltala, J. Tuominen, J. Hakalax, H. Hyoty, J. Ilonen, R. Veijola, T. Simell, M. Knip, O. Simell Nasal insulin to prevent type 1 diabetes in children with HLA genotypes and autoantibodies conferring increased risk of disease: a double-blind, randomised controlled trial Lancet 372 2008 1746 1755
15. P.D. Hardt, N. Ewald, K. Brockling, S. Tanaka, T. Endo, H.U. Kloer, R.G. Bretzel, C. Jaeger, H. Shimura, T. Kobayashi Distinct autoantibodies against exocrine pancreatic antigens in European patients with type 1 diabetes mellitus and non-alcoholic chronic pancreatitis JOP 9 2008 683 689
16. L. Panicot, E. Mas, C. Thivolet, D. Lombardo Circulating antibodies against an exocrine pancreatic enzyme in type 1 diabetes Diabetes 48 1999 2316 2323 (Pubitemid 30395422)
17. T. Taniguchi, J. Tanaka, S. Seko, K. Okazaki, M. Okamoto Association of rapid-onset type 1 diabetes and clinical acute pancreatitis positive for autoantibodies to the exocrine pancreas Diabetes Care 24 2001 2156 2157
18. T. Taniguchi, K. Okazaki, M. Okamoto, S. Seko, J. Tanaka, K. Uchida, K. Nagashima, T. Kurose, Y. Yamada, T. Chiba, Y. Seino High prevalence of autoantibodies against carbonic anhydrase II and lactoferrin in type 1 diabetes: concept of autoimmune exocrinopathy and endocrinopathy of the pancreas Pancreas 27 2003 26 30 (Pubitemid 36775975)
19. W. Creutzfeldt, D. Gleichmann, J. Otto, F. Stockmann, P. Maisonneuve, P.G. Lankisch Follow-up of exocrine pancreatic function in type-1 diabetes mellitus Digestion 72 2005 71 75 (Pubitemid 41507265)
20. J.L. Gaglia, A.R. Guimaraes, M. Harisinghani, S.E. Turvey, R. Jackson, C. Benoist, D. Mathis, R. Weissleder Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients J Clin Invest 121 2011 442 445
21. J.J. Meier, A. Bhushan, A.E. Butler, R.A. Rizza, P.C. Butler Sustained beta cell apoptosis in patients with long-standing type 1 diabetes: indirect evidence for islet regeneration? Diabetologia 48 2005 2221 2228 (Pubitemid 41618910)
22. A. Kondrashova, H. Viskari, P. Kulmala, A. Romanov, J. Ilonen, H. Hyoty, M. Knip Signs of beta-cell autoimmunity in nondiabetic schoolchildren: a comparison between Russian Karelia with a low incidence of type 1 diabetes and Finland with a high incidence rate Diabetes Care 30 2007 95 100 (Pubitemid 46052505)
23. T. Oilinki, T. Otonkoski, J. Ilonen, M. Knip, P. Miettinen Prevalence and characteristics of diabetes among Somali children and adolescents living in Helsinki, Finland Pediatr Diabetes 13 2012 176 180
24. J.W. Yoon, M. Austin, T. Onodera, A.L. Notkins Isolation of a virus from the pancreas of a child with diabetic ketoacidosis N Engl J Med 300 1979 1173 1179 (Pubitemid 9191515)
25. I. Adlerberth, E. Lindberg, N. Aberg, B. Hesselmar, R. Saalman, I.L. Strannegard, A.E. Wold Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle? Pediatr Res 59 2006 96 101
26. C.C. Patterson, G.G. Dahlquist, E. Gyurus, A. Green, G. Soltesz Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study Lancet 373 2009 2027 2033
27. C. Bizzarri, P.I. Patera, C. Arnaldi, S. Petrucci, M.L. Bitti, R. Scrocca, S. Manfrini, R. Portuesi, R. Buzzetti, M. Cappa, P. Pozzilli Incidence of type 1 diabetes has doubled in Rome and the Lazio region in the 0- to 14-year age-group: a 6-year prospective study (2004-2009) Diabetes Care 33 2010 e140
28. V. Hall, R.W. Thomsen, O. Henriksen, N. Lohse Diabetes in Sub Saharan Africa 1999-2011: epidemiology and Public Health Implications A systematic review BMC Public Health 11 2011 564
29. D.S. Acton, M.J. Plat-Sinnige, W. van Wamel, N. de Groot, A. van Belkum Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis 28 2009 115 127
30. B. Lundequist, C.E. Nord, J. Winberg The composition of the faecal microflora in breastfed and bottle fed infants from birth to eight weeks Acta Paediatr Scand 74 1985 45 51 (Pubitemid 15174105)
