Immune-mediated β-cell death in type 1 diabetes: Lessons from human β-cell lines

European Journal of Clinical Investigation

Volumn 42, Issue 11, 2012, Pages 1244-1251

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

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

Author keywords

cells; cell killing; Autoimmunity; Human cell lines; Islets; Type 1 diabetes

Indexed keywords

INSULIN;

AUTOIMMUNITY; B LYMPHOCYTE; CELL DEATH; CELL KILLING; CELL LINE; CYTOTOXICITY; DISEASE COURSE; DISORDERS OF CARBOHYDRATE METABOLISM; ENVIRONMENTAL FACTOR; GLUCOSE BLOOD LEVEL; HEREDITY; HUMAN; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MITOCHONDRION; MOLECULAR MECHANICS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW;

AUTOIMMUNITY; CELL DEATH; CELL LINE; DIABETES MELLITUS, TYPE 1; HUMANS; INSULIN-SECRETING CELLS; PANCREAS;

EID: 84867744391     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/j.1365-2362.2012.02711.x     Document Type: Review

References (72)

1. Schatz D, Cuthbertson D, Atkinson M, Salzler MC, Winter W, Muir A et al. Preservation of C-peptide secretion in subjects at high risk of developing type 1 diabetes mellitus--a new surrogate measure of non-progression? Pediatr Diabetes 2004;5:72-9.
2. In't Veld P. Insulitis in human type 1 diabetes: The quest for an elusive lesion. Islets 2011;3:131-8.
3. Pescovitz MD, Greenbaum CJ, Krause-Steinrauf H, Becker DJ, Gitelman SE, Goland R et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N Engl J Med 2009;361:2143-52.
4. Zhang L, Eisenbarth GS. Prediction and prevention of Type 1 diabetes mellitus. J Diabetes 2011;3:48-57.
5. Martin S, Wolf-Eichbaum D, Duinkerken G, Scherbaum WA, Kolb H, Noordzij JG et al. Development of type 1 diabetes despite severe hereditary B-lymphocyte deficiency. N Engl J Med 2001;345:1036-40.
6. Hanafusa T, Imagawa A. Insulitis in human type 1 diabetes. Ann N Y Acad Sci 2008;1150:297-9.
7. Itoh N, Hanafusa T, Miyazaki A, Miyagawa J, Yamagata K, Yamamoto K et al. Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J Clin Invest 1993;92:2313-22.
8. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG. Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol 2009;155:173-81.
9. In't Veld P, Lievens D, De Grijse J, Ling Z, Van der Auwera B, Pipeleers-Marichal M et al. Screening for insulitis in adult autoantibody-positive organ donors. Diabetes 2007;56:2400-4.
10. Coppieters KT, Dotta F, Amirian N, Campbell PD, Kay TW, Atkinson MA 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.
11. Christianson SW, Shultz LD, Leiter EH. Adoptive transfer of diabetes into immunodeficient NOD-scid/scid mice. Relative contributions of CD4+ and CD8+ T-cells from diabetic versus prediabetic NOD.NON-Thy-1a donors. Diabetes 1993;42:44-55.
12. Velthuis JH, Unger WW, Abreu JR, Duinkerken G, Franken K, Peakman M et al. Simultaneous detection of circulating autoreactive CD8+ T-cells specific for different islet cell-associated epitopes using combinatorial MHC multimers. Diabetes 2010;59:1721-30.
13. Unger WW, Pinkse GG, Mulder-van der Kracht S, van der Slik AR, Kester MG, Ossendorp F et al. Human clonal CD8 autoreactivity to an IGRP islet epitope shared between mice and men. Ann N Y Acad Sci 2007;1103:192-5.
14. Narendran P, Williams AJ, Elsegood K, Leech NJ, Dayan CM. Humoral and cellular immune responses to proinsulin in adults with newly diagnosed type 1 diabetes. Diabetes Metab Res Rev 2003;19:52-9.
15. Skowera A, Ellis RJ, Varela-Calviño R, Arif S, Huang GC, Van-Krinks C et al. CTLs are targeted to kill beta cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope. J Clin Invest 2008;118:3390-402.
