Role of the mitochondria in immune-mediated apoptotic death of the human pancreatic β cell line βLox5

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Lightfoot, Yaíma L ^a   Chen, Jing ^a   Mathews, Clayton E ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYTOKINE; FAS ANTIGEN; GAMMA INTERFERON; MITOCHONDRIAL DNA; TUMOR NECROSIS FACTOR ALPHA; HEAT SHOCK PROTEIN;

APOPTOSIS; ARTICLE; CELL DESTRUCTION; CELL FUNCTION; CELL KILLING; CELL SELECTION; CELL STRAIN; CELL STRAIN BETALOX5; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; CROSS PRESENTATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRION; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; SIGNAL TRANSDUCTION; CELL LINE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; METABOLISM; NECROSIS;

EUKARYOTA;

ANTIGENS, CD95; APOPTOSIS; CASPASES; CELL LINE; DNA, MITOCHONDRIAL; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HEAT-SHOCK PROTEINS; HUMANS; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; MITOCHONDRIA; NECROSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79959596385     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020617     Document Type: Article

References (74)

1. Imagawa A, Hanafusa T, Tamura S, Moriwaki M, Itoh N, 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.
2. Mathews CE, (2005) Utility of murine models for the study of spontaneous autoimmune type 1 diabetes. Pediatr Diabetes 6: 165-177.
3. Eizirik DL, Colli ML, Ortis F, (2009) The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 5: 219-226.
4. Rabinovitch A, (1998) An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab Rev 14: 129-151.
5. 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.
6. Eizirik DL, Mandrup-Poulsen T, (2001) A choice of death-the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 44: 2115-2133.
7. Andersson AK, Flodström M, Sandler S, (2001) Cytokine-induced inhibition of insulin release from mouse pancreatic beta-cells deficient in inducible nitric oxide synthase. Biochem Biophys Res Commun 281: 396-403.
8. Bellmann K, Jäättelä M, Wissing D, Burkart V, Kolb H, (1996) Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett 391: 185-188.
9. Bellmann K, Wenz A, Radons J, Burkart V, Kleemann R, et al. (1995) Heat shock induces resistance in rat pancreatic islet cells against nitric oxide, oxygen radicals and streptozotocin toxicity in vitro. J Clin Invest 95: 2840-2845.
10. Chambers KT, Unverferth JA, Weber SM, Wek RC, Urano F, et al. (2008) The role of nitric oxide and the unfolded protein response in cytokine-induced beta-cell death. Diabetes 57: 124-132.
11. Corbett JA, Sweetland MA, Wang JL, Lancaster JR, McDaniel ML, (1993) Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans. Proc Natl Acad Sci U S A 90: 1731-1735.
12. Johannesen J, Karlsen AE, Pociot F, Roenn SG, Nerup J, (2003) Strain dependent rat iNOS promoter activity-correlation to identified WT1 transcription factor binding site. Autoimmunity 36: 167-175.
13. Liu D, Pavlovic D, Chen MC, Flodstrom M, Sandler S, et al. (2000) Cytokines induce apoptosis in beta-cells isolated from mice lacking the inducible isoform of nitric oxide synthase (iNOS-/-). Diabetes 49: 1116-1122.
14. Mathews CE, Suarez-Pinzon WL, Baust JJ, Strynadka K, Leiter EH, et al. (2005) Mechanisms Underlying Resistance of Pancreatic Islets from ALR/Lt Mice To Cytokine-Induced Destruction. J Immunol 175: 1248-1256.
15. Scarim AL, Heitmeier MR, Corbett JA, (1998) Heat shock inhibits cytokine-induced nitric oxide synthase expression by rat and human islets. Endocrinology 139: 5050-5057.
16. Thomas HE, Irawaty W, Darwiche R, Brodnicki TC, Santamaria P, et al. (2004) IL-1 receptor deficiency slows progression to diabetes in the NOD mouse. Diabetes 53: 113-121.
17. Grunnet LG, Aikin R, Tonnesen MF, Paraskevas S, Blaabjerg L, et al. (2009) Proinflammatory cytokines activate the intrinsic apoptotic pathway in beta-cells. Diabetes 58: 1807-1815.
