Critical role of SCD1 in autophagy regulation via lipogenesis and lipid rafts-coupled AKT-FOXO1 signaling pathway

Autophagy

Volumn 10, Issue 2, 2014, Pages 226-242

  Tan, Shi Hao ^a,b   Shui, Guanghou ^c   Zhou, Jing ^a   Shi, Yin ^a   Huang, Jingxiang ^d   Xia, Dajing ^e   Wenk, Markus R ^a,b   Shen, Han Ming ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

AKT; Autophagy; FOXO1; Lipid rafts; Lipogenesis; SCD1; TSC2

Indexed keywords

ACYL COENZYME A DESATURASE 1; BECLIN 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MESSENGER RNA; PROTEIN BNIP3; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR; TUBERIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOLYSOSOME; AUTOPHAGY; CELL GROWTH; CELL SURVIVAL; CELL VIABILITY; EMBRYO; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME INHIBITION; FIBROBLAST; GENE SILENCING; GENETIC TRANSCRIPTION; LIPID METABOLISM; LIPID RAFT; LIPOGENESIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AKT; AUTOPHAGY; FOXO1; LIPID RAFTS; LIPOGENESIS; SCD1; TSC2;

ACYL COENZYME A; ANIMALS; APOPTOSIS; AUTOPHAGY; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; LIPID METABOLISM; LIPOGENESIS; MICE; MULTIPROTEIN COMPLEXES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84894468653     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.27003     Document Type: Article

References (64)

