Inhibition of stearoyl-CoA desaturase 1 Expression Induces CHOP-dependent cell death in human cancer cells

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Minville Walz, Mélaine ^a   Pierre, Anne Sophie ^a   Pichon, Laurent ^a   Bellenger, Sandrine ^a   Fèvre, Cécile ^a   Bellenger, Jérôme ^a   Tessier, Christian ^a   Narce, Michel ^a   Rialland, Mickaël ^a  

^a Chu   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE 1; CASPASE 3; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; MESSENGER RNA; MONOUNSATURATED FATTY ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OLEIC ACID; SMALL INTERFERING RNA; X BOX BINDING PROTEIN 1; ACYL COENZYME A DESATURASE; FATTY ACID; HEAT SHOCK PROTEIN; INITIATION FACTOR 2; MOLECULAR CHAPERONE GRP78;

APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FATTY ACID SYNTHESIS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; RNA SPLICING; SIGNAL TRANSDUCTION; UPREGULATION; BIOSYNTHESIS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; DRUG ANTAGONISM; METABOLISM; NEOPLASM; TUMOR CELL LINE;

APOPTOSIS; CELL DEATH; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; EUKARYOTIC INITIATION FACTOR-2; FATTY ACIDS; HEAT-SHOCK PROTEINS; HUMANS; NEOPLASMS; OLEIC ACID; RNA, SMALL INTERFERING; STEAROYL-COA DESATURASE; TRANSCRIPTION FACTOR CHOP;

EID: 78650725619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014363     Document Type: Article

References (63)

