Increased levels of type 1 interferon in a type 1 diabetic mouse model induce the elimination of B cells from the periphery by apoptosis and increase their retention in the spleen

Cellular Physiology and Biochemistry

Volumn 35, Issue 1, 2015, Pages 137-147

  Badr, Badr Mohamed ^a   Moustafa, Nadia Ahmed ^b   Eldien, Heba M Saad ^c   Mohamed, Amany O ^c   Ibrahim, Hany M ^a   El Elaimy, Ibrahim A ^a   Mahmoud, Mohamed H ^d,e   Badr, Gamal ^f  

^a Menoufia University   (Egypt)

^b Beni Suef University   (Egypt)

^c Assiut University Faculty of Medicine   (Egypt)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

^e NATIONAL RESEARCH CENTRE   (Egypt)

^f Assiut University   (Egypt)

Author keywords

Apoptosis; B lymphocytes; Diabetes mellitus; IFN ; Spleen

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; INSULIN; INTERFERON; INTERFERON ANTIBODY; ANTIBODY; LIPID; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; DYSLIPIDEMIA; ENZYME ACTIVITY; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SPLEEN; ANIMAL; B LYMPHOCYTE; BLOOD; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; EXPERIMENTAL DIABETES MELLITUS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; PANCREAS; PATHOLOGY; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; ANTIBODIES; APOPTOSIS; B-LYMPHOCYTES; CASPASE 3; CASPASE 8; CASPASE 9; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-SECRETING CELLS; INTERFERON TYPE I; LIPIDS; MICE; PANCREAS; SIGNAL TRANSDUCTION; SPLEEN; STREPTOZOCIN;

EID: 84921415156     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000369682     Document Type: Article

References (56)

