Rosiglitazone protects against palmitate-induced pancreatic beta-cell death by activation of autophagy via 5′-AMP-activated protein kinase modulation

Endocrine

Volumn 44, Issue 1, 2013, Pages 87-98

  Wu, Jie ^a,b   Wu, Jun Jie ^c   Yang, Lin Jun ^a   Wei, Li Xin ^d   Zou, Da Jin ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b TONGJI UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

AMPK; Autophagy; Palmitate; Rosiglitazone

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PALMITIC ACID; ROSIGLITAZONE; S6 KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CELL DEATH; CELLS, CULTURED; CYTOPROTECTION; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; PALMITIC ACID; RATS; RNA, SMALL INTERFERING; THIAZOLIDINEDIONES;

EID: 84881122467     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-012-9826-5     Document Type: Article

References (48)

1. M.Y. Donath, P.A. Halban, Decreased beta-cell mass in diabetes: significance, mechanisms and therapeutic implications. Diabetologia 47(3), 581-589 (2004)
2. I.W. Campbell, S. Mariz, Beta-cell preservation with thiazolidinediones. Diabetes Res. Clin. Pract. 76(2), 163-176 (2007)
3. L.L. Baggio, D.J. Drucker, Therapeutic approaches to preserve islet mass in type 2 diabetes. Annu. Rev. Med. 57, 265-281 (2006)
4. B. Levine, D.J. Klionsky, Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6(4), 463-477 (2004)
5. B. Levine, G. Kroemer, Autophagy in the pathogenesis of disease. Cell 132(1), 27-42 (2008)
6. F. Reggiori, D.J. Klionsky, Autophagy in the eukaryotic cell. Eukaryot. Cell 1(1), 11-21 (2002)
7. D.J. Klionsky, H. Abeliovich, P. Agostinis, D.K. Agrawal, G. Aliev, D.S. Askew, M. Baba, E.H. Baehrecke, B.A. Bahr, A. Ballabio, B.A. Bamber, D.C. Bassham, E. Bergamini, X. Bi, M. Biard-Piechaczyk, J.S. Blum, D.E. Bredesen, J.L. Brodsky, J.H. Brumell, U.T. Brunk, W. Bursch, N. Camougrand, E. Cebollero, F. Cecconi, Y. Chen, L.S. Chin, A. Choi, C.T. Chu, J. Chung, P.G. Clarke, R.S. Clark, S.G. Clarke, C. Clave, J.L. Cleveland, P. Codogno, M.I. Colombo, A. Coto-Montes, J.M. Cregg, A.M. Cuervo, J. Debnath, F. Demarchi, P.B. Dennis, P.A. Dennis, V. Deretic, R.J. Devenish, F. Di Sano, J.F. Dice, M. Difiglia, S. Dinesh-Kumar, C.W. Distelhorst, M. Djavaheri-Mergny, F.C. Dorsey, W. Droge, M. Dron, W.A. Dunn Jr, M. Duszenko, N.T. Eissa, Z. Elazar, A. Esclatine, E.L. Eskelinen, L. Fesus, K.D. Finley, J.M. Fuentes, J. Fueyo, K. Fujisaki, B. Galliot, F.B. Gao, D.A. Gewirtz, S.B. Gibson, A. Gohla, A.L. Goldberg, R. Gonzalez, C. Gonzalez-Estevez, S. Gorski, R.A. Gottlieb, D. Haussinger, Y.W. He, K. Heidenreich, J.A. Hill, M. Hoyer-Hansen, X. Hu, W.P. Huang, A. Iwasaki, M. Jaattela, W.T. Jackson, X. Jiang, S. Jin, T. Johansen, J.U. Jung, M. Kadowaki, C. Kang, A. Kelekar, D.H. Kessel, J.A. Kiel, H.P. Kim, A. Kimchi, T.J. Kinsella, K. Kiselyov, K. Kitamoto, E. Knecht, M. Komatsu, E. Kominami, S. Kondo, A.L. Kovacs, G. Kroemer, C.Y. Kuan, R. Kumar, M. Kundu, J. Landry, M. Laporte, W. Le, H.Y. Lei, M.J. Lenardo, B. Levine, A. Lieberman, K.L. Lim, F.C. Lin, W. Liou, L.F. Liu, G. Lopez-Berestein, C. Lopez-Otin, B. Lu, K.F. Macleod, W. Malorni, W. Martinet, K. Matsuoka, J. Mautner, A.J. Meijer, A. Melendez, P. Michels, G. Miotto, W.P. Mistiaen, N. Mizushima, B. Mograbi, I. Monastyrska, M.N. Moore, P.I. Moreira, Y. Moriyasu, T. Motyl, C. Munz, L.O. Murphy, N.I. Naqvi, T.P. Neufeld, I. Nishino, R.A. Nixon, T. Noda, B. Nurnberg, M. Ogawa, N.L. Oleinick, L.J. Olsen, B. Ozpolat, S. Paglin, G.E. Palmer, I. Papassideri, M. Parkes, D.H. Perlmutter, G. Perry, M. Piacentini, R. Pinkas-Kramarski, M. Prescott, T. Proikas-Cezanne, N. Raben, A. Rami, F. Reggiori, B. Rohrer, D.C. Rubinsztein, K.M. Ryan, J. Sadoshima, H. Sakagami, Y. Sakai, M. Sandri, C. Sasakawa, M. Sass, C. Schneider, P.O. Seglen, O. Seleverstov, J. Settleman, J.J. Shacka, I.M. Shapiro, A. Sibirny, E.C. Silva-Zacarin, H.U. Simon, C. Simone, A. Simonsen, M.A. Smith, K. Spanel-Borowski, V. Srinivas, M. Steeves, H. Stenmark, P.E. Stromhaug, C.S. Subauste, S. Sugimoto, D. Sulzer, T. Suzuki, M.S. Swanson, I. Tabas, F. Takeshita, N.J. Talbot, Z. Talloczy, K. Tanaka, I. Tanida, G.S. Taylor, J.P. Taylor, A. Terman, G. Tettamanti, C.B. Thompson, M. Thumm, A.M. Tolkovsky, S.A. Tooze, R. Truant, L.V. Tumanovska, Y. Uchiyama, T. Ueno, N.L. Uzcategui, I. van der Klei, E.C. Vaquero, T. Vellai, M.W. Vogel, H.G. Wang, P. Webster, J.W. Wiley, Z. Xi, G. Xiao, J. Yahalom, J.M. Yang, G. Yap, X.M. Yin, T. Yoshimori, L. Yu, Z. Yue, M. Yuzaki, O. Zabirnyk, X. Zheng, X. Zhu, R.L. Deter, Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4(2), 151-175 (2008)
8. S.W. Yu, S.H. Baek, R.T. Brennan, C.J. Bradley, S.K. Park, Y.S. Lee, E.J. Jun, K.J. Lookingland, E.K. Kim, H. Lee, J.L. Goudreau, S.W. Kim, Autophagic death of adult hippocampal neural stem cells following insulin withdrawal. Stem Cells 26(10), 2602-2610 (2008)
9. K. Sato, K. Tsuchihara, S. Fujii, M. Sugiyama, T. Goya, Y. Atomi, T. Ueno, A. Ochiai, H. Esumi, Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 67(20), 9677-9684 (2007)
10. P. Codogno, A.J. Meijer, Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 12(Suppl 2), 1509-1518 (2005)
11. E. Corcelle, N. Djerbi, M. Mari, M. Nebout, C. Fiorini, P. Fenichel, P. Hofman, P. Poujeol, B. Mograbi, Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 3(1), 57-59 (2007)
12. K.Y. Hur, H.S. Jung, M.S. Lee, Role of autophagy in beta-cell function and mass. Diabetes Obes. Metab. 12(Suppl 2), 20-26 (2010)
13. G. Las, O.S. Shirihai, The role of autophagy in beta-cell lipotoxicity and type 2 diabetes. Diabetes Obes. Metab. 12(Suppl 2), 15-19 (2010)
14. J. Zhou, W. Zhang, B. Liang, M.C. Casimiro, D. Whitaker-Menezes, M. Wang, M.P. Lisanti, S. Lanza-Jacoby, R.G. Pestell, C. Wang, PPARgamma activation induces autophagy in breast cancer cells. Int. J. Biochem. Cell Biol. 41(11), 2334-2342 (2009)
15. J. Yan, H. Yang, G. Wang, L. Sun, Y. Zhou, Y. Guo, Z. Xi, X. Jiang, Autophagy augmented by troglitazone is independent of EGFR transactivation and correlated with AMP-activated protein kinase signaling. Autophagy 6(1), 67-73 (2010)
16. E. Karaskov, C. Scott, L. Zhang, T. Teodoro, M. Ravazzola, A. Volchuk, Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147(7), 3398-3407 (2006)
