Induction of autophagy by palmitic acid via protein kinase C-mediated signaling pathway independent of mTOR (mammalian target of rapamycin)

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14364-14376

  Tan, Shi Hao ^a,c   Shui, Guanghou ^b   Zhou, Jing ^a   Li, Jasmine Jia'En ^b   Bay, Boon Huat ^b   Wenk, Markus R ^a,b,c   Shen, Han Ming ^a,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; CONTRIBUTING FACTOR; CYTOTOXIC EFFECTS; DIACYLGLYCEROL; FAT ACCUMULATION; ISOFORMS; MAMMALIAN TARGET; METABOLIC DISEASE; NON-ALCOHOLIC FATTY LIVER; PROTEIN KINASE; PROTEIN KINASE C; SIGNALING PATHWAYS; THERAPEUTIC STRATEGY;

CELLS; CYTOLOGY; CYTOTOXICITY; ENZYMES; GLYCEROL; OLEIC ACID; PALMITIC ACID; SATURATED FATTY ACIDS; UNSATURATED FATTY ACIDS;

ANTIBIOTICS;

DIACYLGLYCEROL; MAMMALIAN TARGET OF RAPAMYCIN; OLEIC ACID; PALMITIC ACID; PROTEIN KINASE C; PROTEIN KINASE C ALPHA;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME INHIBITORS; HEP G2 CELLS; HUMANS; MICE; PALMITIC ACID; PROTEIN KINASE C-ALPHA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

MAMMALIA;

EID: 84860372433     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.294157     Document Type: Article

References (50)

