Insulin secretion, DNA damage, and apoptosis in human and rat islets of langerhans following exposure to nitric oxide, peroxynitrite, and cytokines

Nitric Oxide - Biology and Chemistry

Volumn 2, Issue 6, 1998, Pages 429-441

  Hadjivassiliou, V ^a   Green, M H L ^a,b   James, R F L ^c   Swift, S M ^c   Clayton, H A ^c   Green, I C ^a,b  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY OF BRIGHTON   (United Kingdom)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Apoptosis; Comet assay; Cytokines; Insulin secretion; Islets of Langerhans; Superoxide

Indexed keywords

ARGININE DERIVATIVE; DNA; GLUCOSE; HYPOXANTHINE; INSULIN; LINSIDOMINE; NITRIC OXIDE; NITRIC OXIDE DONOR; PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; RECOMBINANT CYTOKINE; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 1BETA; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; S NITROSOGLUTATHIONE; XANTHINE OXIDASE;

ADULT; AGED; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DIABETES MELLITUS; DNA DAMAGE; DNA STRAND BREAKAGE; FEMALE; HUMAN; HUMAN TISSUE; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT;

ANIMALIA;

EID: 0032434935     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1006/niox.1998.0203     Document Type: Article

References (74)

1. Mandrup-Poulsen T., Bendtzen K., Nerup J., Dinarello C. A., Svenson M., Nielsen J. Affinity-purified human interleukin-1 is cytotoxic to isolated islets of Langerhans. Diabetologia. 29:1986;63-67.
2. Comens P., Wolf B. A., Unanue E. R., Lacy P. E., McDaniel M. L. Interleukin 1 is a potent modulator of insulin secretion from isolated rat islets of Langerhans. Diabetes. 36:1987;963-970.
3. Southern C., Schulster D., Green I. C. Inhibition of insulin secretion by interleukin-1β and tumour necrosis factor-α via anL. FEBS Lett. 276:1990;42-44.
4. Sandler S., Andersson A., Hellerström C. Inhibitory effects of interleukin 1 on insulin secretion, insulin biosynthesis, and oxidative metabolism of isolated rat pancreatic islets. Endocrinology. 121:1987;1424-1431.
5. Spinas G. A., Hansen B. S., Linde S., Kastern W., Molvig J., Mandrup-Poulsen T., Dinarello C. A., Nielsen J. H., Nerup J. Interleukin-1 dose-dependently affects the biosynthesis of (pro)insulin in isolated rat islets of Langerhans. Diabetologia. 30:1987;474-478.
6. Di Matteo M. A., Loweth A. C., Thomas S., Mabley J. G., Morgan N. G., Thorpe J. R., Green I. C. Superoxide, nitric oxide, peroxynitrite and cytokine combinations all cause functional impairment and morphological changes in rat islets of Langerhans and insulin-secreting cell lines but dictate cell death by different mechanisms. Apoptosis. 2:1997;164-177.
7. Southern C., Schulster D., Green I. C. Inhibition of insulin secretion from rat islets of Langerhans by interleukin-6 - An effect distinct from that of interleukin-1. Biochem. J. 272:1990;243-245.
8. Bolaffi J. L., Rodd G. G., Wang J., Grodsky G. M. Interrelationship of changes in islet nicotine adeninedinucleotide, insulin secretion, and cell viability induced by interleukin-1β Endocrinology. 134:1994;537-542.
9. Mehta V., Hao W., Brooks-Worrell B. M., Palmer J. P. The functional state of the β-cell modulates IL-1 and TNF-induced cytotoxicity. Lymph. Cyto. Res. 12:1993;255-259.
10. Rabinovitch A., Baquerizo H., Sumoski W. Cytotoxic effects of cytokines on islet β-cells: Evidence for involvement of eicosanoids. Endocrinology. 126:1990;67-71.
11. Kaneto H., Fujii J., Seo H. G., Suzuki K., Matsuoka T., Nakamura M., Tatsumi H., Yamasaki Y., Kamada T., Taniguchi N. Apoptotic cell death triggered by nitric oxide in pancreatic β-cells. Diabetes. 44:1995;733-738.
12. Dunger A., Augstein P., Schmidt S., Fischer U. Identification of interleukin-1-induced apoptosis in rat islets using in situ specific labelling of fragmented DNA. J. Autoimmun. 9:1996;309-313.
13. Eizirik D. L., Welsh N., Hellerström C. Predominance of stimulatory effects of interleukin-1β on isolated human pancreatic islets. J. Clin. Endocrinol. Metab. 76:1993;399-403.
