Increased immune cell infiltration of the exocrine pancreas: A possible contribution to the pathogenesis of type 1 diabetes

Diabetes

Volumn 63, Issue 11, 2014, Pages 3880-3890

  Rodriguez Calvo, Teresa ^a   Ekwall, Olov ^a,b   Amirian, Natalie ^a   Zapardiel Gonzalo, Jose ^c   Von Herrath, Matthias G ^a,d  

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

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c Freelance Consultant   (United States)

^d NOVO NORDISK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CD4 ANTIGEN; CD8 ANTIGEN; GLYCOPROTEIN P 15095; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL DENSITY; CELL INFILTRATION; CELL KILLING; CONTROLLED STUDY; DIABETIC PATIENT; DISEASE DURATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; INFLAMMATORY INFILTRATE; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PATHOGENESIS; TISSUE DISTRIBUTION; CD4+ T LYMPHOCYTE; CYTOLOGY; EXOCRINE PANCREAS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; IN VITRO STUDY; METABOLISM; PANCREAS ISLET; PATHOLOGY;

ADULT; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IN VITRO TECHNIQUES; ISLETS OF LANGERHANS; MALE; PANCREAS, EXOCRINE;

EID: 84908635248     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0549     Document Type: Article

References (45)

1. van Belle TL, Coppieters KT, von Herrath MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 2011;91:79-118
2. Foulis AK, Farquharson MA, Hardman R. Aberrant expression of class II major histocompatibility complex molecules by B cells and hyperexpression of class I major histocompatibility complex molecules by insulin containing islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 1987;30:333-343
3. Coppieters KT, Dotta F, Amirian N, et al. Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 2012;209:51-60
4. Bending D, Zaccone P, Cooke A. Inflammation and type one diabetes. Int Immunol 2012;24:339-346
5. Padgett LE, Broniowska KA, Hansen PA, Corbett JA, Tse HM. The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Ann N Y Acad Sci 2013;1281:16-35
6. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 1998;4:781-785
7. Fujinami RS, von Herrath MG, Christen U, Whitton JL. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 2006;19:80-94
8. Wieser V, Moschen AR, Tilg H. Inflammation, cytokines and insulin resistance: a clinical perspective. Arch Immunol Ther Exp (Warsz) 2013;61:119-125
9. Sell H, Habich C, Eckel J. Adaptive immunity in obesity and insulin resistance. Nat Rev Endocrinol 2012;8:709-716
10. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 2011;11:98-107
11. Brooks-Worrell B, Narla R, Palmer JP. Islet autoimmunity in phenotypic type 2 diabetes patients. Diabetes Obes Metab 2013;15(Suppl. 3):137-140
12. Brooks-Worrell BM, Palmer JP. Attenuation of islet-specific T cell responses is associated with C-peptide improvement in autoimmune type 2 diabetes patients. Clin Exp Immunol 2013;171:164-170
13. Sarikonda G, Pettus J, Phatak S, et al. CD8 T-cell reactivity to islet antigens is unique to type 1 while CD4 T-cell reactivity exists in both type 1 and type 2 diabetes. J Autoimmun 2014;50:77-82
14. Kaminski BM, Klingensmith GJ, Beck RW, et al. Body mass index at the time of diagnosis of autoimmune type 1 diabetes in children. J Pediatr 2013;162:736-740.e1
15. Pozzilli P, Guglielmi C. Double diabetes: a mixture of type 1 and type 2 diabetes in youth. Endocr Dev 2009;14:151-166
16. In't Veld P. Insulitis in human type 1 diabetes: The quest for an elusive lesion. Islets 2011;3:131-138
17. Campbell-Thompson ML, Atkinson MA, Butler AE, et al. The diagnosis of insulitis in human type 1 diabetes. Diabetologia 2013;56:2541-2543
18. Chen N, Unnikrishnan I R, Anjana RM, Mohan V, Pitchumoni CS. The complex exocrine-endocrine relationship and secondary diabetes in exocrine pancreatic disorders. J Clin Gastroenterol 2011;45:850-861
19. Lifson N, Kramlinger KG, Mayrand RR, Lender EJ. Blood flow to the rabbit pancreas with special reference to the islets of Langerhans. Gastroenterology 1980;79:466-473
