Islet infiltration, cytokine expression and beta cell death in the NOD mouse, BB rat, Komeda rat, LEW.1AR1-iddm rat and humans with type 1 diabetes

Diabetologia

Volumn 57, Issue 3, 2014, Pages 512-521

  Jörns, Anne ^a   Arndt, Tanja ^a   Zu Vilsendorf, Andreas Meyer ^a   Klempnauer, Jürgen ^a   Wedekind, Dirk ^a   Hedrich, Hans Jürgen ^a   Marselli, Lorella ^b   Marchetti, Piero ^b   Harada, Nagakatsu ^c   Nakaya, Yutaka ^c   Wang, Gen Sheng ^d   Scott, Fraser W ^d   Gysemans, Conny ^e   Mathieu, Chantal ^e   Lenzen, Sigurd ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF PISA   (Italy)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Animal models; Cytokines; Human; Immune cells; Pancreatic islets; Type 1 diabetes

Indexed keywords

CYTOKINE; GAMMA INTERFERON; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; APOPTOSIS; B LYMPHOCYTE; BIOBREEDING RAT; COMPARATIVE STUDY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; LEWIS RAT; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PANCREAS ISLET BETA CELL; PATHOLOGY; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; MICE; MICE, INBRED NOD; RATS; RATS, INBRED BB; RATS, INBRED LEW; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84894542402     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-013-3125-4     Document Type: Article

References (50)