18. Bottino R, Balamurugan AN, Bertera S, Pietropaolo M, Trucco M, et al. (2002) Preservation of human islet cell functional mass by anti-oxidative action of a novel SOD mimic compound. Diabetes 51: 2561-2567.
19. Bottino R, Balamurugan AN, Tse H, Thirunavukkarasu C, Ge X, et al. (2004) Response of human islets to isolation stress and the effect of antioxidant treatment. Diabetes 53: 2559-2568.
20. Hanafusa T, Imagawa A, (2008) Insulitis in human type 1 diabetes. Ann N Y Acad Sci 1150: 297-299.
21. Moriwaki M, Itoh N, Miyagawa J, Yamamoto K, Imagawa A, et al. (1999) Fas and Fas ligand expression in inflamed islets in pancreas sections of patients with recent-onset Type I diabetes mellitus. Diabetologia 42: 1332-1340.
22. Halvorsen TL, Leibowitz G, Levine F, (1999) Telomerase activity is sufficient to allow transformed cells to escape from crisis. Mol Cell Biol 19: 1864-1870.
23. Stephens LA, Thomas HE, Kay TW, (1997) Protection of NIT-1 pancreatic beta-cells from immune attack by inhibition of NF-kappaB. J Autoimmun 10: 293-298.
24. Stephens LA, Thomas HE, Ming L, Grell M, Darwiche R, et al. (1999) Tumor necrosis factor-alpha-activated cell death pathways in NIT-1 insulinoma cells and primary pancreatic beta cells. Endocrinology 140: 3219-3227.
25. Burkart V, Liu H, Bellmann K, Wissing D, Jaattela M, et al. (2000) Natural resistance of human beta cells toward nitric oxide is mediated by heat shock protein 70. J Biol Chem 275: 19521-19528.
26. Dai T, Patel-Chamberlin M, Natarajan R, Todorov I, Ma J, et al. (2009) Heat shock protein 27 overexpression mitigates cytokine-induced islet apoptosis and streptozotocin-induced diabetes. Endocrinology 150: 3031-3039.
27. Holcik M, Korneluk RG, (2001) XIAP, the guardian angel. Nat Rev Mol Cell Biol 2: 550-556.
28. Scaffidi P, Misteli T, Bianchi ME, (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
29. Steer SA, Scarim AL, Chambers KT, Corbett JA, (2006) Interleukin-1 stimulates beta-cell necrosis and release of the immunological adjuvant HMGB1. PLoS Med 3: e17.
30. Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB, (2004) Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 18: 1272-1282.
31. Narushima M, Kobayashi N, Okitsu T, Tanaka Y, Li SA, et al. (2005) A human beta-cell line for transplantation therapy to control type 1 diabetes. Nat Biotechnol 23: 1274-1282.
32. Baroni MG, Cavallo MG, Mark M, Monetini L, Stoehrer B, et al. (1999) Beta-cell gene expression and functional characterisation of the human insulinoma cell line CM. J Endocrinol 161: 59-68.
33. Cavallo MG, Dotta F, Monetini L, Dionisi S, Previti M, et al. (1996) Beta-cell markers and autoantigen expression by a human insulinoma cell line: similarities to native beta cells. J Endocrinol 150: 113-120.
34. Dorff G, Meyer G, Krone D, Pozzilli P, Zuhlke H, (2002) Neuronal NO synthase and its inhibitor PIN are present and influenced by glucose in the human beta-cell line CM and in rat INS-1 cells. Biol Chem 383: 1357-1361.
35. Monetini L, Cavallo MG, Barone F, Valente L, Russo M, et al. (1999) T cell reactivity to human insulinoma cell line (CM) antigens in patients with type 1 diabetes. Autoimmunity 29: 171-177.
36. Ou D, Metzger DL, Wang X, Huang J, Pozzilli P, et al. (2002) TNF-related apoptosis-inducing ligand death pathway-mediated human beta-cell destruction. Diabetologia 45: 1678-1688.
37. Ou D, Metzger DL, Wang X, Pozzilli P, Tingle AJ, (2002) beta-cell antigen-specific CD56(+) NKT cells from type 1 diabetic patients: autoaggressive effector T cells damage human CD56(+) beta cells by HLA-restricted and non-HLA-restricted pathways. Hum Immunol 63: 256-270.
