Oleate-mediated activation of phospholipase D and mammalian target of rapamycin (mTOR) regulates proliferation and rapamycin sensitivity of hepatocarcinoma cells

Diabetologia

Volumn 54, Issue 4, 2011, Pages 954-964

  Arous, C ^a,b   Naimi M ^a,b,c   Van Obberghen, E ^a,b,c  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b INSERM   (France)

^c PASTEUR HOSPITAL   (France)

Author keywords

Liver cancer; mTORC1; Oleate; Phospholipase D; Proliferation; Rapamycin resistance

Indexed keywords

FATTY ACID; FREE FATTY ACID BSA; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; OLEIC ACID; PHOSPHOLIPASE D; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CELL CULTURE; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL STRAIN HEPG2; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG SENSITIVITY; ENZYME ACTIVATION; FATTY LIVER; FLUORESCENCE ACTIVATED CELL SORTING; LIVER CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BLOTTING, WESTERN; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN A; FLOW CYTOMETRY; HEP G2 CELLS; HUMANS; OLEIC ACID; PHOSPHOLIPASE D; PHOSPHOPROTEINS; PROTEINS; SIROLIMUS; TRIGLYCERIDES;

EID: 79953830502     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-2032-1     Document Type: Article

References (39)

1. Whittaker S, Marais R, Zhu AX (2010) The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene 29:4989-5005
2. Fausto N (1999) Mouse liver tumorigenesis: models, mechanisms, and relevance to human disease. Semin Liver Dis 19:243-252
3. Caldwell SH, Crespo DM, Kang HS, Al-Osaimi AM (2004) Obesity and hepatocellular carcinoma. Gastroenterology 127:S97-S103 (Pubitemid 39423375)
4. Shteyer E, Liao Y, Muglia LJ, Hruz PW, Rudnick DA (2004) Disruption of hepatic adipogenesis is associated with impaired liver regeneration in mice. Hepatology 40:1322-1332 (Pubitemid 39657006)
5. Tiniakos DG, Vos MB, Brunt EM (2010) Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol 5:145-171
6. Malhi H, Bronk SF, Werneburg NW, Gores GJ (2006) Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 281:12093-12101 (Pubitemid 43855473)
7. Vinciguerra M, Carrozzino F, Peyrou M et al (2009) Unsaturated fatty acids promote hepatoma proliferation and progression through downregulation of the tumor suppressor PTEN. J Hepatol 50:1132-1141
8. Park EJ, Lee JH, Yu GY et al (2010) Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 140:197-208
9. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J (2004) mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 24:200-216 (Pubitemid 38010048)
10. Mordier S, Iynedjian PB (2007) Activation of mammalian target of rapamycin complex 1 and insulin resistance induced by palmitate in hepatocytes. Biochem Biophys Res Commun 362:206-211 (Pubitemid 47296312)
11. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471-484
12. Toschi A, Lee E, Xu L, Garcia A, Gadir N, Foster DA (2009) Regulation of mTORC1 and mTORC2 complex assembly by phosphatidic acid: competition with rapamycin. Mol Cell Biol 29:1411-1420
13. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J (2001) phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294:1942-1945 (Pubitemid 33101594)
14. Lehman N, Ledford B, Di Fulvio M, Frondorf K, McPhail LC, Gomez-Cambronero J (2007) Phospholipase D2-derived phosphatidic acid binds to and activates ribosomal p70 S6 kinase independently of mTOR. FASEB J 21:1075-1087 (Pubitemid 46495697)
15. Kim JH, Kim Y, Lee SD et al (1999) Selective activation of phospholipase D2 by unsaturated fatty acid. FEBS Lett 454:42-46 (Pubitemid 29296922)
16. Foster DA (2009) Phosphatidic acid signaling to mTOR: signals for the survival of human cancer cells. Biochim Biophys Acta 1791:949-955