14. Vara E., Arias-Días J., García C., Balibrea J. L. Effect of cytokines on insulin release and glucose oxidation by cultured human islets of ventral and dorsal origin. Transpl. Proc. 26:1994;695-697.
15. Mandrup-Poulsen T., Helqvist S., Wogensen L. D., Molvig J., Pociot F., Johannesen J., Nerup J. Cytokines and free radicals as effector molecules in the destruction of pancreatic β cells. Human Diabetes - Genetic, Environmental and Autoimmune Etiology. 1990;Springer, Berlin/Heidelberg/New York. p. 166-193.
16. Cunningham J. M., Green I. C. Cytokines, nitric oxide and insulin secreting cells. Growth Regul. 4:1994;173-180.
17. Mandrup-Poulsen T. The role of interleukin-1 in the pathogenesis of IDDM. Diabetologia. 39:1996;1005-1029.
18. Mandrup-Poulsen T., Bendtzen K., Dinarello C. A., Nerup J. Human tumor necrosis factor potentiates human interleukin-1-mediated rat pancreatic beta-cell cytotoxicity. J. Immunol. 139:1987;4077-4082.
19. Heitmeier M. R., Scarim A. L., Corbett J. A. Interferon-γ increases the sensitivity of islets of Langerhans for inducible nitric-oxide synthase expression induced by interleukin 1. J. Biol. Chem. 272:1997;13697-13704.
20. Corbett J. A., Lancaster J. R. J., Sweetland M. A., McDaniel M. L. Interleukin-1β-induced formation of EPR-detectable iron-nitrosyl complexes in islets of Langerhans. J. Biol. Chem. 266:1991;21351-21354.
21. Rabinovitch A., Suarez W. L., Thomas P. D., Strynadka K., Simpson I. Cytotoxic effects of cytokines on rat islets: Evidence for involvement of free radicals and lipid peroxidation. Diabetologia. 35:1992;409-413.
22. Dunger A. M., Cunningham J., Delaney C. A., Lowe J. E., Green M. H. L., Bone A. J., Green I. C. Tumour necrosis factor-α and interferon-γ inhibit insulin secretion and cause DNA damage in unweaned-rat islets: Extent of nitric oxide involvement. Diabetes. 45:1996;183-189.
23. Kawahara D. J., Kenney J. S. Species difference in human and rat islet sensitivity to human cytokines: Monoclonal anti-interleukin-1 (IL-1) influences on direct and indirect IL-1-mediated islet effects. Cytokine. 3:1991;117-124.
24. Soldevila G., Buscema M., Doshi M., James R. F. L., Bottazzo G. F., Pujol-Borrell R. Cytotoxic effect of IFN-γ plus TNF-α on human islet cells. J. Autoimmun. 4:1991;291-306.
25. Corbett J. A., Lin Wang J., Misko T. P., Zhao W., Hickey W. F., McDaniel M. L. Nitric oxide mediates IL-β-induced islet dysfunction and destruction: Prevention by dexamethasone. Autoimmunity. 15:1993;145-153.
26. Eizirik D. L., Sandler S., Welsh N., Cetkovic-Cvrlje M., Nieman A., Geller D. A., Pipeleers D. G., Bendtzen K., Hellerström C. Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J. Clin. Invest. 93:1994;1968-1974.
27. Corbett J. A., Sweetland M. A., Wang J. L., Lancaster J. R., McDaniel M. L. Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans. Proc. Natl. Acad. Sci. USA. 90:1993;1731-1735.
28. Rabinovitch A., Suarez-Pinzon W. L., Strynadka K., Schulz R., Lakey J. R. T., Warnock G. L., Rajotte R. V. Human pancreatic islet β-cell destruction by cytokines is independent of nitric oxide production. J. Clin. Endocrinol. Metab. 79:1994;1058-1062.
29. Flodström M., Welsh N., Eizirik D. L. Cytokines activate the nuclear factor κB (NFκB) and induce nitric oxide production in human pancreatic islets. FEBS Lett. 385:1996;4-6.
30. Rabinovitch A., Suarez-Pinzon W. L., Strynadka K., Lakey J. R. T., Rajotte R. V. Human pancreatic islet β-cell destruction by cytokines involves oxygen free radicals and aldehyde production. J. Clin. Endocrinol. Metab. 81:1996;3197-3202.
31. Mandrup-Poulsen T., Egeberg J., Nerup J., Bendtzen K., Nielsen J. H., Dinarello C. A. Ultrastructural studies of time-course and cellular specificity of interleukin-1 mediated islet cytotoxicity. Acta Pathol. Microbiol. Immunol. Scand. 95:1987;55-63.
32. Eizirik D. L., Pipeleers D. G., Ling Z., Welsh N., Hellerström C., Andersson A. Major species differences between humans and rodents in the susceptibility to pancreatic β-cell injury. Proc. Natl. Acad. Sci. USA. 91:1994;9253-9256.