17. W. El-Assaad, J. Buteau, M.L. Peyot, C. Nolan, R. Roduit, S. Hardy, E. Joly, G. Dbaibo, L. Rosenberg, M. Prentki, Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death. Endocrinology 144(9), 4154-4163 (2003)
18. C. Bauvy, P. Gane, S. Arico, P. Codogno, E. Ogier-Denis, Autophagy delays sulindac sulfide-induced apoptosis in the human intestinal colon cancer cell line HT-29. Exp. Cell Res. 268(2), 139-149 (2001)
19. K. Komiya, T. Uchida, T. Ueno, M. Koike, H. Abe, T. Hirose, R. Kawamori, Y. Uchiyama, E. Kominami, Y. Fujitani, H. Watada, Free fatty acids stimulate autophagy in pancreatic beta-cells via JNK pathway. Biochem. Biophys. Res. Commun. 401(4), 561-567 (2010)
20. R.K. Amaravadi, D. Yu, J.J. Lum, T. Bui, M.A. Christophorou, G.I. Evan, A. Thomas-Tikhonenko, C.B. Thompson, Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117(2), 326-336 (2007)
21. V.R. Solomon, H. Lee, Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies. Eur. J. Pharmacol. 625(1-3), 220-233 (2009)
22. B. Ravikumar, C. Vacher, Z. Berger, J.E. Davies, S. Luo, L.G. Oroz, F. Scaravilli, D.F. Easton, R. Duden, C.J. O'Kane, D.C. Rubinsztein, Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36(6), 585-595 (2004)
23. Z. Feng, H. Zhang, A.J. Levine, S. Jin, The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 102(23), 8204-8209 (2005)
24. D.T. Finegood, M.D. McArthur, D. Kojwang, M.J. Thomas, B.G. Topp, T. Leonard, R.E. Buckingham, Beta-cell mass dynamics in Zucker diabetic fatty rats. Rosiglitazone prevents the rise in net cell death. Diabetes 50(5), 1021-1029 (2001)
25. J.W. Kim, J.H. Yang, H.S. Park, C. Sun, S.H. Lee, J.H. Cho, C.W. Yang, K.H. Yoon, Rosiglitazone protects the pancreatic beta-cell death induced by cyclosporine A. Biochem. Biophys. Res. Commun. 390(3), 763-768 (2009)
26. B.H. Chung, C. Li, B.K. Sun, S.W. Lim, K.O. Ahn, J.H. Yang, Y.H. Choi, K.H. Yoon, A. Sugawara, S. Ito, J. Kim, C.W. Yang, Rosiglitazone protects against cyclosporine-induced pancreatic and renal injury in rats. Am. J. Transplant. 5(8), 1856-1867 (2005)
27. C.Y. Lin, T. Gurlo, L. Haataja, W.A. Hsueh, P.C. Butler, Activation of peroxisome proliferator-activated receptor-gamma by rosiglitazone protects human islet cells against human islet amyloid polypeptide toxicity by a phosphatidylinositol 3′-kinase-dependent pathway. J. Clin. Endocrinol. Metab. 90(12), 6678-6686 (2005)
28. C. Ebato, T. Uchida, M. Arakawa, M. Komatsu, T. Ueno, K. Komiya, K. Azuma, T. Hirose, K. Tanaka, E. Kominami, R. Kawamori, Y. Fujitani, H. Watada, Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab. 8(4), 325-332 (2008)
29. S.E. Choi, S.M. Lee, Y.J. Lee, L.J. Li, S.J. Lee, J.H. Lee, Y. Kim, H.S. Jun, K.W. Lee, Y. Kang, Protective role of autophagy in palmitate-induced INS-1 beta-cell death. Endocrinology 150(1), 126-134 (2009)
30. R. Scherz-Shouval, Z. Elazar, Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 36(1), 30-38 (2011)
31. W.X. Ding, H.M. Ni, W. Gao, T. Yoshimori, D.B. Stolz, D. Ron, X.M. Yin, Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 171(2), 513-524 (2007)
32. M. Cnop, M. Igoillo-Esteve, D.A. Cunha, L. Ladriere, D.L. Eizirik, An update on lipotoxic endoplasmic reticulum stress in pancreatic beta-cells. Biochem. Soc. Trans. 36(Pt 5), 909-915 (2008)