16. Campbell PD, Estella E, Dudek NL, Jhala G, Thomas HE, Kay TW et al. Cytotoxic T-lymphocyte-mediated killing of human pancreatic islet cells in vitro. Hum Immunol 2008;69:543-51.
17. Bulek AM, Cole DK, Skowera A, Dolton G, Gras S, Madura F et al. Structural basis for the killing of human beta cells by CD8(+) T cells in type 1 diabetes. Nat Immunol 2012;13:283-9.
18. Hohmeier HE, Newgard CB. Cell lines derived from pancreatic islets. Mol Cell Endocrinol 2004;228:121-8.
19. Soldevila G, Buscema M, Marini V, Sutton R, James RF, Bloom SR et al. Transfection with SV40 gene of human pancreatic endocrine cells. J Autoimmun 1991;4:381-96.
20. Gueli NTA, Palmieri G, Carmenini G, Delpino A, Ferrini U. In vitro growth of a cell line originated from a human insulinoma. J Exp Clin Cancer Res 1987;6:281.
21. Macfarlane WM, Cragg H, Docherty HM, Read ML, James RF, Aynsley-Green A et al. 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 1997;413:304-8.
22. Halvorsen TL, Leibowitz G, Levine F. Telomerase activity is sufficient to allow transformed cells to escape from crisis. Mol Cell Biol 1999;19:1864-70.
23. Narushima M, Kobayashi N, Okitsu T, Tanaka Y, Li SA, Chen Y et al. A human beta-cell line for transplantation therapy to control type 1 diabetes. Nat Biotechnol 2005;23:1274-82.
24. Ravassard P, Hazhouz Y, Pechberty S, Bricout-Neveu E, Armanet M, Czernichow P et al. A genetically engineered human pancreatic β cell line exhibiting glucose-inducible insulin secretion. J Clin Invest 2011;121:3589-97.
25. McCluskey JT, Hamid M, Guo-Parke H, McClenaghan NH, Gomis R, Flatt PR. Development and functional characterization of insulin-releasing human pancreatic beta cell lines produced by electrofusion. J Biol Chem 2011;286:21982-92.
26. Lieber M, Mazzetta J, Nelson-Rees W, Kaplan M, Todaro G. Establishment of a continuous tumor-cell line (panc-1) from a human carcinoma of the exocrine pancreas. Int J Cancer 1975;15:741-7.
27. Guo-Parke H, McCluskey JT, Kelly C, Hamid MH, McClenaghan NH, Flatt PR. Configuration of electrofusion derived human insulin-secreting cell line as pseudoislets enhances functionality and therapeutic utility. J Endocrinol 2012; Available at: http://www.ncbi.nlm.nih.gov/pubmed/22685334.
28. Soldevila G, Buscema M, Doshi M, James R, Bottazzo G, Pujol-Borrell R. Cytotoxic effect of IFN-gamma plus TNF-alpha on human islet cells. J Autoimmun 1991;4:291-306.
29. Vives M, Soldevila G, Alcalde L, Lorenzo C, Somoza N, Pujol-Borrell R. Adhesion molecules in human islet beta-cells. De novo induction of ICAM-1 but not LFA-3. Diabetes 1991;40:1382-90.
30. Vives-Pi M, Somoza N, Fernández-Alvarez J, Vargas F, Caro P, Alba A et al. Evidence of expression of endotoxin receptors CD14, toll-like receptors TLR4 and TLR2 and associated molecule MD-2 and of sensitivity to endotoxin (LPS) in islet beta cells. Clin Exp Immunol 2003;133:208-18.
31. Muñoz A, Gallart T, Gomis R. Analysis of islet cell antibodies reactivity to a human islet cell line. J Endocrinol Invest 1992;15:109-12.
32. Ou D, Metzger DL, Wang X, Huang J, Pozzilli P, Tingle AJ. TNF-related apoptosis-inducing ligand death pathway-mediated human beta-cell destruction. Diabetologia 2002;45:1678-88.
33. Ou D, Wang X, Metzger DL, Ao Z, Pozzilli P, James RF et al. Suppression of human T-cell responses to beta-cells by activation of B7-H4 pathway. Cell Transplant 2006;15:399-410.
34. Baroni MG, Cavallo MG, Mark M, Monetini L, Stoehrer B, Pozzilli P. Beta-cell gene expression and functional characterisation of the human insulinoma cell line CM. J Endocrinol 1999;161:59-68.
