Impaired immune responses in streptozotocin-induced type I diabetes in mice. Involvement of high glucose

Clinical and Experimental Immunology

Volumn 154, Issue 2, 2008, Pages 235-246

  Rubinstein, R ^a   Genaro, A M ^a   Motta, A ^a   Cremaschi, G ^a   Wald, M R ^a  

^a Centre de Estudios Farmacologicos y Botanicos   (Argentina)

Author keywords

Diabetes; High glucose; Immune response; Oxidative stress; T and B lymphocyte proliferation

Indexed keywords

GLUCOSE; IMMUNOGLOBULIN G; T LYMPHOCYTE ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DISEASE DURATION; DOSE TIME EFFECT RELATION; FEMALE; HYPERGLYCEMIA; IMMUNE DEFICIENCY; IMMUNITY; IMMUNOGLOBULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; SECONDARY IMMUNE RESPONSE; SPLEEN CELL; SUPERNATANT; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FEMALE; GLUCOSE; HYPERGLYCEMIA; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LIPID PEROXIDATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MITOGENS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; T-LYMPHOCYTES;

EID: 53349109076     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2008.03742.x     Document Type: Article

References (75)

1. Peleg AY, Weerarathna T, McCarthy JS, Davis TM. Common infections in diabetes: pathogenesis, management and relationship to glycaemic control. Diabetes Metab Res Rev 2007 23 : 3 13.
2. Joshi N, Caputo GM, Weitekamp MR, Karchmer AW. Infections in patients with diabetes mellitus. N Engl J Med 1999 341 : 1906 12.
3. Pozzilli P, Leslie RD. Infections and diabetes: mechanisms and prospects for prevention. Diabet Med 1994 11 : 935 41.
4. Wheat LJ. Infection and diabetes mellitus. Diabetes Care 1980 3 : 187 97.
5. Bertoni AG, Saydah S, Brancati FL. Diabetes and the risk of infection-related mortality in the U.S. Diabetes Care 2001 24 : 1044 9.
6. McMahon MM, Bistrian BR. Host defenses and susceptibility to infection in patients with diabetes mellitus. Infect Dis Clin North Am 1995 9 : 1 9.
7. DCCT: The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993 329 : 977 86.
8. DCCT: The Diabetes Control and Complications Trial Research Group. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005 353 : 2643 53.
9. UK Prospective Diabetes Study Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 1998 352 : 854 65.
10. Furnary AP, Zerr KJ, Grunkemeier GL, Starr A. Continuous intravenous insulin infusion reduces the incidence of deep sternal wound infection in diabetic patients after cardiac surgical procedures. Ann Thorac Surg 1999 67 : 352 60.
11. Butler SO, Btaiche IF, Alaniz C. Relationship between hyperglycemia and infection in critically ill patients. Pharmacotherapy 2005 25 : 963 76.
12. Latham R, Lancaster AD, Covington JF, Pirolo JS, Thomas CS. The association of diabetes and glucose control with surgical-site infections among cardiothoracic surgery patients. Infect Control Hosp Epidemiol 2001 22 : 607 12.
13. Christiansen C, Toft P, Jorgensen HS, Andersen SK, Tonnesen E. Hyperglycaemia and mortality in critically ill patients. A prospective study. Intensive Care Med 2004 30 : 1685 8.
14. Baynes JW. Role of oxidative stress in the development of complications in diabetes. Diabetes 1991 40 : 405 12.
15. 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.
16. Schreck R, Baeuerle PA. A role for oxygen radicals as second messengers. Trends Cell Biol 1991 1 : 39 42.
17. Burdon RH. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol Med 1995 18 : 775 94.
18. Whitacre CM, Cathcart MK. Oxygen free radical generation and regulation of proliferative activity of human mononuclear cells responding to different mitogens. Cell Immunol 1992 144 : 287 95.
19. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 2003 52 : 1 8.
20. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001 414 : 813 20.
21. Vincent AM, Russell JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocrine Reviews 2004 25 : 612 28.
22. Ceriello A, Bortolotti N, Crescentini A et al. Antioxidant defenses are reduced during the oral glucose tolerance test in normal and non-insulin-dependent diabetic subjects. Eur J Clin Invest 1998 28 : 329 33.
23. Merzouk S, Hichami A, Madani S et al. Antioxidant status and levels of different vitamins determined by high performance liquid chromatography in diabetic subjects with multiple complications. Gen Physiol Biophys 2003 22 : 15 27.