1. Imagawa A, Hanafusa T, Itoh N et al (1996) Islet-infiltrating T lymphocytes in insulin-dependent diabetic patients express CD80 (B7-1) and CD86 (B7-2). J Autoimmun 9:391-396
2. Imagawa A, Hanafusa T, Tamura S et al (2001) Pancreatic biopsy as a procedure for detecting in situ autoimmune phenomena in type 1 diabetes: close correlation between serological markers and histological evidence of cellular autoimmunity. Diabetes 50:1269-1273
3. Uno S, Imagawa A, Okita K et al (2007) Macrophages and dendritic cells infiltrating islets with or without beta cells produce tumour necrosis factor-alpha in patients with recent-onset type 1 diabetes. Diabetologia 50:596-601
4. Makino S, Kunimoto K, Muraoka Y, Mizushima Y, Katagiri K, Tochino Y (1980) Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 29:1-13
5. Anderson MS, Bluestone JA (2005) The NOD mouse: a model of immune dysregulation. Annu Rev Immunol 23:447-485
6. Gysemans C, Callewaert H, Moore F et al (2009) Interferon regulatory factor-1 is a key transcription factor in murine beta cells under immune attack. Diabetologia 52:2374-2384
7. Koulmanda M, Bhasin M, Awdeh Z et al (2012) The role of TNF-alpha in mice with type 1- and 2- diabetes. PLoS One 7:e33254
8. Nakhooda AF, Like AA, Chappel CI, Murray FT, Marliss EB (1977) The spontaneously diabetic Wistar rat. Metabolic and morphologic studies. Diabetes 26:100-112
9. Mordes JP, Bortell R, Blankenhorn EP, Rossini AA, Greiner DL (2004) Rat models of type 1 diabetes: genetics, environment, and autoimmunity. ILAR J 45:278-291
10. Wang GS, Kauri LM, Patrick C, Bareggi M, Rosenberg L, Scott FW (2010) Enhanced islet expansion by beta-cell proliferation in young diabetes-prone rats fed a protective diet. J Cell Physiol 224:501-508
11. Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T (1991) New inbred strain of Long-Evans Tokushima lean rats with IDDM without lymphopenia. Diabetes 40:1375-1381
12. Komeda K, Noda M, Terao K, Kuzuya N, Kanazawa M, Kanazawa Y (1998) Establishment of two substrains, diabetes-prone and non-diabetic, from Long-Evans Tokushima Lean (LETL) rats. Endocr J 45:737-744
13. Lenzen S, Tiedge M, Elsner M et al (2001) The LEW.1AR1/Ztm-iddm rat: a new model of spontaneous insulin-dependent diabetes mellitus. Diabetologia 44:1189-1196
14. Jörns A, Günther A, Hedrich HJ, Wedekind D, Tiedge M, Lenzen S (2005) Immune cell infiltration, cytokine expression, and beta-cell apoptosis during the development of type 1 diabetes in the spontaneously diabetic LEW.1AR1/Ztm-iddm rat. Diabetes 54:2041-2052
15. (+) T cell frequency in peripheral blood lymphocytes associated with type 1 diabetes mellitus development in the LEW.1AR1-iddm rat. PLoS One 8:e64305
16. King AJ (2012) The use of animal models in diabetes research. Br J Pharmacol 166:877-894
17. Buschard K (2011) What causes type 1 diabetes? Lessons from animal models. APMIS, Suppl 132:1-19
18. Roep BO, Atkinson M, von Herrath M (2004) Satisfaction (not) guaranteed: re-evaluating the use of animal models of type 1 diabetes. Nat Rev Immunol 4:989-997
19. Roep BO, Buckner J, Sawcer S, Toes R, Zipp F (2012) The problems and promises of research into human immunology and autoimmune disease. Nat Med 18:48-53
20. Pearson T, Greiner DL, Shultz LD (2008) Creation of "humanized" mice to study human immunity. Curr Protoc Immunol Chapter 15:Unit 15.21
21. Jörns A, Rath KJ, Terbish T et al (2010) Diabetes prevention by immunomodulatory FTY720 treatment in the LEW.1AR1-iddm rat despite immune cell activation. Endocrinology 151:3555-3565
22. MacMurray AJ, Moralejo DH, Kwitek AE et al (2002) Lymphopenia in the BB rat model of type 1 diabetes is due to a mutation in a novel immune-associated nucleotide (Ian)-related gene. Genome Res 12:1029-1039
23. Sommandas V, Rutledge EA, van Yserloo B, Fuller J, Lernmark A, Drexhage HA (2007) Low-density cells isolated from the rat thymus resemble branched cortical macrophages and have a reduced capability of rescuing double-positive thymocytes from apoptosis in the BB-DP rat. J Leukoc Biol 82:869-876
24. Atkinson MA, Bluestone JA, Eisenbarth GS et al (2011) How does type 1 diabetes develop? the notion of homicide or beta-cell suicide revisited. Diabetes 60:1370-1379
25. Reddy S, Chai RC, Rodrigues JA, Hsu TH, Robinson E (2008) Presence of residual beta cells and co-existing islet autoimmunity in the NOD mouse during longstanding diabetes: a combined histochemical and immunohistochemical study. J Mol Histol 39:25-36