1. Bhaskar PT, Hay N. The two TORCs and Akt. Dev Cell 2007; 12:487-502; PMID:17419990; http://dx.doi.org/10.1016/j.devcel.2007.03.020
2. Kwiatkowski DJ, Manning BD. Tuberous sclerosis: a GAP at the crossroads of multiple signaling pathways. Hum Mol Genet 2005; 14 Spec No. 2:R251-8; PMID:16244323; http://dx.doi.org/10.1093/hmg/ddi260
3. Jewell JL, Guan KL. Nutrient signaling to mTOR and cell growth. Trends Biochem Sci 2013; 38:233-42; PMID:23465396; http://dx.doi.org/10.1016/j.tibs. 2013.01.004
4. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004; 18:1926-45; PMID:15314020; http://dx.doi.org/10.1101/gad.1212704
5. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011; 12:21-35; PMID:21157483; http://dx.doi.org/10.1038/nrm3025
6. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149:274-93; PMID:22500797; http://dx.doi.org/10.1016/j.cell.2012.03. 017
7. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
8. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324:1029-33; PMID:19460998; http://dx.doi.org/10.1126/science.1160809
9. Düvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, Triantafellow E, Ma Q, Gorski R, Cleaver S, et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 2010; 39:171-83; PMID:20670887; http://dx.doi.org/10.1016/j.molcel.2010.06.022
10. Caron E, Ghosh S, Matsuoka Y, Ashton-Beaucage D, Therrien M, Lemieux S, Perreault C, Roux PP, Kitano H. A comprehensive map of the mTOR signaling network. Mol Syst Biol 2010; 6:453; PMID:21179025; http://dx.doi.org/10.1038/ msb.2010.108
11. Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA, Balderas E, Guertin DA, Madden KL, Carpenter AE, Finck BN, et al. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011; 146:408-20; PMID:21816276; http://dx.doi.org/10.1016/j.cell.2011.06.034
12. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, Griffiths JR, Chung YL, Schulze A. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 2008; 8:224-36; PMID:18762023; http://dx.doi.org/10.1016/j.cmet.2008.07.007
13. Menendez JA, Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 2007; 7:763-77; PMID:17882277; http://dx.doi.org/10.1038/nrc2222
14. Mashima T, Seimiya H, Tsuruo T. De novo fatty-acid synthesis and related pathways as molecular targets for cancer therapy. Br J Cancer 2009; 100:1369-72; PMID:19352381; http://dx.doi.org/10.1038/sj.bjc.6605007
15. Ntambi JM, Miyazaki M. Recent insights into stearoyl-CoA desaturase-1. Curr Opin Lipidol 2003; 14:255-61; PMID:12840656; http://dx.doi.org/10.1097/ 00041433-200306000-00005
16. Scaglia N, Caviglia JM, Igal RA. High stearoyl-CoA desaturase protein and activity levels in simian virus 40 transformed-human lung fibroblasts. Biochim Biophys Acta 2005; 1687:141-51; PMID:15708362; http://dx.doi.org/10.1016/j. bbalip.2004.11.015
17. Scaglia N, Igal RA. Stearoyl-CoA desaturase is involved in the control of proliferation, anchorage-independent growth, and survival in human transformed cells. J Biol Chem 2005; 280:25339-49; PMID:15851470; http://dx.doi.org/10.1074/ jbc.M501159200
18. Fritz V, Benfodda Z, Rodier G, Henriquet C, Iborra F, Avancès C, Allory Y, de la Taille A, Culine S, Blancou H, et al. Abrogation of de novo lipogenesis by stearoyl-CoA desaturase 1 inhibition interferes with oncogenic signaling and blocks prostate cancer progression in mice. Mol Cancer Ther 2010; 9:1740-54; PMID:20530718; http://dx.doi.org/10.1158/1535-7163.MCT-09-1064
19. Hess D, Chisholm JW, Igal RA. Inhibition of stearoylCoA desaturase activity blocks cell cycle progression and induces programmed cell death in lung cancer cells. PLoS One 2010; 5:e11394; PMID:20613975; http://dx.doi.org/10. 1371/journal.pone.0011394
20. Minville-Walz M, Pierre AS, Pichon L, Bellenger S, Fèvre C, Bellenger J, Tessier C, Narce M, Rialland M. Inhibition of stearoyl-CoA desaturase 1 expression induces CHOP-dependent cell death in human cancer cells. PLoS One 2010; 5:e14363; PMID:21179554; http://dx.doi.org/10.1371/journal.pone. 0014363
21. Scaglia N, Chisholm JW, Igal RA. Inhibition of stearoylCoA desaturase-1 inactivates acetyl-CoA carboxylase and impairs proliferation in cancer cells: role of AMPK. PLoS One 2009; 4:e6812; PMID:19710915; http://dx.doi.org/10.1371/ journal.pone.0006812
22. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
23. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003; PMID:19225151; http://dx.doi.org/10.1091/mbc. E08-12-1249
24. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 2010; 22:132-9; PMID:20056399; http://dx.doi.org/10.1016/j. ceb.2009.12.004