33. Eizirik D. L., Delaney C. A., Green M. H. L., Cunningham J. M., Thorpe J. R., Pipeleers D. G., Hellerström C., Green I. C. Nitric oxide donors decrease the function and survival of human pancreatic islets. Mol. Cell. Endocrinol. 118:1996;71-83.
34. Cunningham J. M., Mabley J. G., Delaney C. A., Green I. C. The effect of nitric oxide donors on insulin secretion, cyclic GMP and cyclic AMP in rat islets of Langerhans and the insulin-secreting lines HIT-T15 and RINm5F. Mol. Cell. Endocrinol. 102:1994;23-29.
35. Kröncke K. D., Kolb-Bachofen V., Berschick B., Burkart V., Kolb H. Activated macrophages kill pancreatic syngenic islet cells via arginine-dependent nitric oxide generation. Biochem. Biophys. Res. Commun. 175:1991;752-758.
36. Mandrup-Poulsen T., Corbett J. A., McDaniel M. L., Nerup J. What are the types and cellular sources of free-radicals in the pathogenesis of type-1 (insulin-dependent) diabetes-mellitus? Diabetologia. 36:1993;470-471.
37. Ames B. N., Gold L. S. Endogenous mutagens and the causes of aging and cancer. Mutat. Res. 250:1991;3-16.
38. McKelvey-Martin V. J., Green M. H. L., Schmezer P., Pool-Zobel B. L., De Méo M. P., Collins A. The single cell gel electrophoresis (comet assay): A European review. Mutat. Res. 288:1993;47-63.
39. Delaney C. A., Green M. H. L., Lowe J. E., Green I. C. Endogenous nitric oxide induced by interleukin-1β in rat islets of Langerhans and HIT-T15 cells causes significant DNA damage as measured by the 'comet' assay. FEBS Lett. 333:1993;291-295.
40. Delaney C. A., Pavlovic D., Hoorens A., Pipeleers D. G., Eizirik D. L. Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells. Endocrinology. 138:1997;2610-2614.
41. Loweth A. C., Williams G. T., James R. F. L., Scarpello J. H. B., Morgan N. G. Human islets of Langerhans constitutively express Fas-Ligand and undergo apoptosis in response to interleukin-1β and Fas ligation. Diabetes. 47:1998;727-732.
42. Green M. H. L., Lowe J. E., Delaney C. A., Green I. C. Comet assay to detect nitric oxide-dependent DNA damage in mammalian cells. Packer L. Methods in Enzymology (Nitric Oxide). 1996;243-267 Academic Press, New York.
43. Mabley J. G., Belin V. D., John N. E., Green I. C. Insulin-like growth factor 1 reverses interleukin-1β inhibition of insulin secretion, induction of nitric oxide synthase and cytokine-mediated apoptosis in rat islets of Langerhans. FEBS Lett. 417:1997;235-238.
44. Ricordi C., Lacy P. E., Finke E. H., Olack B. J., D. W. S. Automated method for isolation of human pancreatic islets. Diabetes. 37:1988;413-420.
45. Robertson G. S. M., Chadwick D. R., Contractor H., London N. J. M., James R. F. L. The optimization of large scale density human islet isolation. Acta Diabetol. 30:1993;93-98.
46. White R., Crow J., Spear N., Thomas S., Patel R., Green I., Beckman J., Darley-Usmar V. Titherage M. A. Making and Working with Peroxynitrite: Nitric Oxide Protocols. 1998;Humana, Totowa.
47. Pryor W. A., Cueto R., Jln X., Ngu-Schwemlein M., Squadrito G. L., Uppu P. L., Uppu R. M. A practical method for preparing peroxynitrite solutions of low ionic strength and free of hydrogen peroxide. Free Rad. Biol. Med. 18:1995;75-83.
48. Delaney C. A., Tyrberg B., Bouwens L., Vaghef H., Hellman B., Eizirik D. L. Sensitivity of human pancreatic islets to peroxynitrite-induced cell dysfunction and death. FEBS Lett. 394:1996;300-306.
49. Szabo C., Zingarelli B., O'Connor M., Salzman A. L. DNA strand breakage, activation of poly(ATP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity in macrophages and smooth muscle cells exposed to peroxynitrite. Proc. Natl. Acad. Sci. USA. 93:1996;1753-1758.
50. Beckman J. S., Beckman T. W., Chen J., Marshall P. A., Freeman B. A. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87:1990;1620-1624.
51. Green I. C., Delaney C. A., Cunningham J. M., Karmiris V., Southern C. Interleukin-1β effects on cyclic GMP and cyclic AMP in cultured rat islets of Langerhans - Arginine-dependence and relationship to insulin secretion. Diabetologia. 36:1993;9-16.
52. Green I. C., Perrin D., Penman E., Ray K., Howell S. L. Effect of dynorphin on insulin and somatostatin secretion, calcium uptake and cAMP levels in isolated rat islets of Langerhans. Diabetes. 32:1983;685-690.