24. Tessier D, Khalil A, Fülöp T. Effects of an oral glucose challenge on free radicals/antioxidants balance in an older population with type II diabetes. J Gerontol A Biol Sci Med Sci 1999 54 : M541 5.
25. Giugliano D, Ceriello A, P. Oxidative stress and diabetic vascular complications. Diabetes Care 1996 19 : 257 67.
26. Rodríguez-Mañas L, Angulo J, Vallejo S et al. Early and intermediate Amadori glycosylation adducts, oxidative stress, and endothelial dysfunction in the streptozotocin-induced diabetic rats vasculature. Diabetologia 2003 46 : 556 66.
27. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H. Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 2003 14 (8 Suppl. 3 S241 5.
28. Ha H, Kim KH. Pathogenesis of diabetic nephropathy: the role of oxidative stress and protein kinase C. Diabetes Res Clin Pract 1999 45 : 147 51.
29. Dröge W, Eck HP, Mihm S. HIV-induced cysteine deficiency and T-cell dysfunction-a rationale for treatment with N-acetylcysteine. Immunol Today 1992 13 : 211 14.
30. Staal FJ, Ela SW, Roederer M, Anderson MT, Herzenberg LA, Herzenberg LA. Glutathione deficiency and human immunodeficiency virus infection. Lancet 1992 339 : 909 12.
31. Robinson MK, Rodrick ML, Jacobs DO et al. Glutathione depletion in rats impairs T-cell and macrophage immune function. Arch Surg 1993 128 : 29 34.
32. Like AA, Rossini AA. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 1976 193 : 415 17.
33. Silberman DM, Wald MR, Genaro AM. Acute and chronic stress exerts opposing effects on antibody responses associated with changes in stress hormone regulation of T-lymphocyte reactivity. J Neuroimmunol 2003 144 : 53 60.
34. Silberman DM, Wald M, Genaro AM. Effects of chronic mild stress on lymphocyte proliferative response. Participation of serum thyroid hormones and corticosterone. Int Immunopharmacol 2002 2 : 487 97.
35. Cazaux CA, Sterin-Borda L, Gorelik G, Cremaschi GA. Down-regulation of beta-adrenergic receptors induced by mitogen activation of intracellular signaling events in lymphocytes. FEBS Lett 1995 364 : 120 4.
36. Nicolletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 1991 139 : 271 9.
37. Zamai L, Falcieri E, Zauli G, Cataldi A, Vitale M. Optimal detection of apoptosis by flow cytometry depends on cell morphology. Cytometry 1993 14 : 891 7.
38. Bass DA, Parce JW, Dechatelet LR, Szejda P, Seeds MC, Thomas M. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J Immunol 1983 130 : 1910 17.
39. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1979 52 : 302 10.
40. Cerami A, Vlassara H, Brownlee M. Role of advanced glycosylation products in complications of diabetes. Diabetes Care 1988 1 : 73 9.
41. Imani F, Horii Y, Suthanthiran M et al. Advanced glycosylation endproduct-specific receptors on human and rat T-lymphocytes mediate synthesis of interferon gamma: role in tissue remodeling. J Exp Med 1993 178 : 2165 72.
42. Moser B, Desai DD, Downie MP et al. Receptor for advanced glycation end products expression on T cells contributes to antigen-specific cellular expansion in vivo. J Immunol 2007 179 : 8051 8.
43. Leiter EH, Le PH, Prochazka M, Worthen SM, Huppi K. Genetic and environmental control of diabetes induction by multi-dose streptozotocin in two BALB/c substrains. Diabetes Res 1988 9 : 5 10.
44. Eibl N, Spatz M, Fischer GF et al. Impaired primary immune response in type-1 diabetes: results from a controlled vaccination study. Clin Immunol 2002 103 : 249 59.
45. Moutschen MP, Scheen AJ, Lefebvre PJ. Impaired immune responses in diabetes mellitus: analysis of the factors and mechanisms involved. Relevance to the increased susceptibility of diabetic patients to specific infections. Diabete Metab 1992 18 : 187 201.
46. Saiki O, Negoro S, Tsuyuguchi I, Yamamura Y. Depressed immunological defence mechanisms in mice with experimentally induced diabetes. Infect Immun 1980 28 : 127 31.
47. Chang FY, Shaio MF. Decreased cell-mediated immunity in patients with non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract 1995 28 : 137 46.
48. Plouffe JF, Silva J, Fekety R, Allen JL. Cell-mediated immunity in diabetes mellitus. Infect Immun 1978 21 : 425 29.
49. De Maria R, Todaro M, Stassi G et al. Cell receptor/CD3 complex signaling in human type I diabetes. Eur J Immunol 1994 24 : 999 1002.