25. Tee AR, Fingar DC, Manning BD, Kwiatkowski DJ, Cantley LC, Blenis J. Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. Proc Natl Acad Sci U S A 2002; 99:13571-6; PMID:12271141; http://dx.doi.org/10.1073/pnas. 202476899
26. Laplante M, Sabatini DM. An emerging role of mTOR in lipid biosynthesis. Curr Biol 2009; 19:R1046-52; PMID:19948145; http://dx.doi.org/10.1016/j.cub. 2009.09.058
27. Nashed M, Chisholm JW, Igal RA. Stearoyl-CoA desaturase activity modulates the activation of epidermal growth factor receptor in human lung cancer cells. Exp Biol Med (Maywood) 2012; 237:1007-17; PMID:22946088; http://dx.doi.org/10.1258/ebm.2012.012126
28. Igal RA. Stearoyl-CoA desaturase-1: a novel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis 2010; 31:1509-15; PMID:20595235; http://dx.doi.org/10.1093/ carcin/bgq131
29. Ng S, Wu YT, Chen B, Zhou J, Shen HM. Impaired autophagy due to constitutive mTOR activation sensitizes TSC2-null cells to cell death under stress. Autophagy 2011; 7:1173-86; PMID:21808151; http://dx.doi.org/10.4161/ auto.7.10.16681
30. Huang J, Dibble CC, Matsuzaki M, Manning BD. The TSC1-TSC2 complex is required for proper activation of mTOR complex 2. Mol Cell Biol 2008; 28:4104-15; PMID:18411301; http://dx.doi.org/10.1128/MCB.00289-08
31. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005; 307:1098-101; PMID:15718470; http://dx.doi.org/10.1126/science.1106148
32. Zhang C, Wendel AA, Keogh MR, Harris TE, Chen J, Coleman RA. Glycerolipid signals alter mTOR complex 2 (mTORC2) to diminish insulin signaling. Proc Natl Acad Sci U S A 2012; 109:1667-72; PMID:22307628; http://dx.doi.org/10.1073/pnas. 1110730109
33. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006; 22:159-68; PMID:16603397; http://dx.doi.org/10.1016/j. molcel.2006.03.029
34. García-Martínez JM, Alessi DR. mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem J 2008; 416:375-85; PMID:18925875; http://dx.doi.org/10.1042/BJ20081668
35. Calay D, Vind-Kezunovic D, Frankart A, Lambert S, Poumay Y, Gniadecki R. Inhibition of Akt signaling by exclusion from lipid rafts in normal and transformed epidermal keratinocytes. J Invest Dermatol 2010; 130:1136-45; PMID:20054340; http://dx.doi.org/10.1038/jid.2009.415
36. Zhuang L, Lin J, Lu ML, Solomon KR, Freeman MR. Cholesterol-rich lipid rafts mediate akt-regulated survival in prostate cancer cells. Cancer Res 2002; 62:2227-31; PMID:11956073
37. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1:31-9; PMID:11413487; http://dx.doi.org/10.1038/35036052
38. Yamaguchi H, Takeo Y, Yoshida S, Kouchi Z, Nakamura Y, Fukami K. Lipid rafts and caveolin-1 are required for invadopodia formation and extracellular matrix degradation by human breast cancer cells. Cancer Res 2009; 69:8594-602; PMID:19887621; http://dx.doi.org/10.1158/0008-5472.CAN-09-2305
39. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem 2009; 284:28319-31; PMID:19696026; http://dx.doi.org/10.1074/jbc.M109.024406
40. Xu P, Das M, Reilly J, Davis RJ. JNK regulates FoxO-dependent autophagy in neurons. Genes Dev 2011; 25:310-22; PMID:21325132; http://dx.doi.org/10.1101/ gad.1984311
41. Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S, Wang D, Feng J, Yu L, Zhu WG. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol 2010; 12:665-75; PMID:20543840; http://dx.doi.org/10.1038/ncb2069
42. Zhou J, Liao W, Yang J, Ma K, Li X, Wang Y, Wang D, Wang L, Zhang Y, Yin Y, et al. FOXO3 induces FOXO1-dependent autophagy by activating the AKT1 signaling pathway. Autophagy 2012; 8:1712-23; PMID:22931788; http://dx.doi.org/10.4161/auto.21830
43. Murga C, Laguinge L, Wetzker R, Cuadrado A, Gutkind JS. Activation of Akt/protein kinase B by G protein-coupled receptors. A role for alpha and beta gamma subunits of heterotrimeric G proteins acting through phosphatidylinositol- 3-OH kinasegamma. J Biol Chem 1998; 273:19080-5; PMID:9668091; http://dx.doi.org/10.1074/jbc.273.30.19080
44. Burgering BM, Kops GJ. Cell cycle and death control: long live Forkheads. Trends Biochem Sci 2002; 27:352-60; PMID:12114024; http://dx.doi.org/10.1016/ S0968-0004(02)02113-8
45. Al-Mubarak B, Soriano FX, Hardingham GE. Synaptic NMDAR activity suppresses FOXO1 expression via a cis-acting FOXO binding site: FOXO1 is a FOXO target gene. Channels (Austin) 2009; 3:233-8; PMID:19690465; http://dx.doi.org/10.4161/chan.3.4.9381
46. Nagashima T, Shigematsu N, Maruki R, Urano Y, Tanaka H, Shimaya A, Shimokawa T, Shibasaki M. Discovery of novel forkhead box O1 inhibitors for treating type 2 diabetes: improvement of fasting glycemia in diabetic db/db mice. Mol Pharmacol 2010; 78:961-70; PMID:20736318; http://dx.doi.org/10.1124/ mol.110.065714