33. A.J. Molina, J.D. Wikstrom, L. Stiles, G. Las, H. Mohamed, A. Elorza, G. Walzer, G. Twig, S. Katz, B.E. Corkey, O.S. Shirihai, Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 58(10), 2303-2315 (2009)
34. P. Schrauwen, M.K. Hesselink, Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53(6), 1412-1417 (2004)
35. K. Morino, K.F. Petersen, G.I. Shulman, Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55(Suppl 2), S9-S15 (2006)
36. M. Qatanani, M.A. Lazar, Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev. 21(12), 1443-1455 (2007)
37. M. Masini, M. Bugliani, R. Lupi, S. del Guerra, U. Boggi, F. Filipponi, L. Marselli, P. Masiello, P. Marchetti, Autophagy in human type 2 diabetes pancreatic beta cells. Diabetologia 52(6), 1083-1086 (2009)
38. H.Y. Xiong, X.L. Guo, X.X. Bu, S.S. Zhang, N.N. Ma, J.R. Song, F. Hu, S.F. Tao, K. Sun, R. Li, M.C. Wu, L.X. Wei, Autophagic cell death induced by 5-FU in Bax or PUMA deficient human colon cancer cell. Cancer Lett. 288(1), 68-74 (2010)
39. L. Yu, A. Alva, H. Su, P. Dutt, E. Freundt, S. Welsh, E.H. Baehrecke, M.J. Lenardo, Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304(5676), 1500-1502 (2004)
40. G. Kroemer, B. Levine, Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 9(12), 1004-1010 (2008)
41. C.H. Jung, S.H. Ro, J. Cao, N.M. Otto, D.H. Kim, mTOR regulation of autophagy. FEBS Lett. 584(7), 1287-1295 (2010)
42. D. Han, B. Yang, L.K. Olson, A. Greenstein, S.H. Baek, K.J. Claycombe, J.L. Goudreau, S.W. Yu, E.K. Kim, Activation of autophagy through modulation of 5′-AMP-activated protein kinase protects pancreatic beta-cells from high glucose. Biochem J 425(3), 541-551 (2010)
43. M. Stumvoll, Thiazolidinediones - some recent developments. Expert Opin. Investig. Drugs 12(7), 1179-1187 (2003)
44. M. Jiang, S. Fernandez, W.G. Jerome, Y. He, X. Yu, H. Cai, B. Boone, Y. Yi, M.A. Magnuson, P. Roy-Burman, R.J. Matusik, S.B. Shappell, S.W. Hayward, Disruption of PPARgamma signaling results in mouse prostatic intraepithelial neoplasia involving active autophagy. Cell Death Differ. 17(3), 469-481 (2010)
45. D.F. Mahmood, I. Jguirim-Souissi, H. el Khadija, N. Blondeau, V. Diderot, S. Amrani, M.N. Slimane, T. Syrovets, T. Simmet, M. Rouis, Peroxisome proliferator-activated receptor gamma induces apoptosis and inhibits autophagy of human monocyte-derived macrophages via induction of cathepsin L: potential role in atherosclerosis. J. Biol. Chem. 286(33), 28858-28866 (2011)
46. L. Cerquetti, C. Sampaoli, D. Amendola, B. Bucci, L. Masuelli, R. Marchese, S. Misiti, A. De Venanzi, M. Poggi, V. Toscano, A. Stigliano, Rosiglitazone induces autophagy in H295R and cell cycle deregulation in SW13 adrenocortical cancer cells. Exp. Cell Res. 317(10), 1397-1410 (2011)
47. L.G. Fryer, A. Parbu-Patel, D. Carling, The Anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J. Biol. Chem. 277(28), 25226-25232 (2002)
48. D.H. van Raalte, M. Diamant, Glucolipotoxicity and beta cells in type 2 diabetes mellitus: target for durable therapy? Diabetes Res. Clin. Pract. 93(Suppl 1), S37-005346 (2011)