1. Kelemen K: The role of T cells in beta cell damage in NOD mice and humans. Adv Exp Med Biol 2004;552:117-128.
2. Thomas H, Kay T: Beta cell destruction in the development of autoimmune diabetes in the non-obese diabetic (NOD) mouse. Diabetes Metab Res Rev 2000;16:251-261.
3. Beyan H, Buckley L, Yousaf N, Londei M, Leslie R: A role for innate immunity in type 1 diabetes. Diabetes Metab Res Rev 2003;19:89-100.
4. Silveira PA, and Grey ST: B-cells in the spotlight: innocent bystanders or major players in the pathogenesis of type 1 diabetes. Trends Endocrinol Metab 2006;17:128-135.
5. Noorchashm H, Noorchashm N, Kern J, Rostami SY, Barker CF, Naji A: B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes 1997;46:941-946.
6. Serreze DV, Chapman HD, Varnum DS, Hanson MS, Reifsnyder PC, Richard SD, Fleming SA, Leiter EH, Shultz LD: B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new speed congenic stock of NOD.Ig mu null mice. J Exp Med 1996;184:2049-2053.
7. Greeley SA, Katsumata M, Yu L, Eisenbarth GS, Moore DJ, Goodarzi H, Barker CF, Naji A, Noorchashm H: Elimination of maternally transmitted autoantibodies prevents diabetes in nonobese diabetic mice. Nat Med 2002;8:399-402.
8. Noorchashm H, Lieu YK, Noorchashm N, Rostami SY, Greeley SA, Schlachterman A, Song HK, Noto LE, Jevnikar AM, Barker CF, Naji A: I-Ag7-mediated antigen presentation by B lymphocytes is critical in overcoming a checkpoint in T cell tolerance to islet beta cells of nonobese diabetic mice. J Immunol 1999;163:743-750.
9. Serreze DV, Fleming SA, Chapman HD, Richard SD, Leiter EH, Tisch RM: B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Immunol, 1998;161:3912-3918.
10. Falcone M, Lee J, Patstone G, Yeung B, Sarvetnick N: B lymphocytes are crucial antigen-presenting cells in the pathogenic autoimmune response to GAD65 antigen in nonobese diabetic mice. J Immunol 1998;161:1163-1168.
11. Loder F, Mutschler B, Ray RJ, Paige CJ, Sideras P, Torres R, Lamers MC, Carsetti R: B-cell development in the spleen takes place in discrete steps and is determined by the quality of B-cell receptor-derived signals. J Exp Med 1999;190:75-89.
12. Martin F and Kearney JF: B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B-cells as part of a natural immune memory. Immunol Rev 2000;175:70-79.
13. Pillai S, Cariappa A, Moran ST: Marginal zone B-cells. Annu Rev Immunol 2005;23:161-196.
14. Song H and Cerny J: Functional heterogeneity of marginal zone B-cells revealed by their ability to generate both early antibody-forming cells and germinal centers with hypermutation and memory in response to a T-dependent antigen. J Exp Med 2003;198:1923-1935.
15. Snapper CM, Yamada H, Smoot D, Sneed R, Lees A, Mond JJ: Comparative in vitro analysis of proliferation, Ig secretion, and Ig class switching by murine marginal zone and follicular B-cells. J Immunol 1993;150:2737-2745.
16. Oliver AM, Martin F, Kearney JF: IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B-cells. J Immunol 1999;162:7198-7207.
17. Oliver AM, Martin F, Gartland GL, Carter RH, Kearney JF: Marginal zone B-cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur J Immunol 1997;27:2366-2374.
18. Attanavanich K and Kearney JF: Marginal zone, but not follicular B-cells, are potent activators of naive CD4 T cells. J Immunol 2004;172:803-811.
19. Martin F, Oliver AM, Kearney JF: Marginal zone and B1 B-cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001;14:617-629.
20. Rolf J, Motta V, Duarte N, Lundholm M, Berntman E, Bergman ML, Sorokin L, Cardell SL, Holmberg D: The enlarged population of marginal zone/ CD1d(high) B lymphocytes in nonobese diabetic mice maps to diabetes susceptibility region Idd11. J Immunol 2005;174:4821-4827.
21. Quinn WJ, Noorchashm N, Crowley JE, Reed AJ, Noorchashm H, Naji A, Cancro MP: Cutting edge: impaired transitional B-cell production and selection in the nonobese diabetic mouse. J Immunol 2006;176:7159-7164.
22. Thompson CS: Animal models of diabetes mellitus: relevance to vascular complications. Curr Pharm Des 2008;14:309-324.
23. Soedamah-Muthu SS, Chaturvedi N, Toeller M, Ferriss B, Reboldi P, Michel G, Manes C, Fuller JH: Risk factors for coronary heart disease in type 1 diabetic patients in Europe the EURODIAB Prospective Complications Study. Diabetes Care 2004;27:530-537.
24. Grauslund J, Jrgensen TM, Nybo M, Green A, Rasmussen LM, Sjlie AK: Risk factors for mortality and ischemic heart disease in patients with long-term type 1 diabetes. J Diabetes Complications 2010;24:223-228.
25. Edge JA, James T, Shine B: Longitudinal screening of serum lipids in children and adolescents with Type 1 diabetes in a UK clinic population. Diabet Med 2008;25:942-948.
26. Maahs DM, Ogden LG, Dabelea D, Snell-Bergeon JK, Daniels SR, Hamman RF, Rewers M: Association of glycaemia with lipids in adults with type 1 diabetes: modification by dyslipidaemia medication. Diabetologia 2010;53:2518-2525.
27. Theofilopoulos AN, Baccala R, Beutler B, Kono DH: Type 1interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 2005;23:307-336.
28. Baynes JW: Role of oxidative stress in development of complications in diabetes. Diabetes 1991;40:405-412.