35. Monetini L, Cavallo MG, Barone F, Valente L, Russo M, Walker B et al. T cell reactivity to human insulinoma cell line (CM) antigens in patients with type 1 diabetes. Autoimmunity 1999;29:171-7.
36. Cavallo MG, Monetini L, Valente L, Barone F, Beales P, Russo M et al. Glutathione protects a human insulinoma cell line from tumor necrosis factor-alpha-mediated cytotoxicity. Int J Clin Lab Res 1997;27:44-7.
37. Burkart V, Liu H, Bellmann K, Wissing D, Jaattela M, Cavallo MG et al. Natural resistance of human beta cells toward nitric oxide is mediated by heat shock protein 70. J Biol Chem 2000;275:19521-8.
38. Ou D, Wang X, Metzger DL, Robbins M, Huang J, Jobin C et al. 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 2005;66:799-809.
39. Ou D, Wang X, Metzger DL, James RF, Pozzilli P, Plesner A et al. 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 2005;66:274-84.
40. Le Bacquer O, Shu L, Marchand M, Neve B, Paroni F, Kerr Conte J et al. TCF7L2 splice variants have distinct effects on beta-cell turnover and function. Hum Mol Genet 2011;20:1906-15.
41. Jonnakuty C, Gragnoli C. Karyotype of the human insulinoma CM cell line--beta cell model in vitro? J Cell Physiol 2007;213:661-2.
42. Gragnoli C. The CM cell line derived from liver metastasis of malignant human insulinoma is not a valid beta cell model for in vitro studies. J Cell Physiol 2008;216:569-70.
43. Cavallo MG, Pozzilli P, Misiti S, Baroni MG. Insulinoma CM cell line as in vitro model for beta-cell. J Cell Physiol 2008;216:568.
44. Macfarlane WM, Shepherd RM, Cosgrove KE, James RF, Dunne MJ, Docherty K. Glucose modulation of insulin mRNA levels is dependent on transcription factor PDX-1 and occurs independently of changes in intracellular Ca2+. Diabetes 2000;49:418-23.
45. Macfarlane WM, O'Brien RE, Barnes PD, Shepherd RM, Cosgrove KE, Lindley KJ et al. Sulfonylurea receptor 1 and Kir6.2 expression in the novel human insulin-secreting cell line NES2Y. Diabetes 2000;49:953-60.
46. Cosgrove KE, Straub SG, Barnes PD, Chapman J, Sharp GW, Dunne MJ. Y-26763: aTP-sensitive K+ channel activation and the inhibition of insulin release from human pancreatic beta-cells. Eur J Pharmacol 2004;486:133-9.
47. MacFarlane WM, Chapman JC, Shepherd RM, Hashmi MN, Kamimura N, Cosgrove KE et al. Engineering a glucose-responsive human insulin-secreting cell line from islets of Langerhans isolated from a patient with persistent hyperinsulinemic hypoglycemia of infancy. J Biol Chem 1999;274:34059-66.
48. Weng J, Macfarlane WM, Lehto M, Gu HF, Shepherd LM, Ivarsson SA et al. Functional consequences of mutations in the MODY4 gene (IPF1) and coexistence with MODY3 mutations. Diabetologia 2001;44:249-58.
49. Fürstova V, Kopska T, James RF, Kovar J. Comparison of the effect of individual saturated and unsaturated fatty acids on cell growth and death induction in the human pancreatic beta-cell line NES2Y. Life Sci 2008;82:684-91.
50. Němcová-Fürstová V, James RF, Kovář J. Inhibitory effect of unsaturated fatty acids on saturated fatty acid-induced apoptosis in human pancreatic β-cells: activation of caspases and ER stress induction. Cell Physiol Biochem 2011;27:525-38.
51. Tree TI, O'Byrne D, Tremble JM, MacFarlane WM, Haskins K, James RF et al. Evidence for recognition of novel islet T cell antigens by granule-specific T cell lines from new onset type 1 diabetic patients. Clin Exp Immunol 2000;121:100-5.
52. Adams GG, Uddin A, Vives-Pi M, Pujol-Borrell R, James RF. Characterisation of the NES2Y cell line and its use in the production of human glucose-responsive insulin producing (hGRIP) cell lines by cell-cell fusion. Islets 2009;1:117-23.
