Effects of antioxidants coenzyme Q10 and lipoic acid on interleukin-1β-mediated inhibition of glucose-stimulated insulin release from cultured mouse pancreatic islets

Immunopharmacology and Immunotoxicology

Volumn 27, Issue 1, 2005, Pages 109-122

  Schroeder, Michelle M ^a   Belloto Jr , Robert J ^a   Hudson, Richard A ^a   McInerney, Marcia F ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Antioxidant; Coenzyme Q; Diabetes; Insulin release; Islets; Lipoic acid

Indexed keywords

DNA; FREE RADICAL; GLUCOSE; INSULIN; INTERLEUKIN 1BETA; LIPID; NITROGEN RADICAL; OXYGEN RADICAL; PROTEIN; THIOCTIC ACID; UBIDECARENONE; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; DNA DAMAGE; FEMALE; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET; PRIORITY JOURNAL;

EID: 15244343075     PISSN: 08923973     EISSN: 15322513     Source Type: Journal    
DOI: 10.1081/IPH-51755     Document Type: Article

References (48)

1. Rabinovitch, A.; Suarez, W.L.; Power, R.F. Lazaroid antioxidant reduces incidence of diabetes and insulitis in nonobese diabetic mice. J. Lab. Clin. Med. 1993, 121, 603-607.
2. Kikutani, H.; Makino, S. The murine autoimmune diabetes model: NOD and related strains. Adv. Immunol. 1992, 51, 285-322.
3. Kolb, H.; Kantwerk, G.; Treichel, U.; Kurner, T.; Kiesel, U.; Hoppe, T.; Kolb-Bachofen, V. Prospective analysis of islet lesions in BB rats. Diabetologia 1986, 29 (Suppl. 1), A559.
4. Lee, K.U.; Kim, M.K.; Amano, K.; Pak, C.Y.; Jaworski, M.A.; Mehta, J.G.; Yoon, J.W. Preferential infiltration of macrophages during early stages of insulitis in diabetes-prone BB rats. Diabetes 1989, 37, 1053-1058.
5. Voorbij, H.A.M.; Jeucken, P.H.M.; Kabel, P.J.; DeHaan, M.; Drexhage, H.A. Dentritic cells and scavenger macrophages in pancreatic islets of prediabetic BB rats. Diabetes 1989, 38, 1623-1629.
6. Walker, R.; Bone, A.J.; Cooke, A.; Baird, J.D. Distinct macrophage subpopulations in pancreas of prediabetic BB/E rats: a possible role for macrophages in the pathogenesis of IDDM. Diabetes 1988, 37, 1301-1304.
7. Jansen, A.; Homo-Delarche, R.; Hooijkaas, H.; Leenen, P.J.; Dardenne, M.; Drexhage, H.A. Immunohistochemical characterization of monocyte-macrophage and dendritic cells in the initiation of insulitis and beta cell destruction in NOD mice. Diabetes 1994, 43, 667-675.
8. Amano, K.; Yoon, J.W. Studies on autoimmunity for the initiation of beta cell destruction. V. Decrease of macrophage dependent T-effector cells and natural killer cytotoxicity in silica-treated BB rats. Diabetes 1990, 39, 590-596.
9. Lee, K.U.; Amano, K.; Yoon, J.W. Evidence for initial involvement of macrophage in development of insulitis in NOD mice. Diabetes 1988, 37, 989-991.
10. Oschilewski, U.; Kiesel, U.; Kolb, H. Administration of silica prevents diabetes in BB rats. Diabetes 1985, 34, 197-199.
11. Lee, K.U.; Pak, C.Y.; Amano, K.; Yoon, J.W. Prevention of lymphocytic thyroditis and insulitis in diabetes prone BB rats by the depletion of macrophages. Diabetologia 1988, 31, 400-402.
12. Jun, H.-S.; Yoon, C.-S.; Zbytnuik, L.; van Rooijen, N.; Yoon, J.-W. The role of macrophages in T-cell mediated autoimmune diabetes in nonobese diabetic mice. J. Exp. Med. 1999, 189, 347-358.
13. Rabinovitch, A.; Suarez-Pinzon, W. Cytokines and their roles in pancreatic islet β cell destruction and insulin-dependent diabetes mellitus. Biochem. Pharmacol. 1998, 55, 1139-1149.
14. Zumsteg, U.; Reimers, J.I.; Pociot, F.; Morch, L.; Helqvist, M.; Brendel, M.; Alejandro, R.; Mandrup-Poulsen, T.; Dinarello, CA.; Nerup, J. Differential interleukin-1 receptor antagonism on pancreatic beta and alpha cells. Studies in rodent and human islets and in normal rats. Diabetelogia 1993, 36, 759-766.