50. Sakowicz-Burkiewicz M, Kocbuch K, Grden M, Szutowicz A, Pawelczyk T. Diabetes-induced decrease of adenosine kinase expression impairs the proliferation potential of diabetic rat T lymphocytes. Immunology 2006 118 : 402 12.
51. Stratton IM, Adler AI, Neil H et al. On behalf of the UK Prospective Diabetes Study Group. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000 321 : 405 12.
52. Koya D, King GL. Protein kinase C activation and the development of diabetic complications. Diabetes 1998 47 : 859 66.
53. Yan SF, Ramasamy R, Schmidt AM. Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications. Nat Clin Pract Endocrinol Metab 2008 4 : 285 93.
54. Ceriello A, dello Russo P, Amstad P, Cerutti P. High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 1996 45 : 471 7.
55. Catherwood MA, Powell LA, Anderson P, McMaster D, Sharpe PC, Trimble ER. Glucose-induced oxidative stress in mesangial cells. Kidney Int 2002 61 : 599 608.
56. Ho FM, Liu SH, Liau CS, Huang PJ, Lin-Shiau SY. High glucose-induced apoptosis in human endothelial cells is mediated by sequential activations of c-Jun NH(2)-terminal kinase and caspase-3. Circulation 2000 101 : 2618 24.
57. Schmitt A, Bigl K, Meiners I, Schmitt J. Induction of reactive oxygen species and cell survival in the presence of advanced glycation end products and similar structures. Biochim Biophys Acta 2006 1763 : 927 36.
58. Novogrodsky A, Ravid A, Rubin AL, Stenzel KH. Hydroxyl radical scavengers inhibit lymphocyte mitogenest. Proc Natl Acad Sci USA 1982 79 : 1171 4.
59. Hamilos DL, Wedner HJ. The role of glutathione in lymphocyte activation. I. Comparison of inhibitory effects of buthionine sulfoximine and 2-cyclohexene-1-one by nuclear size transformation. J Immunol 1985 135 : 2740 7.
60. Hildeman DA, Mitchell T, Teague TK et al. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 1999 10 : 735 44.
61. Burton KP, McCord JM, Ghai G. Myocardial alterations due to free-radical generation. Am J Physiol 1984 246 : H776 83.
62. Stohs SJ. The role of free radicals in toxicity and disease. J Basic Clin Physiol Pharmacol 1995 6 : 205 28.
63. Buttke TM, Sandstrom PA. Redox regulation of programmed cell death in lymphocytes. Free Radic Res 1995 22 : 389 97.
64. Aukrust P, Svardal AM, Muller F et al. Increased levels of oxidized glutathione in CD4+ lymphocytes associated with disturbed intracellular redox balance in human immunodeficiency virus type 1 infection. Blood 1995 86 : 258 67.
65. Aukrust P, Svardal AM, Muller F, Lunden B, Berge RK, Froland SS. Decreased levels of total and reduced glutathione in CD4+ lymphocytes in common variable immunodeficiency are associated with activation of the tumor necrosis factor system: possible immunopathogenic role of oxidative stress. Blood 1995 86 : 1383 91.
66. Ceriello A, Quagliaro L, D'Amico M et al. Acute hyperglycemia induces nitrotyrosine formation and apoptosis in perfused heart from rat. Diabetes 2002 51 : 1076 82.
67. Frustaci A, Kajstura J, Chimenti C et al. Myocardial cell death in human diabetes. Circ Res 2000 87 : 1123 32.
68. von Harsdorf R, Li PF, Dietz R. Signaling pathways in reactive oxygen species-induced cardiomyocyte apoptosis. Circulation 1999 99 : 2934 41.
69. Baumgartner-Parzer SM, Wagner L, Pettermann M, Grillari J, Gessl A, Waldhausl W. High-glucose - triggered apoptosis in cultured endothelial cells. Diabetes 1995 44 : 1323 7.
70. Du XL, Sui GZ, Stockklauser-Farber K et al. Introduction of apoptosis by high proinsulin and glucose in cultured human umbilical vein endothelial cells is mediated by reactive oxygen species. Diabetologia 1998 41 : 249 56.
71. Wu QD, Wang JH, Fennessy F, Redmond HP, Bouchier-Hayes D. Taurine prevents high-glucose-induced human vascular endothelial cell apoptosis. Am J Physiol Cell Physiol 1999 277 : C1229 38.
72. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry 2003 27 : 283 90.
73. Chu Y, Faraci FM, Ooboshi H, Heistad DD. Increase in TUNEL positive cells in aorta from diabetic rats. Endothelium 1997 5 : 241 50.
74. Gallacher SJ, Thomson G, Fraser WD, Fisher BM, Gemmell CG, MacCuish AC. Neutrophil bactericidal function in diabetes mellitus: evidence for association with blood glucose control. Diabet Med 1995 12 : 916 20.
75. Rassias AJ, Marrin CA, Arruda J, Whalen PK, Beach M, Yeager MP. Insulin infusion improves neutrophil function in diabetic cardiac surgery patients. Anesth Analg 1999 88 : 1011 16.