1. Klionsky, D. J., and Emr, S. D. (2000) Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721 (Pubitemid 32004796)
2. Mizushima, N. (2007) Autophagy. Process and function. Genes Dev. 21, 2861-2873
3. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (Pubitemid 351317450)
4. He, C., and Klionsky, D. J. (2009) Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93
5. Jung, C. H., Jun, C. B., Ro, S. H., Kim, Y. M., Otto, N. M., Cao, J., Kundu, M., and Kim, D. H. (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20, 1992-2003
6. Mizushima, N. (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 22, 132-139
7. Brookheart, R. T., Michel, C. I., and Schaffer, J. E. (2009) As a matter of fat. Cell Metab. 10, 9-12
8. Kim, J. K., Michael, M. D., Previs, S. F., Peroni, O. D., Mauvais-Jarvis, F., Neschen, S., Kahn, B. B., Kahn, C. R., and Shulman, G. I. (2000) Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J. Clin. Invest. 105, 1791-1797 (Pubitemid 30421760)
9. Chiu, H. C., Kovacs, A., Ford, D. A., Hsu, F. F., Garcia, R., Herrero, P., Saffitz, J. E., and Schaffer, J. E. (2001) A novel mouse model of lipotoxic cardiomyopathy. J. Clin. Invest. 107, 813-822 (Pubitemid 32274034)
10. Chavez, J. A., and Summers, S. A. (2010) Lipid oversupply, selective insulin resistance, and lipotoxicity molecular mechanisms. Biochim. Biophys. Acta 1801, 252-265
11. Schaffer, J. E. (2003) Lipotoxicity. When tissues overeat. Curr. Opin. Lipidol. 14, 281-287
12. Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A. M., and Czaja, M. J. (2009) Autophagy regulates lipid metabolism. Nature 458, 1131-1135
13. Yang, L., Li, P., Fu, S., Calay, E. S., and Hotamisligil, G. S. (2010) Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 11, 467-478
14. Ebato, C., Uchida, T., Arakawa, M., Komatsu, M., Ueno, T., Komiya, K., Azuma, K., Hirose, T., Tanaka, K., Kominami, E., Kawamori, R., Fujitani, Y., and Watada, H. (2008) Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high fat diet. Cell Metab. 8, 325-332
15. Choi, S. E., Lee, S. M., Lee, Y. J., Li, L. J., Lee, S. J., Lee, J. H., Kim, Y., Jun, H. S., Lee, K. W., and Kang, Y. (2009) Protective role of autophagy in palmitate-induced INS-1 beta cell death. Endocrinology 150, 126-134
16. Koga, H., Kaushik, S., and Cuervo, A. M. (2010) Altered lipid content inhibits autophagic vesicular fusion. FASEB J. 24, 3052-3065
17. Listenberger, L. L., and Brown, D. A. (2007) Fluorescent detection of lipid droplets and associated proteins. Curr. Protoc. Cell Biol., Chapter 24, Unit 24.2
18. Hosokawa, N., Hara, Y., and Mizushima, N. (2007) Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett. 581, 2623-2629
19. Wu, Y. T., Tan, H. L., Shui, G., Bauvy, C., Huang, Q., Wenk, M. R., Ong, C. N., Codogno, P., and Shen, H. M. (2010) Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J. Biol. Chem. 285, 10850-10861
20. Wu, Y. T., Tan, H. L., Huang, Q., Kim, Y. S., Pan, N., Ong, W. Y., Liu, Z. G., Ong, C. N., and Shen, H. M. (2008) Autophagy plays a protective role during zVAD-induced necrotic cell death. Autophagy 4, 457-466 (Pubitemid 351705142)
21. Shui, G., Stebbins, J. W., Lam, B. D., Cheong, W. F., Lam, S. M., Gregoire, F., Kusonoki, J., and Wenk, M. R. (2011) Comparative plasma lipidome between human and cynomolgus monkey. Are plasma polar lipids good biomarkers for diabetic monkeys? PLoS One 6, e19731
22. Shui, G., Guan, X. L., Low, C. P., Chua, G. H., Goh, J. S., Yang, H., and Wenk, M. R. (2010) Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry. Application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol. Biosyst. 6, 1008-1017
23. Listenberger, L. L., Han, X., Lewis, S. E., Cases, S., Farese, R. V., Jr., Ory, D. S, and Schaffer, J. E. (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. U.S.A. 100, 3077-3082 (Pubitemid 36356542)
24. Mizushima, N., Yoshimori, T., and Levine, B. (2010) Methods in mammalian autophagy research. Cell 140, 313-326
25. Codogno, P., and Meijer, A. J. (2005) Autophagy and signaling. Their role in cell survival and cell death. Cell Death Differ. 12, 1509-1518 (Pubitemid 41553987)
26. Sarbassov, D. D., Ali, S. M., and Sabatini, D. M. (2005) Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17, 596-603 (Pubitemid 41540408)
27. Holland, W. L., and Summers, S. A. (2008) Sphingolipids, insulin resistance, and metabolic disease. New insights from in vivo manipulation of sphingolipid metabolism. Endocr. Rev. 29, 381-402 (Pubitemid 351831506)
28. Scarlatti, F., Bauvy, C., Ventruti, A., Sala, G., Cluzeaud, F., Vandewalle, A., Ghidoni, R., and Codogno, P. (2004) Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1. J. Biol. Chem. 279, 18384-18391 (Pubitemid 38623254)