53. de laTourD, Halvorsen T, Demeterco C, Tyrberg B, Itkin-Ansari P, Loy M et al. Beta-cell differentiation from a human pancreatic cell line in vitro and in vivo. Mol Endocrinol 2001;15:476-83.
54. Lightfoot YL, Chen J, Mathews CE. Role of the mitochondria in immune-mediated apoptotic death of the human pancreatic β cell line βLox5. PLoS One 2011;6:e20617.
55. Tiedge M, Lortz S, Drinkgern J, Lenzen S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997;46:1733-42.
56. Gusdon AM, Corbett JA, Mathews CE. Type 1 diabetes: islet inflammation - the contribution of cytokines and beta cells. Drug Discov Today Dis Mech 2006;3:367-72.
57. Rabinovitch A, Sumoski W, Rajotte RV, Warnock GL. Cytotoxic effects of cytokines on human pancreatic islet cells in monolayer culture. J Clin Endocrinol Meta 1990;71:152-6.
58. Nerup J, Mandrup-Poulsen T, Helqvist S, Andersen HU, Pociot F, Reimers JI et al. On the pathogenesis of IDDM. Diabetologia 1994;37(Suppl 2):S82-9.
59. Corbett JA, McDaniel ML. Intraislet release of interleukin 1 inhibits beta cell function by inducing beta cell expression of inducible nitric oxide synthase. J Exp Med 1995;181:559-68.
60. Rabinovitch A, Suarez-Pinzon WL. Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem Pharmacol 1998;55:1139-49.
61. Uno S, Imagawa A, Okita K, Sayama K, Moriwaki M, Iwahashi H et al. 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 2007;50:596-601.
62. Liu D, Pavlovic D, Chen MC, Flodstrom M, Sandler S, Eizirik DL. Cytokines induce apoptosis in beta-cells isolated from mice lacking the inducible isoform of nitric oxide synthase (iNOS-/-). Diabetes 2000;49:1116-22.
63. Rabinovitch A, Suarez-Pinzon W, Strynadka K, Schulz R, Lakey J, Warnock G et al. Human pancreatic islet beta-cell destruction by cytokines is independent of nitric oxide production. J Clin Endocrinol Metab 1994;79:1058-62.
64. Welsh N, Margulis B, Borg LA, Wiklund HJ, Saldeen J, Flodström M et al. Differences in the expression of heat-shock proteins and antioxidant enzymes between human and rodent pancreatic islets: implications for the pathogenesis of insulin-dependent diabetes mellitus. Mol Med 1995;1:806-20.
65. Scarim AL, Heitmeier MR, Corbett JA. Heat shock inhibits cytokine-induced nitric oxide synthase expression by rat and human islets. Endocrinology 1998;139:5050-7.
66. Rabinovitch A. An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab Rev 1998;14:129-51.
67. Grunnet L, Aikin R, Tonnesen M, Paraskevas S, Blaabjerg L, Størling J et al. Proinflammatory cytokines activate the intrinsic apoptotic pathway in beta-cells. Diabetes 2009;58:1807-15.
68. Irawaty W, Kay TW, Thomas HE. Transmembrane TNF and IFNgamma induce caspase-independent death of primary mouse pancreatic beta cells. Autoimmunity 2002;35:369-75.
69. Rabinovitch A, Suarez-Pinzon W, Strynadka K, Ju Q, Edelstein D, Brownlee M et al. Transfection of human pancreatic islets with an anti-apoptotic gene (bcl-2) protects beta-cells from cytokine-induced destruction. Diabetes 1999;48:1223-9.
70. Barthson J, Germano CM, Moore F, Maida A, Drucker DJ, Marchetti P et al. Tumor necrosis factor-{alpha} and interferon-{gamma} induce pancreatic {beta}-cell apoptosis through STAT1-mediated Bim activation. J Biol Chem 2011;286:39632-43.
71. Mehmeti I, Gurgul-Convey E, Lenzen S, Lortz S. Induction of the intrinsic apoptosis pathway in insulin-secreting cells is dependent on oxidative damage of mitochondria but independent of caspase-12 activation. Biochim Biophys Acta 2011;1813:1827-35.
72. Borutaite V, Brown GC. Caspases are reversibly inactivated by hydrogen peroxide. FEBS Lett 2001;500:114-8.