31. E. Lindberg, I. Adlerberth, P. Matricardi, C. Bonanno, S. Tripodi, V. Panetta, B. Hesselmar, R. Saalman, N. Aberg, A.E. Wold Effect of lifestyle factors on Staphylococcus aureus gut colonization in Swedish and Italian infants Clin Microbiol Infect 17 2011 1209 1215
32. M.O. Efuntoye, A.I. Adetosoye Enterotoxigenicity and drug sensitivity of staphylococci from children aged five years and below with sporadic diarrhoea East Afr Med J 80 2003 656 659 (Pubitemid 41295494)
33. A. Kinsner, V. Pilotto, S. Deininger, G.C. Brown, S. Coecke, T. Hartung, A. Bal-Price Inflammatory neurodegeneration induced by lipoteichoic acid from Staphylococcus aureus is mediated by glia activation, nitrosative and oxidative stress, and caspase activation J Neurochem 95 2005 1132 1143 (Pubitemid 41713496)
34. C. Flores, I. Maguilnik, E. Hadlich, L.Z. Goldani Microbiology of choledochal bile in patients with choledocholithiasis admitted to a tertiary hospital J Gastroenterol Hepatol 18 2003 333 336 (Pubitemid 36513164)
35. A.A. Negm, A. Schott, R.P. Vonberg, T.J. Weismueller, A.S. Schneider, S. Kubicka, C.P. Strassburg, M.P. Manns, S. Suerbaum, J. Wedemeyer, T.O. Lankisch Routine bile collection for microbiological analysis during cholangiography and its impact on the management of cholangitis Gastrointest Endosc 72 2010 284 291
36. S.W. Schmid, W. Uhl, H. Friess, P. Malfertheiner, M.W. Buchler The role of infection in acute pancreatitis Gut 45 1999 311 316 (Pubitemid 29333786)
37. I. Stelzmueller, N. Berger, S. Wiesmayr, M. Eller, W. Tabarelli, M. Fille, R. Margreiter, H. Bonatti Group milleri streptococci: significant pathogens in solid organ recipients Transpl Int 20 2007 51 56 (Pubitemid 44950363)
38. C. Megevand, A. Gervaix, U. Heininger, C. Berger, C. Aebi, B. Vaudaux, C. Kind, H.P. Gnehm, M. Hitzler, G. Renzi, J. Schrenzel, P. Francois Molecular epidemiology of the nasal colonization by methicillin-susceptible Staphylococcus aureus in Swiss children Clin Microbiol Infect 16 2010 1414 1420
39. M. Goto, T.M. Eich, M. Felldin, A. Foss, R. Kallen, K. Salmela, A. Tibell, G. Tufveson, K. Fujimori, M. Engkvist, O. Korsgren Refinement of the automated method for human islet isolation and presentation of a closed system for in vitro islet culture Transplantation 78 2004 1367 1375 (Pubitemid 39507978)
40. S.W. Behrman, M.H. Bahr, P.V. Dickson, B.L. Zarzaur The microbiology of secondary and postoperative pancreatic infections: implications for antimicrobial management Arch Surg 146 2011 613 619
41. E.J. Luiten, W.C. Hop, J.F. Lange, H.A. Bruining Differential prognosis of gram-negative versus gram-positive infected and sterile pancreatic necrosis: results of a randomized trial in patients with severe acute pancreatitis treated with adjuvant selective decontamination Clin Infect Dis 25 1997 811 816 (Pubitemid 127774285)
42. J.J. Couper, N. Kallincos, A. Pollard, M. Honeyman, P. Prager, L.C. Harrison, M. Rischmueller Toxic shock syndrome associated with newly diagnosed type I diabetes J Paediatr Child Health 36 2000 279 282 (Pubitemid 30394931)
43. S.C. Bunnag, S. Bunnag, N.E. Warner Microcirculation in the islets of Langerhans of the mouse Anat Rec 146 1963 117 123
44. A.N. Gorsuch, K.M. Spencer, J. Lister, J.M. McNally, B.M. Dean, G.F. Bottazzo, A.G. Cudworth Evidence for a long prediabetic period in type I (insulin-dependent) diabetes mellitus Lancet 2 1981 1363 1365 (Pubitemid 12239439)
45. A. Skowera, R.J. Ellis, R. Varela-Calvino, S. Arif, G.C. Huang, C. Van-Krinks, A. Zaremba, C. Rackham, J.S. Allen, T.I. Tree, M. Zhao, C.M. Dayan, A.K. Sewell, W.W. Unger, J.W. Drijfhout, F. Ossendorp, B.O. Roep, M. Peakman CTLs are targeted to kill beta cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope J Clin Invest 118 2008 3390 3402
46. H.E. Larsson, K. Lynch, B. Lernmark, A. Nilsson, G. Hansson, P. Almgren, A. Lernmark, S.A. Ivarsson Diabetes-associated HLA genotypes affect birthweight in the general population Diabetologia 48 2005 1484 1491 (Pubitemid 41175500)