20. Campbell-Thompson M, Wasserfall C, Montgomery EL, Atkinson MA, Kaddis JS. Pancreas organ weight in individuals with disease-associated autoantibodies at risk for type 1 diabetes. JAMA 2012;308:2337-2339
21. Williams AJ, Thrower SL, Sequeiros IM, et al. Pancreatic volume is reduced in adult patients with recently diagnosed type 1 diabetes. J Clin Endocrinol Metab 2012;97:E2109-E2113
22. Hardt PD, Krauss A, Bretz L, et al. Pancreatic exocrine function in patients with type 1 and type 2 diabetes mellitus. Acta Diabetol 2000;37:105-110
23. In't Veld P, De Munck N, Van Belle K, et al. Beta-cell replication is increased in donor organs from young patients after prolonged life support. Diabetes 2010; 59:1702-1708
24. Saxena V, Ondr JK, Magnusen AF, Munn DH, Katz JD. The countervailing actions of myeloid and plasmacytoid dendritic cells control autoimmune diabetes in the nonobese diabetic mouse. J Immunol 2007;179:5041-5053
25. Nikolic T, Bouma G, Drexhage HA, Leenen PJ. Diabetes-prone NOD mice show an expanded subpopulation of mature circulating monocytes, which preferentially develop into macrophage-like cells in vitro. J Leukoc Biol 2005;78:70-79
26. Calderon B, Suri A, Miller MJ, Unanue ER. Dendritic cells in islets of Langerhans constitutively present beta cell-derived peptides bound to their class II MHC molecules. Proc Natl Acad Sci U S A 2008;105:6121-6126
27. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12:298-306
28. Ma C, Zhang Q, Ye J, et al. Tumor-infiltrating gd T lymphocytes predict clinical outcome in human breast cancer. J Immunol 2012;189:5029-5036
29. Krogvold L, Edwin B, Buanes T, et al. Pancreatic biopsy by minimal tail resection in live adult patients at the onset of type 1 diabetes: experiences from the DiViD study. Diabetologia 2014;57:841-843
30. Gianani R, Campbell-Thompson M, Sarkar SA, et al. Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 2010;53:690-698
31. Bettini M, Vignali DA. T cell-driven initiation and propagation of autoimmune diabetes. Curr Opin Immunol 2011;23:754-760
32. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol 2009;10:524-530
33. Mueller SN, Gebhardt T, Carbone FR, Heath WR. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 2013;31:137-161
34. Mackay LK, Stock AT, Ma JZ, et al. Long-lived epithelial immunity by tissueresident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci U S A 2012;109:7037-7042
35. Coppieters KT, Amirian N, Pagni PP, et al. Functional redundancy of CXCR3/CXCL10 signaling in the recruitment of diabetogenic cytotoxic T lymphocytes to pancreatic islets in a virally induced autoimmune diabetes model. Diabetes 2013; 62:2492-2499
36. Sarkar SA, Lee CE, Victorino F, et al. Expression and regulation of chemokines in murine and human type 1 diabetes. Diabetes 2012;61:436-446
37. Frigerio S, Junt T, Lu B, et al. Beta cells are responsible for CXCR3- mediated T-cell infiltration in insulitis. Nat Med 2002;8:1414-1420
38. Skog O, Korsgren S, Melhus A, Korsgren O. Revisiting the notion of type 1 diabetes being a T-cell-mediated autoimmune disease. Curr Opin Endocrinol Diabetes Obes 2013;20:118-123
39. Sato M, Yamamoto K, Mayama H, Yamashiro Y. Exocrine pancreatic function in diabetic children. J Pediatr Gastroenterol Nutr 1984;3:415-420
40. Solanki NS, Barreto SG, Saccone GT. Acute pancreatitis due to diabetes: the role of hyperglycaemia and insulin resistance. Pancreatology 2012;12:234-239
41. Lefebvre DE, Powell KL, Strom A, Scott FW. Dietary proteins as environmental modifiers of type 1 diabetes mellitus. Annu Rev Nutr 2006;26:175-202
42. Graham S, Courtois P, Malaisse WJ, Rozing J, Scott FW, Mowat AM. Enteropathy precedes type 1 diabetes in the BB rat. Gut 2004;53:1437-1444
43. Nishimura S, Manabe I, Nagasaki M, et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009;15:914-920
44. Lagathu C, Yvan-Charvet L, Bastard JP, et al. Long-term treatment with interleukin-1beta induces insulin resistance in murine and human adipocytes. Diabetologia 2006;49:2162-2173
45. Sartipy P, Loskutoff DJ. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc Natl Acad Sci U S A 2003;100:7265-7270