29. Jain SK: Hyperglycemia can cause membrane lipid peroxidation and osmotic fragility in human red blood cells. J Biol Chem 1989;264:21340-21345.
30. Orhan H and Sahin G: Erythrocyte glutathione S-transferase activity in diabetes mellitus: the effect of the treatment. ABAD J Pharm Sci 1999;24:127-131.
31. Sato Y, Hotta N, and Sakamoto N: Lipid peroxide level in plasma of diabetic patients. Biochem Med 1979;21:104-107.
32. Kaji H, Kurasaki M, and Ito K: Increased lipoperoxide value and glutathione peroxidase activity in blood plasma of type 2 (non-insulin-dependent) diabetic women. Klin Wochenschr 1985;63:765-768.
33. Stewart TA, Hultgren B, Huang X, Pitts-Meek S, Hully J, MacLachlan NJ: Induction of type 1diabetes by interferon-alpha in transgenic mice. Science 1993;260:1942-1946.
34. Nakazawa T, Satoh J, Takahashi K, Sakata Y, Ikehata F, Takizawa Y, Bando SI, Housai T, Li Y, Chen C, Masuda T, Kure S, Kato I, Takasawa S, Taniguchi T, Okamoto H, Toyota T: Complete suppression of insulitis and diabetes in NOD mice lacking interferon regulatory factor-1. J Autoimmunity 2011;17:119-125.
35. Saad Eldien HM, El-Elaimy IA, Ibrahim HM, Badr BM, Badr G: Increased level of Type 1Interferon during Type 1diabetes induces apoptosis in spleen-homing T cells. African J Pharm Pharmacol 2012;6:2675-2681.
36. Ibrahim HM, El-Elaimy IA, Saad Eldien HM, Badr BM, Rabah DM, Badr G: Blocking type 1interferon signaling rescues lymphocytes from oxidative stress, exhaustion, and apoptosis in a streptozotocin-induced mouse model of type 1diabetes. Oxid Med Cell Longev 2013;12:148725.
37. Badr G, Waly H, Saad Eldien HM, Abdel-Tawab H, Hassan K, Alhazza IM, Ebaid H, Alwasel SH: Blocking type 1interferon (IFN) signaling impairs antigen responsiveness of circulating lymphocytes and alters their homing to lymphoid organs: protective role of type 1IFN. Cell Physiol Biochem 2010;26:1029-1040.
38. Kashino SS, Vallerskog T, Martens G, Troudt J, Keyser A, Taylor J, Izzo A, Kornfeld H, Campos-Neto A: Initiation of Acquired Immunity in the Lungs of Mice Lacking Lymph Nodes after Infection with Aerosolized Mycobacterium tuberculosis. Am J Pathol 2010;176:198-204.
39. Marino E, Batten M, Groom J, Walters S, Liuwantara D, Mackay F, Grey ST: Marginal zone B cells of Non-obese diabetic mice expand with diabetes onset; invade the pancreatic lymph nodes and present auto-antigen to diabetogenic T cells. Diabetes 2008;57:395-404.
40. Stolp J, Mario E, Batten M, Sierro F, Cox SL, Grey ST, Silveira PA: Intrinsic molecular factors cause aberrant expansion of the splenic marginal zone B cell population in nonobese diabetic mice. J Immunol 2014;191:97-109.
41. Huang X, Yuang J, Goddard A, Foulis A, James RF, Lernmark A, Pujol-Borrell R, Rabinovitch A, Somoza N, Stewart TA: Interferon expression in the pancreases of patients with type 1diabetes. Diabetes 1995;44:658-664.
42. Baynes JW: Role of oxidative stress in the development of complications in diabetes. Diabetes 1991; 40:405-412.
43. Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L: The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001;17:189-212.
44. Fabris P, Floreani A, Tositti G, Vergani D, De Lalla F, Betterle C: Type 1 diabetes mellitus in patients with chronic hepatitis C before and after interferon therapy. Aliment Pharmacol Ther 2003;18:549-558.
45. Guerci AP, Guerci B, Livy-Marchal C, Ongagna J, Ziegler O, Candiloros H, Guerci O, Drouin P: Onset of insulin-dependent diabetes mellitus after interferon-α therapy for hairy cell leukaemia. Lancet 1994;343:1167-1168.
46. Huang X, Hultgren B, Dybdal N, Stewart TA: Islet expression of interferon- α precedes diabetes in both the BB rat and streptozotocin-treated mice. Immunity 1994;1:469-478.
47. Vergs B: Insulin sensitiviy and lipids. Diabetes Metab 2001;27:223-227.
48. Ginsberg HN: Diabetic dyslipidemia: basic mechanisms underlying the common hypertriglyceridemia and low HDL cholesterol levels. Diabetes 1996;45:27-30.
49. Hellerstein MK, Grunfeld C, Wu K, Christiansen M, Kaempfer S, Kletke C, Shackleton CH: Increased de novo hepatic lipogenesis in human immunodeficiency virus infection. J Clin Endocrinol Metab 1993;76:559-565.
50. Tominaga M, Uno K, Yagi K, Fukui M, Hasegawa G, Yoshikawa T, Nakamura N: Association between capacity of interferon-alpha production and metabolic parameters. J Interferon Cytokine Res 2010;30:451-454.
51. Chan AC: Vitamin E and atherosclerosis. J Nutr 1998;128:1593-1596.
52. Whitacre CM and Cathcart MK: Oxygen free radical generation and regulation of proliferative activity of human mononuclear cells responding to different mitogens. Cell Immunol 1992;144: 287-295.
53. Burdon RH: Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol Med 1995;18:775-794.
54. Jaakkola I, Jalkanen S, Hanninen A: Diabetogenic T cells are primed both in pancreatic and gut-associated lymph nodes in NOD mice. Eur J Immunol 2003;33:3255-3264.
55. Hoglund P, Mintern J, Waltzinger C, Heath W, Benoist C, Mathis D: Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J Exp Med 1999;189:331-339.
56. Gagnerault MC, Luan JJ, Lotton C, Lepault F: Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J Exp Med 2002;196:369-377.