38. Ou D, Wang X, Metzger DL, Ao Z, Pozzilli P, et al. (2006) Suppression of human T-cell responses to beta-cells by activation of B7-H4 pathway. Cell Transplant 15: 399-410.
39. Ou D, Wang X, Metzger DL, James RF, Pozzilli P, et al. (2005) Synergistic inhibition of tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in human pancreatic beta cells by Bcl-2 and X-linked inhibitor of apoptosis. Hum Immunol 66: 274-284.
40. Ou D, Wang X, Metzger DL, Robbins M, Huang J, et al. (2005) Regulation of TNF-related apoptosis-inducing ligand-mediated death-signal pathway in human beta cells by Fas-associated death domain and nuclear factor kappaB. Hum Immunol 66: 799-809.
41. Macfarlane WM, Cragg H, Docherty HM, Read ML, James RF, et al. (1997) Impaired expression of transcription factor IUF1 in a pancreatic beta-cell line derived from a patient with persistent hyperinsulinaemic hypoglycaemia of infancy (nesidioblastosis). FEBS Lett 413: 304-308.
42. Wang S, Beattie GM, Mally MI, Lopez AD, Hayek A, et al. (1997) Analysis of a human fetal pancreatic islet cell line. Transplant Proc 29: 2219.
43. Ball AJ, Abrahamsson AE, Tyrberg B, Itkin-Ansari P, Levine F, (2007) HES6 reverses nuclear reprogramming of insulin-producing cells following cell fusion. Biochem Biophys Res Commun 355: 331-337.
44. Demeterco C, Itkin-Ansari P, Tyrberg B, Ford LP, Jarvis RA, et al. (2002) c-Myc controls proliferation versus differentiation in human pancreatic endocrine cells. J Clin Endocrinol Metab 87: 3475-3485.
45. Itkin-Ansari P, Demeterco C, Bossie S, de la Tour DD, Beattie GM, et al. (2000) PDX-1 and cell-cell contact act in synergy to promote delta-cell development in a human pancreatic endocrine precursor cell line. Mol Endocrinol 14: 814-822.
46. Itkin-Ansari P, Geron I, Hao E, Demeterco C, Tyrberg B, et al. (2003) Cell-based therapies for diabetes: progress towards a transplantable human beta cell line. Ann N Y Acad Sci 1005: 138-147.
47. Chervonsky AV, Wang Y, Wong FS, Visintin I, Flavell RA, et al. (1997) The role of Fas in autoimmune diabetes. Cell 89: 17-24.
48. Su X, Hu Q, Kristan JM, Costa C, Shen Y, et al. (2000) Significant role for Fas in the pathogenesis of autoimmune diabetes. J Immunol 164: 2523-2532.
49. Suarez-Pinzon WL, Power RF, Rabinovitch A, (2000) Fas ligand-mediated mechanisms are involved in autoimmune destruction of islet beta cells in non-obese diabetic mice. Diabetologia 43: 1149-1156.
50. Anderson B, Park BJ, Verdaguer J, Amrani A, Santamaria P, (1999) Prevalent CD8(+) T cell response against one peptide/MHC complex in autoimmune diabetes. Proc Natl Acad Sci U S A 96: 9311-9316.
51. Amrani A, Verdaguer J, Thiessen S, Bou S, Santamaria P, (2000) IL-1alpha, IL-1beta, and IFN-gamma mark beta cells for Fas-dependent destruction by diabetogenic CD4(+) T lymphocytes. J Clin Invest 105: 459-468.
52. Barnhart BC, Alappat EC, Peter ME, (2003) The CD95 type I/type II model. Semin Immunol 15: 185-193.
53. Augstein P, Bahr J, Wachlin G, Heinke P, Berg S, et al. (2004) Cytokines activate caspase-3 in insulinoma cells of diabetes-prone NOD mice directly and via upregulation of Fas. J Autoimmun 23: 301-309.
54. Augstein P, Heinke P, Salzsieder E, Grimm R, Giebel J, et al. (2008) Dominance of cytokine- over FasL-induced impairment of the mitochondrial transmembrane potential (Deltapsim) in the pancreatic beta-cell line NIT-1. Diab Vasc Dis Res 5: 198-204.