15. Corbett, J.A.; McDaniel, M.L. Intraislet release of interleukin 1 inhibits β cell function by inducing β cell expression of inducible nitric oxide synthase. J. Exp. Med. 1995, 181, 559-568.
16. Welsh, N.; Eizirik, D.L.; Bendtzen, K.; Sandler, S. Interleukin-1β- induced nitric oxide production in isolated rat pancreatic islets requires gene transcription and may lead to inhibition of the krebs cycle enzyme aconitase. Endocrinology 1991, 129, 3167-3173.
17. Corbett, J.A.; Wang, J.L.; Sweetland, M.A.; Lancaster, J.R.; McDaniel, M.L. Interleukin 1-beta induces the formation of nitric oxide by beta-cells purified from rodent islets of Langerhans. Evidence for the beta-cell as a source and site of action of nitric oxide. J. Clin. Invest. 1992, 90 (6), 2384-2391.
18. Corbett, J.A.; McDaniel, M.L. Reversibility of interleukin-1 beta-induced islet dysfunction by the inhibition of nitric oxide synthetase. Biochem. J. 1994, 299 (part 3), 719-724.
19. Corbett, J.A.; Lancaster, J.R., Jr.; Sweetland, M.A.; McDaniel, M.L. Interleukin-1β-induced formation of EPR-detectable iron-nitrosyl complexes in islets of Langerhans-role of nitric oxide in interleukin-1β-induced inhibition of insulin secretion. J. Biol. Chem. 1991, 266, 21351-21354.
20. Corbett, J.A.; Mikhael, A.; Shimizu, J.; Frederick, K.; Misko, T.P.; McDaniel, M.L.; Kanagawa, O.; Unanue, E.R. Nitric oxide production in islets from nonobese diabetic mice: aminoguanidine-sensitive and resistant stages in the immunological diabetic process. Proc. Natl. Acad. Sci. U. S. A. 1893, 90, 8992-8995.
21. Arnush, M.; Scarim, A.L.; Heitmeier, M.R.; Kelly, C.B.; Corbett, J.A. Potential role of resident islet macrophage activation in the initiation of autoimmune diabetes. J. Immunol. 1908, 160 (6), 2684-2691.
22. Arnush, M.; Heitmeier, M.R.; Scarim, A.L.; Marino, M.H.; Manning, P.T.; Corbett, J.A. IL-1 produced and released endogenously within human islets inhibits beta cell function. J.Clin. Invest. 1998, 202, 516-526.
23. Maxwell, S.R. Prospects for the use of antioxidant therapies. Drugs 1995, 49 (3), 345-361.
24. Maxwell, S.R. Antioxidant therapy: does it have a role in the treatment of human disease. Curr. Drugs 1997, 6 (3), 211-236.
25. Maxwell, S.R.; Thomason, H.; Sandler, D.; Leguen, C.; Baxter, MA.; Thorpe, G.H.; Jones, A.F.; Barnett, A.H. Antioxidant status in patients with uncomplicated insulin dependent and non-insulin dependent diabetes mellitus. Eur. J. Clin. Invest. 1997, 27 (6), 484-490.
26. Welsh, N.; Eizirik, D.L.; Bendtzen, K.; Sandler, S. Interleukin-1β- induced nitric oxide production in isolated rat pancreatic islets requires gene transcription and may lead to inhibition of the krebs cycle enzyme aconitase. Endocrinology 1991, 129, 3167-3173.
27. Asayama, K.; Kooy, N.W.; Burr, LM. Effect of vitamin E deficiency and selenium deficiency on insulin secretory reserve and free radical scavenging systems in islets: decrease of islet manganosuperoxide dismutase. J. Lab. Clin. Med. 1986, 107, 459-464.
28. Lenzen, S.; Drinkgern, J.; Tiedge, M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic. Biol. Med. 1996, 20, 463-466.
29. Eizirik, D.L.; Tracey, D.E.; Bendtzen, K.; Sandler, S. An interleukin-1 receptor antagonist protein protects insulin-producing beta cells against suppressive effects of interleukin-1β. Diabetologia 1991, 34, 445-448.
30. Nicoletti, F.; Di Marco, R.; Barcellini, W.; Magro, G.; Schorlemmer, H.U.; Kurrle, R.; Lunetta, M.; Grasso, S.; Zaccone, P.; Meroni, P. Protection from experimental autoimmune diabetes in the non-obese diabetic mouse with soluble interleukin-1 receptor. Eur. J. Immunol. 1994, 24, 1843-1847.