17. Toschi A, Lee E, Thompson S et al (2010) Phospholipase DmTOR requirement for the Warburg effect in human cancer cells. Cancer Lett 299:72-79
18. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB (2008) The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 7:11-20
19. Ramirez-Zacarias JL, Castro-Munozledo F, Kuri-Harcuch W (1992) Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry 97:493-497
20. Chaussade C, Pirola L, Bonnafous S et al (2003) Expression of myotubularin by an adenoviral vector demonstrates its function as a phosphatidylinositol 3-phosphate [PtdIns(3)P] phosphatase in muscle cell lines: involvement of PtdIns(3)P in insulin-stimulated glucose transport. Mol Endocrinol 17:2448-2460 (Pubitemid 37542209)
21. Tajima H, Matsumoto K, Nakamura T (1991) Hepatocyte growth factor has potent anti-proliferative activity in various tumor cell lines. FEBS Lett 291:229-232
22. Masaki T, Shiratori Y, Rengifo Wet al (2003) Cyclins and cyclin-dependent kinases: comparative study of hepatocellular carcinoma vs cirrhosis. Hepatology 37:534-543 (Pubitemid 36258774)
23. Huynh H, Do PT, Nguyen TH et al (2004) Extracellular signal-regulated kinase induces cyclin D1 and Cdk-2 expression and phosphorylation of retinoblastoma in hepatocellular carcinoma. Int J Oncol 25:1839-1847
24. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J (2008) Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 105:17414-17419
25. Calle EE, Kaaks R (2004) Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4:579-591 (Pubitemid 39025053)
26. Newgard CB, An J, Bain JR et al (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9:311-326
27. Shimomura I, Matsuda M, Hammer RE, Bashmakov Y, Brown MS, Goldstein JL (2000) Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Mol Cell 6:77-86
28. Li S, Brown MS, Goldstein JL (2010) Bifurcation of insulin signaling pathway in rat liver: mTORC1 required for stimulation of lipogenesis, but not inhibition of gluconeogenesis. Proc Natl Acad Sci USA 107:3441-3446
29. Laplante M, Sabatini DM (2009) An emerging role of mTOR in lipid biosynthesis. Curr Biol 19:R1046-R1052
30. Tsukada Y, Miyazawa K, Kitamura N (2001) High intensity ERK signal mediates hepatocyte growth factor-induced proliferation inhibition of the human hepatocellular carcinoma cell line HepG2. J Biol Chem 276:40968-40976
31. Sato T, Nakashima A, Guo L, Coffman K, Tamanoi F (2010) Single amino-acid changes that confer constitutive activation of mTOR are discovered in human cancer. Oncogene 29:2746-2752
32. Carracedo A, Ma L, Teruya-Feldstein J et al (2008) Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest 118:3065-3074
33. Newell P, Toffanin S, Villanueva A et al (2009) Ras pathway activation in hepatocellular carcinoma and anti-tumoral effect of combined sorafenib and rapamycin in vivo. J Hepatol 51:725-733
34. Patursky-Polischuk I, Stolovich-Rain M, Hausner-Hanochi M et al (2009) The TSC-mTOR pathway mediates translational activation of TOP mRNAs by insulin largely in a raptor- or rictor-independent manner. Mol Cell Biol 29:640-649
35. Sonenberg N, Gingras A-C (1998) The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr Opin Cell Biol 10:268-275 (Pubitemid 28174770)
36. Jiang YP, Ballou LM, Lin RZ (2001) Rapamycin-insensitive regulation of 4e-BP1 in regenerating rat liver. J Biol Chem 276:10943-10951 (Pubitemid 38089273)
37. Brasaemle DL (2006) Cell biology: Enhanced: a metabolic push to proliferate. Science 313:1581-1582
38. Fritz V, Benfodda Z, Rodier G et al (2010) 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 9:1740-1754
39. Thoreen CC, Kang SA, Chang JWet al (2009) An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 284:8023-8032