Mitochondria-targeted antioxidants protect pancreatic β-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity

Cellular Physiology and Biochemistry

Volumn 28, Issue 5, 2011, Pages 873-886

  Lim, Sangbin ^a,b   Rashid, Md Abdur ^a,b,d   Jang, Miran ^a   Kim, Yeonghwan ^a   Won, Hyeran ^a   Lee, Jeonghoon ^a   Woo, Jeong Taek ^b   Kim, Young Seol ^b   Murphy, Michael P ^c   Ali, Liaquat ^d   Ha, Joohun ^a   Kim, Sung Soo ^a,b  

^a Kyung Hee University   (South Korea)

^b Kyung Hee University Hospital   (South Korea)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY OF DHAKA   (Bangladesh)

Author keywords

ER stress; Lipid peroxidation; Lipogenesis; Mitochondrial electron transport chain; Mitochondrial reactive oxygen species; Pancreatic cell failure; Type 2 diabetes

Indexed keywords

ABC TRANSPORTER A1; ANTIOXIDANT; CITRATE SYNTHASE; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; INSULIN RELEASE; LIPID STORAGE; LIPOTOXICITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RESPIRATORY CHAIN;

EID: 83755207504     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000335802     Document Type: Article

References (63)

1. Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, Smeitink JA, Willems PH: Mammalian mitochondrial complex I: Biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 2010;12:1431-1470.
2. Murphy MP: How mitochondria produce reactive oxygen species. Biochem J 2009;417:1-13.
3. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M: Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000;404:787-790. (Pubitemid 30212409)
4. Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, Chandel NS: The qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 2007;177:1029-1036. (Pubitemid 46955707)
5. Zelko IN, Mariani TJ, Folz RJ: Superoxide dismutase multigene family: A comparison of the CuZn-SOD (SOD1), Mn-Sod (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 2002;33:337-349. (Pubitemid 34790245)
6. Sivitz WI, Yorek MA: Mitochondrial dysfunction in diabetes: From molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal 2010;12:537-577.
7. Green K, Brand MD, Murphy MP: Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 2004;53:S110-118. (Pubitemid 38168702)
8. Evans JL, Goldfine ID, Maddux BA, Grodsky GM: Oxidative stress and stressactivated signaling pathways: A unifying hypothesis of type 2 diabetes. Endocr Rev 2002;23:599-622. (Pubitemid 35191625)
9. Nishikawa T, Araki E: Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 2007;9:343-353. (Pubitemid 46150966)
10. Korshunov SS, Skulachev VP, Starkov AA: High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997;416:15-18. (Pubitemid 27470791)
11. Brownlee M: The pathobiology of diabetic complications: A unifying mechanism. Diabetes 2005;54:1615-1625. (Pubitemid 40770750)
12. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R: Metabolic syndrome-a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 2005;111:1448-1454. (Pubitemid 40396812)
13. Poitout V, Robertson RP: Glucolipotoxicity: Fuel excess and beta-cell dysfunction. Endocrine Reviews 2008;29:351-366. (Pubitemid 351679704)
14. Trnka J, Blaikie FH, Smith RAJ, Murphy MP: A mitochondria-targeted nitroxide is reduced to its hydroxylamine by ubiquinol in mitochondria. Free Radical Bio Med 2008;44:1406-1419.
15. James AM, Sharpley MS, Manas ARB, Frerman FE, Hirst J, Smith RAJ, Murphy MP: Interaction of the mitochondriatargeted antioxidant MitoQ with phospholipid bilayers and ubiquinone oxidoreductases. J Biol Chem 2007;282:14708-14718. (Pubitemid 47093346)
16. Murphy MP, Smith RAJ: Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol 2007;47:629-656.
17. Smith RAJ, Adlam VJ, Blaikie FH, Manas ARB, Porteous CM, James AM, Ross MF, Logan A, Cocheme HM, Trnka J, Prime TA, Abakumova I, Jones BA, Filipovska A, Murphye MP: Mitochondria-targeted antioxidants in the treatment of disease. Ann Ny Acad Sci 2008;1147:105-111.
18. Chacko BK, Reily C, Srivastava A, Johnson MS, Ye YZ, Ulasova E, Agarwal A, Zinn KR, Murphy MP, Kalyanaraman B, Darley-Usmar V: Prevention of diabetic nephropathy in Ins2(+/)-(AkitaJ) mice by the mitochondria-targeted therapy MitoQ. Biochem J 2010;432:9-19.
19. Graham D, Huynh NN, Hamilton CA, Beattie E, Smith RAJ, Cocheme HM, Murphy MP, Dominiczak AF: Mitochondria-targeted antioxidant MitoQ(10) improves endothelial function and attenuates cardiac hypertrophy. Hypertension 2009;54:322-328.