31. Sumoski, W.; Baquerizo, H.; Rabinovitch, A. Oxygen free radical scavengers protect rat islets cells from damage by cytokines. Diabetologia 1989, 32, 792-796.
32. 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 1992, 35, 409-413.
33. Rabinovitch, A.; Suarez-Pinzon, W.L.; Strynadka, K.; Lakey, J.R.T.; Rojette, R.V. Human pancreatic islet beta-cell destruction by cytokines involves oxygen free radical and aldehyde production. J. Clin. Endocrinol. Metab. 1996, 81, 3197-3202.
34. Rabinovitch, A.; Suarez, W.L.; Power, R.F. Lazaroid antioxidant reduces incidence of diabetes and insulitis in nonobese diabetic mice. J. Lab. Clin. Med. 1993, 121, 603-607.
35. Mandrup-Poulsen, T.; Helqvist, S.; Wogensen, L.D.; Mølvig, J.; Pociot, F.; Johannesen, J.; Nerup, J. Cytokines and free radicals as effector molecules in the destruction of pancreatic beta cells. Curr. Topics Microbiol. Immunol. 1990, 164, 169-193.
36. McInerney, M.F.; Flynn, J.C.; Goldblatt, P.; Najjar, S.M.; Sherwin, R.S.; Janeway, C.A., Jr. High density insulin receptor-positive lymphocytes from nonobese diabetic mice transfer insulitis and diabetes. J. Immunol. 1996, 157, 3716-3726.
37. Prowse, S.J.; Simeonovic, C.J.; Lafferty, K.J.; Bond, B.C.; Magi, C.E.; Mackie, D. Allogenic islet transplantation without recipient immunosuppression. In Methods in Diabetes Research, Vol. I: Laboratory Methods, Part B; Larner, J., Pohl, S.L., Eds.; John Wiley & Sons: New York, 1984; 253-269.
38. Andersson, A. Isolated mouse pancreatic islets in culture: effects of serum and different culture media on the insulin production of the islets. Diabetologia 1978, 14, 397-404.
39. McInerney, M.F.; Seidel, M.J.; Nguyen, J.M.D.; Flynn, J.C.; Sturm, N.; Lee, H.; Zhang, Z.; Tillekeratne, L.M.V.; Hudson, R.A. Effects of a 33 residue interleukin-1β peptide and the antioxidant PQQ on interleukin-1β- mediated inhibition of glucose stimulated insulin release from culture mouse pancreatic islets. Res. Cornm. Mol. Path. Pharmacol. 1996, 94 (2), 115-128.
40. Knocke, H.W. Radioisotopic Methods for Biological and Medical Research; Oxford University Press: New York, 1991; 402.
41. Hollander, M.; Wolfe, D.A. Nonparametric Statistical Methods; John Wiley & Sons: New York, 1999; 189-202. (Kruskal-Wallis); 240-249 (two-sided, all treatments, multiple comparisons).
42. Ramiya, V.K.; Maraist, M.; Arfors, K.E.; Schatz, D.A.; Peck, A.B.; Cornelius, J.G. Reversal of insulin-dependent diabetes using islets generated in vitro from pancreatic stem cells. Nat. Med. 2000, 6 (3), 278-282.
43. Mandrup-Poulsen, T.; Reimers, J.I.; Andersen, H.U.; Pociot, F.; Karlsen, A.E.; Bjerre, U.; a Nerup, J. Nicotinamide treatment in the prevention of insulin-dependent diabetes mellitus. Diabetes Metab. Rev. 1993, 9, 295-309.
44. Packer, L.; Tritschler, H.J.; Wessel, K. Neuroprotection by the metabolic antioxidant alpha-lipoic acid. Free Radic. Biol. Med. 1887, 22 (1-2), 359-378.
45. Burkart, V.; Koike, T.; Brenner, H.H.; Imai, Y.; Kolb, H. Dihydrolipoic acid protects pancreatic islet cells from inflammatory attack. Agents Actions 1993, 38, 60-65.
46. Packer, L.; Witt, E.H.; Tritschler, H.J. Alpha-lipoic acid as a biological antioxidant. Free Radic. Biol. Med. 1995, 19 (2), 227-250.
47. Faust, A.; Burkart, V.; Ulrich, H.; Weischer, C.H.; Kolb, H. Effect of lipoic acid on cyclophosphamide-induced diabetes and insulitis in non-obese diabetic mice. Int. J. Immunopharmacol. 1994, 16 (1), 61-66.
48. Suzuki, Y.; Kadowaki, H.; Atsumi, Y.; Hosokawa, K.; Katagiri, H.; Kadowski, T.; Oka, Y.; Uyama, K; Mokubo, A.; Asahina, T.; Murata, C.; Matsuoka, K. A case of diabetic amyotrophy associated with 3243 mitochondrial tRNA (leu; UUR) mutation and successful therapy with coenzyme Q10. Endocrin. J. 1995, 42 (2), 141-145.