53. Spinas G. A., Mandrup-Poulsen T., Molvig J., Baek L., Bendtzen K., Dinarello C. A., Nerup J. Low concentrations of interleukin-1 stimulate and high concentrations inhibit insulin release from isolated rat islets of Langerhans. Acta Endocrinol. 113:1986;551-558.
54. Eizirik D. L., Sandler S., Welsh N., Bendtzen K., Hellerström C. Nicotinamide decreases nitric oxide production and partially protects human pancreatic islets against the suppressive effects of combinations of cytokines. Autoimmunity. 19:1994;193-198.
55. Sumoski W., Baquerizo H., Rabinovitch A. Oxygen free radical scavengers protect rat islet cells from damage by cytokines. Diabetologia. 32:1989;792-796.
56. Panagiotidis G., Åkesson B., Rydell E. L., Lundquist I. Influence of nitric oxide synthase inhibition, nitric oxide and hydroperoxide on insulin release induced by various secretagogues. Br. J. Pharmacol. 114:1995;289-296.
57. Fehsel K., Jalowy A., Qi S., Burkart V., Hartmann B., Kolb H. Islet cell DNA is a target of inflammatory attack by nitric oxide. Diabetes. 42:1993;496-500.
58. Rabinovitch A., Suarez-Pinzon W. L., Shi Y., Morgan A. R., Bleackley R. C. DNA fragmentation is an early event in cytokine-induced islet beta-cell destruction. Diabetologia. 37:1994;733-738.
59. Green I. C., Delaney C. A., Cunningham J. M., Mabley J. G., Di Matteo M. A., Green M. H. L. Cytokines, nitric oxide, DNA damage and insulin secreting cells. Environ. Mutat. Res. Commun. 16:1996;245-253.
60. Scaglia L., Cahill C. J., Finegood D. T., Bonner-Weir S. Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinology. 138:1997;1736-1741.
61. Welsh N., Margulis B., Håkan Borg L., Wiklund H. J., Saldeen J., Flodström M., Mello M. A., Andersson A., Pipeleers D. G., Hellerström C., Eizirik D. L. 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. 1:1995;806-820.
62. Bellmann K., Wenz A., Radons J., Burkart V., Kleemann R., Kolb H. Heat shock induces resistance in rat pancreatic islet cells against nitric oxide, oxygen radicals and streptozotocin toxicity in vitro. J. Clin. Invest. 95:1995;2840-2845.
63. Dunger A., Schröder D., Augstein P., Witsruck T., Wachlin G., Vogt L., Ziegler B., Schmidt S. Impact of metabolic activity of beta cells on cytokine-induced damage and recovery of rat pancreatic islets. Acta Diabetol. 32:1995;217-224.
64. Kim Y.-M., De Vera M. E., Watkins S. C., Billiar T. R. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-α-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 272:1997;1402-1411.
65. Yamada K., Takane-Gyotoku N., Yuan X., Ichikawa F., Inada C., Nonaka K. Mouse islet cell lysis mediated by interleukin-1-induced Fas. Diabetologia. 39:1996;1306-1312.
66. Harrison M. J., Dunger A., Berg S., Green I. C. Cytokine activation of Fas in neonatal rat islets of Langerhans. Diabetic Med. 15:1998;S22.
67. Harrison M., Dunger A., Berg S., Mabley J., John N., Green M. H. L., Green I. C. Growth factor protection against cytokine-induced apoptosis in neonatal rat islets of Langerhans: Role of Fas. FEBS Lett. 435:1998;207-210.
68. Suarez-Pinzon W. L., Strynadka K., Rabinovitch A. Destruction of rat pancreatic islet B-cells by cytokines involves the production of cytoxic aldehydes. Endocrinology. 137:1996;5290-5296.
69. Asoh S., Mori T., Hayashi J.-I., Ohta S. Expression of the apoptosis-mediator Fas is enhanced by dysfunctional mitochondria. J. Biochem. 120:1996;600-607.
70. ωL. Diabetes. 44:1995;365-368.
71. GL. Diabetes. 44:1995;360-364.
72. Suarez-Pinzon W. L., Szabó C., Rabinovitch A. Development of autoimmune diabetes in NOD mice is associated with the formation of peroxynitrite in pancreatic islet β-cells. Diabetes. 46:1997;907-911.
73. O'Brien B. A., Harmon B. V., Cameron D. P., Allan D. J. Apoptosis is the mode of β-cell death responsible for the development of IDDM in the nonobese diabetic (NOD) mouse. Diabetes. 46:1997;750-757.
74. O'Brien B. A., Harmon B. V., Cameron D. P., Allan D. J. Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J. Pathol. 178:1996;176-181.