20. Lu C, Zhang DW, Whiteman M, Armstrong JS: Is antioxidant potential of the mitochondrial targeted ubiquinone derivative MitoQ conserved in cells lacking mtDNA Antioxid Redox Sign 2008;10:651-660.
21. Szeto HH: Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J 2006;8:E277-E283.
22. Oprescu AI, Bikopoulos G, Naassan A, Allister EM, Tang C, Park E, Uchino H, Lewis GF, Fantus IG, Rozakis-Adcock M, Wheeler MB, Giacca A: Free fatty acidinduced reduction in glucose-stimulated insulin secretion. Diabetes 2007;56:2927-2937.
23. Ebenezer PJ, Mariappan N, Elks CM, Haque M, Francis J: Diet-induced renal changes in zucker rats are ameliorated by the superoxide dismutase mimetic tempol. Obesity 2009;17:1994-2002.
24. Wilcox CS: Effects of tempol and redoxcycling nitroxides in models of oxidative stress. Pharmacol Ther 2010;126:119-145.
25. Trnka J, Blaikie FH, Smith RA, Murphy MP: A mitochondria-targeted nitroxide is reduced to its hydroxylamine by ubiquinol in mitochondria. Free Radic Biol Med 2008;44:1406-1419.
26. Trnka J, Blaikie FH, Logan A, Smith RA, Murphy MP: Antioxidant properties of mitotempol and its hydroxylamine. Free Radic Res 2009;43:4-12.
27. Choe SS, Choi AH, Lee JW, Kim KH, Chung JJ, Park J, Lee KM, Park KG, Lee IK, Kim JB: Chronic activation of liver X receptor induces beta-cell apoptosis through hyperactivation of lipogenesis: Liver X receptor-mediated lipotoxicity in pancreatic beta-cells. Diabetes 2007;56:1534-1543. (Pubitemid 46842606)
28. Wang H, Maechler P, Antinozzi PA, Herrero L, Hagenfeldt-Johansson KA, Bjorklund A, Wollheim CB: The transcription factor SREBP-1c is instrumental in the development of beta-cell dysfunction. J Biol Chem 2003;278:16622-16629. (Pubitemid 36799525)
29. Rashid MA, Lee S, Tak E, Lee J, Choi TG, Lee JW, Kim JB, Youn JH, Kang I, Ha J, Kim SS: Carbonyl reductase 1 protects pancreatic beta-cells against oxidative stress-induced apoptosis in glucotoxicity and glucolipotoxicity. Free Radical Bio Med 2010;49:1522-1533.
30. 2+ homeostasis after ER stress. J Cell Sci 2008;121:3636-3648.
31. Jones CI, Han Z, Presley T, Varadharaj S, Zweier JL, Ilangovan G, Alevriadou BR: Endothelial cell respiration is affected by the oxygen tension during shear exposure: Role of mitochondrial peroxynitrite. Am J Physiol Cell Physiol 2008;295:C180-191. (Pubitemid 352755805)
32. Lee J, Choi KJ, Lim MJ, Hong F, Choi TG, Tak E, Lee S, Kim YJ, Chang SG, Cho JM, Ha J, Kim SS: Proto-oncogenic H-ras, K-ras, and N-ras are involved in muscle differentiation via phosphatidylinositol 3-kinase. Cell Res 2010;20:919-934.
33. Singh NP: Microgels for estimation of DNA strand breaks, DNA protein crosslinks and apoptosis. Mutat Res 2000;455:111-127.
34. Del Guerra S, Lupi R, Marselli L, Masini M, Bugliani M, Sbrana S, Torri S, Pollera M, Boggi U, Mosca F, Del Prato S, Marchetti P: Functional and molecular defects of pancreatic islets in human type 2 diabetes. Diabetes 2005;54:727-735. (Pubitemid 40322075)
35. Liang G, Yang J, Horton JD, Hammer RE, Goldstein JL, Brown MS: Diminished hepatic response to fasting/refeeding and liver X receptor agonists in mice with selective deficiency of sterol regulatory element-binding protein-1c. J Biol Chem 2002;277:9520-9528. (Pubitemid 34953041)
36. Robertson RP: Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J Biol Chem 2004;279:42351-42354.
37. Doughan AK, Dikalov SI: Mitochondrial redox cycling of mitoquinone leads to superoxide production and cellular apoptosis. Antioxid Redox Signal 2007;9:1825-1836. (Pubitemid 47622346)
38. Schafer M, Schafer C, Ewald N, Piper HM, Noll T: Role of redox signaling in the autonomous proliferative response of endothelial cells to hypoxia. Circ Res 2003;92:1010-1015. (Pubitemid 36588500)
39. Kalivendi SV, Konorev EA, Cunningham S, Vanamala SK, Kaji EH, Joseph J, Kalyanaraman B: Doxorubicin activates nuclear factor of activated t-lymphocytes and fas ligand transcription: Role of mitochondrial reactive oxygen species and calcium. Biochem J 2005;389:527-539. (Pubitemid 41021156)
40. Ogihara T, Chuang JC, Vestermark GL, Garmey JC, Ketchum RJ, Huang X, Brayman KL, Thorner MO, Repa JJ, Mirmira RG, Evans-Molina C: Liver X receptor agonists augment human islet function through activation of anaplerotic pathways and glycerolipid/free fatty acid cycling. J Biol Chem 2010;285:5392-5404.