29. Pattingre, S., Bauvy, C., Carpentier, S., Levade, T., Levine, B., and Codogno, P. (2009) Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J. Biol. Chem. 284, 2719-2728
30. Coleman, R. A., and Mashek, D. G. (2011) Mammalian triacylglycerol metabolism. Synthesis, lipolysis, and signaling. Chem. Rev. 111, 6359-6386
31. Li, L. O., Klett, E. L., and Coleman, R. A. (2010) Acyl-CoA synthesis, lipid metabolism, and lipotoxicity. Biochim. Biophys. Acta. 1801, 246-251
32. Coleman, R., and Bell, R. M. (1976) Triacylglycerol synthesis in isolated fat cells. Studies on the microsomal diacylglycerol acyltransferase activity using ethanol-dispersed diacylglycerols. J. Biol. Chem. 251, 4537-4543
33. Newton, A. C. (2001) Protein kinase C. Structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev. 101, 2353-2364
34. Schmitz-Peiffer, C., and Biden, T. J. (2008) Protein kinase C function in muscle, liver, and beta cells and its therapeutic implications for type 2 diabetes. Diabetes 57, 1774-1783
35. Sakaki, K., Wu, J., and Kaufman, R. J. (2008) Protein kinase Cθ is required for autophagy in response to stress in the endoplasmic reticulum. J. Biol. Chem. 283, 15370-15380
36. Gschwendt, M., Kittstein, W., and Marks, F. (1991) Protein kinase C activation by phorbol esters. Do cysteine-rich regions and pseudosubstrate motifs play a role? Trends Biochem. Sci. 16, 167-169 (Pubitemid 121004427)
37. Listenberger, L. L., Ory, D. S., and Schaffer, J. E. (2001) Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J. Biol. Chem. 276, 14890-14895
38. Levine, B., and Klionsky, D. J. (2004) Development by self-digestion. Molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463-477 (Pubitemid 38456176)
39. Mei, S., Ni, H. M., Manley, S., Bockus, A., Kassel, K. M., Luyendyk, J. P., Copple, B. L., and Ding, W. X. (2011) Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J. Pharmacol. Exp. Ther. 339, 487-498
40. Muoio, D. M., and Newgard, C. B. (2008) Mechanisms of disease. Molecular and metabolic mechanisms of insulin resistance and beta cell failure in type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 193-205 (Pubitemid 351301824)
41. Wang, X., Yu, W., Nawaz, A., Guan, F., Sun, S., and Wang, C. (2010) Palmitate induced insulin resistance by PKCθ-dependent activation of mTOR/S6K pathway in C2C12 myotubes. Exp. Clin. Endocrinol. Diabetes 118, 657-661
42. Chen, J. L., Lin, H. H., Kim, K. J., Lin, A., Ou, J. H., and Ann, D. K. (2009) PKCδ Signaling. A dual role in regulating hypoxic stress-induced autophagy and apoptosis. Autophagy 5, 244-246
43. Smith, S. J., Cases, S., Jensen, D. R., Chen, H. C., Sande, E., Tow, B., Sanan, D. A., Raber, J., Eckel, R. H., and Farese, R. V., Jr. (2000) Obesity resistance and multiple mechanisms of triglyceride synthesis in mice lacking Dgat. Nat. Genet. 25, 87-90 (Pubitemid 30257043)
44. Stone, S. J., Myers, H. M., Watkins, S. M., Brown, B. E., Feingold, K. R., Elias, P. M., and Farese, R. V., Jr. (2004) Lipopenia and skin barrier abnormalities in DGAT2-deficient mice. J. Biol. Chem. 279, 11767-11776 (Pubitemid 38401682)
45. Yu, C., Chen, Y., Cline, G. W., Zhang, D., Zong, H., Wang, Y., Bergeron, R., Kim, J. K., Cushman, S. W., Cooney, G. J., Atcheson, B., White, M. F., Kraegen, E. W., and Shulman, G. I. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277, 50230-50236 (Pubitemid 36042170)
46. Benoit, S. C., Kemp, C. J., Elias, C. F., Abplanalp, W., Herman, J. P., Migrenne, S., Lefevre, A. L., Cruciani-Guglielmacci, C., Magnan, C., Yu, F., Niswender, K., Irani, B. G., Holland, W. L., and Clegg, D. J. (2009) Palmitic acid mediates hypothalamic insulin resistance by altering PKCθ subcellular localization in rodents. J. Clin. Invest. 119, 2577-2589
47. Eitel, K., Staiger, H., Rieger, J., Mischak, H., Brandhorst, H., Brendel, M. D., Bretzel, R. G., Häring, H. U., and Kellerer, M. (2003) Protein kinase Cδactivation and translocation to the nucleus are required for fatty acidinduced apoptosis of insulin-secreting cells. Diabetes 52, 991-997 (Pubitemid 36384269)
48. Shahnazari, S., Yen, W. L., Birmingham, C. L., Shiu, J., Namolovan, A., Zheng, Y. T., Nakayama, K., Klionsky, D. J., and Brumell, J. H. (2010) A diacylglycerol-dependent signaling pathway contributes to regulation of antibacterial autophagy. Cell Host Microbe 8, 137-146
49. Piro, S., Anello, M., Di Pietro, C., Lizzio, M. N., Patanè, G., Rabuazzo, A. M., Vigneri, R., Purrello, M., and Purrello, F. (2002) Chronic exposure to free fatty acids or high glucose induces apoptosis in rat pancreatic islets. Possible role of oxidative stress. Metabolism 51, 1340-1347 (Pubitemid 35174157)
50. Borradaile, N. M., Han, X., Harp, J. D., Gale, S. E., Ory, D. S., and Schaffer, J. E. (2006) Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 47, 2726-2737 (Pubitemid 44936086)