47. L. Blom, L.A. Persson, G. Dahlquist A high linear growth is associated with an increased risk of childhood diabetes mellitus Diabetologia 35 1992 528 533
48. G.J. Bruining Association between infant growth before onset of juvenile type-1 diabetes and autoantibodies to IA-2 Netherlands Kolibrie study group of childhood diabetes Lancet 356 2000 655 656 (Pubitemid 30627597)
49. E. Hypponen, S.M. Virtanen, M.G. Kenward, M. Knip, H.K. Akerblom Obesity, increased linear growth, and risk of type 1 diabetes in children Diabetes Care 23 2000 1755 1760
50. I. Knerr, J. Wolf, T. Reinehr, R. Stachow, M. Grabert, E. Schober, W. Rascher, R.W. Holl The 'accelerator hypothesis': relationship between weight, height, body mass index and age at diagnosis in a large cohort of 9,248 German and Austrian children with type 1 diabetes mellitus Diabetologia 48 2005 2501 2504 (Pubitemid 41738214)
51. H.E. Larsson, G. Hansson, A. Carlsson, E. Cederwall, B. Jonsson, K. Larsson, K. Lynch, J. Neiderud, A. Lernmark, S.A. Ivarsson Children developing type 1 diabetes before 6 years of age have increased linear growth independent of HLA genotypes Diabetologia 51 2008 1623 1630
52. K. Bendtzen, T. Mandrup-Poulsen, J. Nerup, J.H. Nielsen, C.A. Dinarello, M. Svenson Cytotoxicity of human pI 7 interleukin-1 for pancreatic islets of Langerhans Science 232 1986 1545 1547 (Pubitemid 16061563)
53. W.J. Malaisse, F. Malaisse-Lagae, A. Sener, D.G. Pipeleers Determinants of the selective toxicity of alloxan to the pancreatic B cell Proc Natl Acad Sci U S A 79 1982 927 930 (Pubitemid 12160335)
54. G.A. Martens, Y. Cai, S. Hinke, G. Stange, M. Van de Casteele, D. Pipeleers Glucose suppresses superoxide generation in metabolically responsive pancreatic beta cells J Biol Chem 280 2005 20389 20396 (Pubitemid 40776738)
55. A.K. Foulis, J.A. Stewart The pancreas in recent-onset type 1 (insulin-dependent) diabetes mellitus: insulin content of islets, insulitis and associated changes in the exocrine acinar tissue Diabetologia 26 1984 456 461 (Pubitemid 14080823)
56. J.R. Henderson Why are the islets of Langerhans? Lancet 2 1969 469 470
57. B. Karges, I. Durinovic-Bello, E. Heinze, B.O. Boehm, K.M. Debatin, W. Karges Complete long-term recovery of beta-cell function in autoimmune type 1 diabetes after insulin treatment Diabetes Care 27 2004 1207 1208 (Pubitemid 38579793)
58. A.G. Cudworth, G.B. White, J.C. Woodrow, D.R. Gamble, R. Lendrum, A. Bloom Aetiology of juvenile-onset diabetes: a prospective study Lancet 1 1977 385 388
59. G.S. Eisenbarth Type I diabetes mellitus: a chronic autoimmune disease N Engl J Med 314 1986 1360 1368 (Pubitemid 16122469)
60. L. Jansson, D.L. Eizirik, D.G. Pipeleers, L.A. Borg, C. Hellerstrom, A. Andersson Impairment of glucose-induced insulin secretion in human pancreatic islets transplanted to diabetic nude mice J Clin Invest 96 1995 721 726
61. A. Weichselbaum, E. Stangl Zur Kenntniss der feineren Veränderungen des Pankreas bei Diabetes mellitus Wiener Klinische Wochenschrift 41 1901 968 972
62. W.E. Toreson Glycogen infiltration (so-called hydropic degeneration) in the pancreas in human and experimental diabetes mellitus Am J Pathol 27 1951 327 347
63. P.I. Neophytou, B.O. Roep, S.D. Arden, E.M. Muir, G. Duinkerken, A. Kallan, R.R. de Vries, J.C. Hutton T-cell epitope analysis using subtracted expression libraries (TEASEL): application to a 38-kDA autoantigen recognized by T cells from an insulin-dependent diabetic patient Proc Natl Acad Sci U S A 93 1996 2014 2018
64. R. Di Cagno, M. De Angelis, I. De Pasquale, M. Ndagijimana, P. Vernocchi, P. Ricciuti, F. Gagliardi, L. Laghi, C. Crecchio, M.E. Guerzoni, M. Gobbetti, R. Francavilla Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization BMC Microbiol 11 2011 219
65. J. Visser, J. Rozing, A. Sapone, K. Lammers, A. Fasano Tight junctions, intestinal permeability, and autoimmunity: celiac disease and type 1 diabetes paradigms Ann N Y Acad Sci 1165 2009 195 205