41. Oppermann U: Carbonyl reductases: The complex relationships of mammalian carbonyl-and quinone-reducing enzymes and their role in physiology. Annu Rev Pharmacol Toxicol 2007;47:293-322.
42. Cabreiro F, Picot CR, Perichon M, Castel J, Friguet B, Petropoulos I: Overexpression of mitochondrial methionine sulfoxide reductase B2 protects leukemia cells from oxidative stress-induced cell death and protein damage. J Biol Chem 2008;283:16673-16681.
43. Yao K, Ye P, Zhang L, Tan J, Tang X, Zhang Y: Epigallocatechin gallate protects against oxidative stress-induced mitochondria-dependent apoptosis in human lens epithelial cells. Mol Vis 2008;14:217-223. (Pubitemid 351223392)
44. Kohnke R, Mei J, Park M, York DA, Erlanson-Albertsson C: Fatty acids and glucose in high concentration downregulates ATP synthase beta-subunit protein expression in INS-1 cells. Nutr Neurosci 2007;10:273-278.
45. Tiedge M, Hohne M, Lenzen S: Insulin secretion, insulin content and glucose phosphorylation in RINm5F insulinoma cells after transfection with human GLUT2 glucose-transporter cDNA. Biochem J 1993;296:113-118. (Pubitemid 23344737)
46. Diem P, Walseth TF, Zhang HJ, Robertson RP: Secretion and degradation of glucagon by hit cells. Endocrinology 1990;127:1609-1612. (Pubitemid 20315216)
47. 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. (Pubitemid 26077870)
48. Tiedge M, Lortz S, Drinkgern J, Lenzen S: Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997;46:1733-1742. (Pubitemid 27456404)
49. Chen JJ, Yu BP: Alterations in mitochondrial membrane fluidity by lipid peroxidation products. Free Radic Biol Med 1994;17:411-418. (Pubitemid 24320290)
50. Miwa I, Ichimura N, Sugiura M, Hamada Y, Taniguchi S: Inhibition of glucoseinduced insulin secretion by 4-hydroxy-2-nonenal and other lipid peroxidation products. Endocrinology 2000;141:2767-2772. (Pubitemid 32250437)
51. Esterbauer H, Schaur RJ, Zollner H: Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991;11:81-128. (Pubitemid 121003917)
52. Sekiya M, Hiraishi A, Touyama M, Sakamoto K: Oxidative stress induced lipid accumulation via SREBP1c activation in HepG2 cells. Biochem Biophys Res Commun 2008;375:602-607.
53. Furuta E, Pai SK, Zhan R, Bandyopadhyay S, Watabe M, Mo YY, Hirota S, Hosobe S, Tsukada T, Miura K, Kamada S, Saito K, Iiizumi M, Liu W, Ericsson J, Watabe K: Fatty acid synthase gene is up-regulated by hypoxia via activation of akt and sterol regulatory element binding protein-1. Cancer Res 2008;68:1003-1011. (Pubitemid 351278386)
54. Lee H, Lee YJ, Choi H, Ko EH, Kim JW: Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion. J Biol Chem 2009;284:10601-10609.
55. Schroder K, Wandzioch K, Helmcke I, Brandes RP: Nox4 acts as a switch between differentiation and proliferation in preadipocytes. Arterioscler Thromb Vasc Biol 2009;29:239-245.
56. 2+ depletion and cell death in leukemia cells. Mol Pharmacol 2006;70:1424-1434. (Pubitemid 44435995)
57. Guan L, Han B, Li Z, Hua F, Huang F, Wei W, Yang Y, Xu C: Sodium selenite induces apoptosis by ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction in human acute promyelocytic leukemia NB4 cells. Apoptosis 2009;14:218-225.
58. Evans JL, Goldfine ID, Maddux BA, Grodsky GM: Are oxidative stressactivated signaling pathways mediators of insulin resistance and beta-cell dysfunction Diabetes 2003;52:1-8. (Pubitemid 36042100)
59. Sakai K, Matsumoto K, Nishikawa T, Suefuji M, Nakamaru K, Hirashima Y, Kawashima J, Shirotani T, Ichinose K, Brownlee M, Araki E: Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic beta-cells. Biochem Biophys Res Commun 2003;300:216-222. (Pubitemid 36042955)
60. Harding HP, Ron D: Endoplasmic reticulum stress and the development of diabetes: A review. Diabetes 2002;51:S455-S461. (Pubitemid 35403430)
61. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E, Mori M: Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci U S A 2001;98:10845-10850. (Pubitemid 32878707)
62. Gane EJ, Weilert F, Orr DW, Keogh GF, Gibson M, Lockhart MM, Frampton CM, Taylor KM, Smith RA, Murphy MP: The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients. Liver Int 2010;30:1019-1026.
63. Smith RA, Murphy MP: Animal and human studies with the mitochondriatargeted antioxidant MitoQ. Ann N Y Acad Sci 2010;1201:96-103.