47. Hodson L, Fielding BA. Stearoyl-CoA desaturase: rogue or innocent bystander? Prog Lipid Res 2013; 52:15-42; PMID:23000367; http://dx.doi.org/10. 1016/j.plipres.2012.08.002
48. Morgan-Lappe SE, Tucker LA, Huang X, Zhang Q, Sarthy AV, Zakula D, Vernetti L, Schurdak M, Wang J, Fesik SW. Identification of Ras-related nuclear protein, targeting protein for xenopus kinesin-like protein 2, and stearoyl-CoA desaturase 1 as promising cancer targets from an RNAi-based screen. Cancer Res 2007; 67:4390-8; PMID:17483353; http://dx.doi.org/10.1158/0008-5472.CAN-06-4132
49. Tan SH, Shui G, Zhou J, Li JJ, Bay BH, Wenk MR, Shen HM. Induction of autophagy by palmitic acid via protein kinase C-mediated signaling pathway independent of mTOR (mammalian target of rapamycin). J Biol Chem 2012; 287:14364-76; PMID:22408252; http://dx.doi.org/10.1074/jbc.M111.294157
50. Hill MM, Feng J, Hemmings BA. Identification of a plasma membrane Raft-associated PKB Ser473 kinase activity that is distinct from ILK and PDK1. Curr Biol 2002; 12:1251-5; PMID:12176337; http://dx.doi.org/10.1016/S0960- 9822(02)00973-9
51. Simons K, Ikonen E. How cells handle cholesterol. Science 2000; 290:1721-6; PMID:11099405; http://dx.doi.org/10.1126/science.290.5497.1721
52. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007; 8:185-94; PMID:17318224; http://dx.doi.org/10.1038/nrm2122
53. Jones KA, Jiang X, Yamamoto Y, Yeung RS. Tuberin is a component of lipid rafts and mediates caveolin-1 localization: role of TSC2 in post-Golgi transport. Exp Cell Res 2004; 295:512-24; PMID:15093748; http://dx.doi.org/10. 1016/j.yexcr.2004.01.022
54. Miyazaki M, Kim YC, Gray-Keller MP, Attie AD, Ntambi JM. The biosynthesis of hepatic cholesterol esters and triglycerides is impaired in mice with a disruption of the gene for stearoyl-CoA desaturase 1. J Biol Chem 2000; 275:30132-8; PMID:10899171; http://dx.doi.org/10.1074/jbc.M005488200
55. Sun Y, Hao M, Luo Y, Liang CP, Silver DL, Cheng C, Maxfield FR, Tall AR. Stearoyl-CoA desaturase inhibits ATP-binding cassette transporter A1-mediated cholesterol efflux and modulates membrane domain structure. J Biol Chem 2003; 278:5813-20; PMID:12482877; http://dx.doi.org/10.1074/jbc.M208687200
56. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 2011; 286:7468-78; PMID:21159781; http://dx.doi.org/10. 1074/jbc.M110.179242
57. Dobrzyn P, Dobrzyn A, Miyazaki M, Cohen P, Asilmaz E, Hardie DG, Friedman JM, Ntambi JM. Stearoyl-CoA desaturase 1 deficiency increases fatty acid oxidation by activating AMP-activated protein kinase in liver. Proc Natl Acad Sci U S A 2004; 101:6409-14; PMID:15096593; http://dx.doi.org/10.1073/pnas. 0401627101
58. Choo AY, Kim SG, Vander Heiden MG, Mahoney SJ, Vu H, Yoon SO, Cantley LC, Blenis J. Glucose addiction of TSC null cells is caused by failed mTORC1-dependent balancing of metabolic demand with supply. Mol Cell 2010; 38:487-99; PMID:20513425; http://dx.doi.org/10.1016/j.molcel.2010.05.007
59. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ. Autophagy regulates lipid metabolism. Nature 2009; 458:1131-5; PMID:19339967; http://dx.doi.org/10.1038/nature07976
60. Ikenoue T, Hong S, Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods Enzymol 2009; 452:165-80; PMID:19200882; http://dx.doi.org/10.1016/S0076-6879(08)03611-2
61. Wu YT, Zhang S, Kim YS, Tan HL, Whiteman M, Ong CN, Liu ZG, Ichijo H, Shen HM. Signaling pathways from membrane lipid rafts to JNK1 activation in reactive nitrogen species-induced nonapoptotic cell death. Cell Death Differ 2008; 15:386-97; PMID:18007661; http://dx.doi.org/10.1038/sj.cdd.4402273
62. Shui G, Stebbins JW, Lam BD, Cheong WF, Lam SM, Gregoire F, Kusonoki J, Wenk MR. Comparative plasma lipidome between human and cynomolgus monkey: are plasma polar lipids good biomarkers for diabetic monkeys? PLoS One 2011; 6:e19731; PMID:21573191; http://dx.doi.org/10.1371/journal.pone.0019731
63. Shui G, Guan XL, Low CP, Chua GH, Goh JS, Yang H, Wenk MR. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol Biosyst 2010; 6:1008-17; PMID:20485745; http://dx.doi.org/10.1039/b913353d
64. Shui G, Cheong WF, Jappar IA, Hoi A, Xue Y, Fernandis AZ, Tan BK, Wenk MR. Derivatization-independent cholesterol analysis in crude lipid extracts by liquid chromatography/mass spectrometry: applications to a rabbit model for atherosclerosis. J Chromatogr A 2011; 1218:4357-65; PMID:21621788; http://dx.doi.org/10.1016/j.chroma.2011.05.011