26. Coppieters KT, Dotta F, Amirian N et al (2012) Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 209:51-60
27. Lally FJ, Ratcliff H, Bone AJ (2001) Apoptosis and disease progression in the spontaneously diabetic BB/S rat. Diabetologia 44:320-324
28. Mordes JP, Desemone J, Rossini AA (1987) The BB rat. Diabetes Metab Rev 3:725-750
29. Richardson SJ, Willcox A, Bone AJ, Morgan NG, Foulis AK (2011) Immunopathology of the human pancreas in type-I diabetes. Semin Immunopathol 33:9-21
30. Rowe PA, Campbell-Thompson ML, Schatz DA, Atkinson MA (2011) The pancreas in human type 1 diabetes. Semin Immunopathol 33:29-43
31. Carrero JA, Calderon B, Towfic F, Artyomov MN, Unanue ER (2013) Defining the transcriptional and cellular landscape of type 1 diabetes in the NOD mouse. PLoS One 8:e59701
32. Voorbij HA, Jeucken PH, Kabel PJ, de Haan M, Drexhage HA (1989) Dendritic cells and scavenger macrophages in pancreatic islets of prediabetic BB rats. Diabetes 38:1623-1629
33. Akirav EM, Baquero MT, Opare-Addo LW et al (2011) Glucose and inflammation control islet vascular density and beta-cell function in NOD mice: control of islet vasculature and vascular endothelial growth factor by glucose. Diabetes 60:876-883
34. Kleemann R, Scott FW, Worz-Pagenstert U, Nimal Ratnayake WM, Kolb H (1998) Impact of dietary fat on Th1/Th2 cytokine gene expression in the pancreas and gut of diabetes-prone BB rats. J Autoimmun 11:97-103
35. Mastrandrea L, Yu J, Behrens T et al (2009) Etanercept treatment in children with new-onset type 1 diabetes: pilot randomized, placebo-controlled, double-blind study. Diabetes Care 32:1244-1249
36. Arif S, Cox P, Afzali B et al (2010) Anti-TNFalpha therapy-killing two birds with one stone? Lancet 375:2278
37. Kalden JR (2011) Anti-TNF therapy: what have we learned in 12 years? Arthritis Res Ther 13(Suppl. 1): S1
38. Wang F, Smith N, Maier L et al (2012) Etanercept suppresses regenerative hyperplasia in psoriasis by acutely downregulating epidermal expression of IL-19, IL-20 and IL-24. Br J Dermatol 167:92-102
39. Goldbach-Mansky R (2012) Immunology in clinic review series; focus on autoinflammatory diseases: update on monogenic autoinflammatory diseases: the role of interleukin (IL)-1 and an emerging role for cytokines beyond IL-1. Clin Exp Immunol 167:391-404
40. Ordas I, Mould DR, Feagan BG, Sandborn WJ (2012) Anti-TNF monoclonal antibodies in inflammatory bowel disease: pharmacokinetics-based dosing paradigms. Clin Pharmacol Ther 91:635-646
41. Yokoi N, Komeda K, Wang HY et al (2002) Cblb is a major susceptibility gene for rat type 1 diabetes mellitus. Nat Genet 31:391-394
42. Bonner-Weir S, Li WC, Ouziel-Yahalom L, Guo L, Weir GC, Sharma A (2010) Beta-cell growth and regeneration: replication is only part of the story. Diabetes 59:2340-2348
43. Salpeter SJ, Klein AM, Huangfu D, Grimsby J, Dor Y (2010) Glucose and aging control the quiescence period that follows pancreatic beta cell replication. Development 137:3205-3213
44. Rabinovitch A, Suarez-Pinzon WL (1998) Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem Pharmacol 55:1139-1149
45. Bergmann L, Kröncke KD, Suschek C, Kolb H, Kolb-Bachofen V (1992) Cytotoxic action of IL-1 beta against pancreatic islets is mediated via nitric oxide formation and is inhibited by NG-monomethyl-L-arginine. FEBS Lett 299:103-106
46. Kacheva S, Lenzen S, Gurgul-Convey E (2011) Differential effects of proinflammatory cytokines on cell death and ER stress in insulin-secreting INS1E cells and the involvement of nitric oxide. Cytokine 55:195-201
47. Ortis F, Pirot P, Naamane N et al (2008) Induction of nuclear factor-kappaB and its downstream genes by TNF-alpha and IL-1beta has a pro-apoptotic role in pancreatic beta cells. Diabetologia 51:1213-1225
48. Sleater M, Diamond AS, Gill RG (2007) Islet allograft rejection by contact-dependent CD8+ T cells: perforin and FasL play alternate but obligatory roles. Am J Transplant 7:1927-1933
49. Barthson J, Germano CM, Moore F et al (2011) Cytokines tumor necrosis factor-alpha and interferon-gamma induce pancreatic beta-cell apoptosis through STAT1-mediated Bim protein activation. J Biol Chem 286:39632-39643
50. Walz M, Overbergh L, Mathieu C, Kolb H, Martin S (2002) A murine interleukin-4-Ig fusion protein regulates the expression of Th1- and Th2-specific cytokines in the pancreas of NOD mice. Horm Metab Res 34:561-569