55. Cetkovic-Cvrlje M, Eizirik DL, (1994) TNF-alpha and IFN-gamma potentiate the deleterious effects of IL-1 beta on mouse pancreatic islets mainly via generation of nitric oxide. Cytokine 6: 399-406.
56. Zumsteg U, Frigerio S, Holländer GA, (2000) Nitric oxide production and Fas surface expression mediate two independent pathways of cytokine-induced murine beta-cell damage. Diabetes 49: 39-47.
57. Corbett JA, Kwon G, Turk J, McDaniel ML, (1993) IL-1 beta induces the coexpression of both nitric oxide synthase and cyclooxygenase by islets of Langerhans: activation of cyclooxygenase by nitric oxide. Biochemistry 32: 13767-13770.
58. Eizirik DL, Sandler S, Welsh N, Cetkovic-Cvrlje M, Nieman A, et al. (1994) Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest 93: 1968-1974.
59. Gysemans C, Callewaert H, Overbergh L, Mathieu C, (2008) Cytokine signalling in the beta-cell: a dual role for IFNgamma. Biochem Soc Trans 36: 328-333.
60. Rabinovitch A, Suarez-Pinzon WL, Strynadka K, Schulz R, Lakey JR, et al. (1994) Human pancreatic islet beta-cell destruction by cytokines is independent of nitric oxide production. J Clin Endocrinol Metab 79: 1058-1062.
61. Rabinovitch A, Sumoski W, Rajotte RV, Warnock GL, (1990) Cytotoxic effects of cytokines on human pancreatic islet cells in monolayer culture. J Clin Endocrinol Metab 71: 152-156.
62. Soldevila G, Buscema M, Doshi M, James RF, Bottazzo GF, et al. (1991) Cytotoxic effect of IFN-gamma plus TNF-alpha on human islet cells. J Autoimmun 4: 291-306.
63. Suk K, Kim S, Kim YH, Kim KA, Chang I, et al. (2001) IFN-gamma/TNF-alpha synergism as the final effector in autoimmune diabetes: a key role for STAT1/IFN regulatory factor-1 pathway in pancreatic beta cell death. J Immunol 166: 4481-4489.
64. Jitrapakdee S, Wutthisathapornchai A, Wallace JC, MacDonald MJ, (2010) Regulation of insulin secretion: role of mitochondrial signalling. Diabetologia 53: 1019-1032.
65. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD, (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136.
66. Cai J, Yang J, Jones DP, (1998) Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1366: 139-149.
67. Candé C, Cecconi F, Dessen P, Kroemer G, (2002) Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 115: 4727-4734.
68. Candé C, Vahsen N, Garrido C, Kroemer G, (2004) Apoptosis-inducing factor (AIF): caspase-independent after all. Cell Death Differ 11: 591-595.
69. Li JH, Pober JS, (2005) The cathepsin B death pathway contributes to TNF plus IFN-gamma-mediated human endothelial injury. J Immunol 175: 1858-1866.
70. Thomas HE, McKenzie MD, Angstetra E, Campbell PD, Kay TW, (2009) Beta cell apoptosis in diabetes. Apoptosis 14: 1389-1404.
71. Foulis AK, (2008) Pancreatic pathology in type 1 diabetes in human. Novartis Found Symp 292: 2-13; discussion 13-18, 122-129, 202-123.
72. Chen J, Hattori Y, Nakajima K, Eizawa T, Ehara T, et al. (2006) Mitochondrial complex I activity is significantly decreased in a patient with maternally inherited type 2 diabetes mellitus and hypertrophic cardiomyopathy associated with mitochondrial DNA C3310T mutation: a cybrid study. Diabetes Res Clin Pract 74: 148-153.
73. Cunha-Oliveira T, Rego AC, Cardoso SM, Borges F, Swerdlow RH, et al. (2006) Mitochondrial dysfunction and caspase activation in rat cortical neurons treated with cocaine or amphetamine. Brain Res 1089: 44-54.
74. Domingues AF, Esteves AR, Swerdlow RH, Oliveira CR, Cardoso SM, (2008) Calpain-mediated MPP+ toxicity in mitochondrial DNA depleted cells. Neurotox Res 13: 31-38.