1. Deberardinis RJ, Sayed N, Ditsworth D, Thompson CB (2008) Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 18: 54-61.
2. Young CD, Anderson SM (2008) Sugar and fat - that's where it's at: metabolic changes in tumors. Breast Cancer Res 10: 202.
3. Swinnen JV, Van Veldhoven PP, Timmermans L, De Schrijver E, Brusselmans K, et al. (2003) Fatty acid synthase drives the synthesis of phospholipids partitioning into detergent-resistant membrane microdomains. Biochem Biophys Res Commun 302: 898-903.
4. Chajes V, Lanson M, Fetissof F, Lhuillery C, Bougnoux P (1995) Membrane fatty acids of breast carcinoma: contribution of host fatty acids and tumor properties. Int J Cancer 63: 169-175.
5. Riboni L, Ghidoni R, Sonnino S, Omodeo-Sale F, Gaini SM, et al. (1984) Phospholipid content and composition of human meningiomas. Neurochem Pathol 2: 171-188.
6. Robert J, Montaudon D, Hugues P (1983) Incorporation and metabolism of exogenous fatty acids by cultured normal and tumoral glial cells. Biochim Biophys Acta 752: 383-395.
7. Yam D, Ben-Hur H, Dgani R, Fink A, Shani A, et al. (1997) Subcutaneous, omentum and tumor fatty acid composition, and serum insulin status in patients with benign or cancerous ovarian or endometrial tumors. Do tumors preferentially utilize polyunsaturated fatty acids? Cancer Lett 111: 179-185.
8. Szachowicz-Petelska B, Sulkowski S, Figaszewski ZA (2007) Altered membrane free unsaturated fatty acid composition in human colorectal cancer tissue. Mol Cell Biochem 294: 237-242.
9. Sakai K, Okuyama H, Yura J, Takeyama H, Shinagawa N, et al. (1992) Composition and turnover of phospholipids and neutral lipids in human breast cancer and reference tissues. Carcinogenesis 13: 579-584.
10. Sabine J, Abraham S, Chaikoff I (1967) Control of lipid metabolism in hepatomas: insensitivity of rate of fatty acid and cholesterol synthesis by mouse hepatoma BW7756 to fasting and to feedback control. Cancer Res 27: 793-799.
11. Kannan R, Lyon I, Baker N (1980) Dietary control of lipogenesis in vivo in host tissues and tumors of mice bearing Ehrlich ascites carcinoma. Cancer Res 40: 4606-4611.
12. Milgraum LZ, Witters LA, Pasternack GR, Kuhajda FP (1997) Enzymes of the fatty acid synthesis pathway are highly expressed in in situ breast carcinoma. Clin Cancer Res 3: 2115-2120.
13. Swinnen JV, Vanderhoydonc F, Elgamal AA, Eelen M, Vercaeren I, et al. (2000) Selective activation of the fatty acid synthesis pathway in human prostate cancer. Int J Cancer 88: 176-179.
14. Kuhajda FP, Jenner K, Wood FD, Hennigar RA, Jacobs LB, et al. (1994) Fatty acid synthesis: a potential selective target for antineoplastic therapy. Proc Natl Acad Sci U S A 91: 6379-6383.
15. Swinnen JV, Roskams T, Joniau S, Van Poppel H, Oyen R, et al. (2002) Overexpression of fatty acid synthase is an early and common event in the development of prostate cancer. Int J Cancer 98: 19-22.
16. Piyathilake CJ, Frost AR, Manne U, Bell WC, Weiss H, et al. (2000) The expression of fatty acid synthase (FASE) is an early event in the development and progression of squamous cell carcinoma of the lung. Hum Pathol 31: 1068-1073.
17. Rashid A, Pizer ES, Moga M, Milgraum LZ, Zahurak M, et al. (1997) Elevated expression of fatty acid synthase and fatty acid synthetic activity in colorectal neoplasia. Am J Pathol 150: 201-208.
18. Wang J, Yu L, Schmidt RE, Su C, Huang X, et al. (2005) Characterization of HSCD5, a novel human stearoyl-CoA desaturase unique to primates. Biochem Biophys Res Commun 332: 735-742.
19. Falvella FS, Pascale RM, Gariboldi M, Manenti G, De Miglio MR, et al. (2002) Stearoyl-CoA desaturase 1 (Scd1) gene overexpression is associated with genetic predisposition to hepatocarcinogenesis in mice and rats. Carcinogenesis 23: 1933-1936.
20. Griffitts J, Tesiram Y, Reid GE, Saunders D, Floyd RA, et al. (2009) In vivo MRS assessment of altered fatty acyl unsaturation in liver tumor formation of a TGF alpha/c-myc transgenic mouse model. J Lipid Res 50: 611-622.
21. Li J, Ding SF, Habib NA, Fermor BF, Wood CB, et al. (1994) Partial characterization of a cDNA for human stearoyl-CoA desaturase and changes in its mRNA expression in some normal and malignant tissues. Int J Cancer 57: 348-352.
22. Fritz V, Benfodda Z, Rodier G, Henriquet C, Iborra F, 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.
23. Moore S, Knudsen B, True LD, Hawley S, Etzioni R, et al. (2005) Loss of stearoyl-CoA desaturase expression is a frequent event in prostate carcinoma. Int J Cancer 114: 563-571.
24. Scaglia N, Chisholm JW, Igal RA (2009) Inhibition of stearoylCoA desaturase-1 inactivates acetyl-CoA carboxylase and impairs proliferation in cancer cells: role of AMPK. PLoS One 4: e6812.
25. Morgan-Lappe SE, Tucker LA, Huang X, Zhang Q, Sarthy AV, et al. (2007) 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 67: 4390-4398.
26. Scaglia N, Caviglia JM, Igal RA (2005) High stearoyl-CoA desaturase protein and activity levels in simian virus 40 transformed-human lung fibroblasts. Biochim Biophys Acta 1687: 141-151.
27. Ariyama H, Kono N, Matsuda S, Inoue T, Arai H (2010) Decrease in membrane phospholipid unsaturation induces unfolded protein response. J Biol Chem.
28. Scaglia N, Igal RA (2008) Inhibition of Stearoyl-CoA Desaturase 1 expression in human lung adenocarcinoma cells impairs tumorigenesis. Int J Oncol 33: 839-850.
29. Hardy S, Langelier Y, Prentki M (2000) Oleate activates phosphatidylinositol 3- kinase and promotes proliferation and reduces apoptosis of MDA-MB-231 breast cancer cells, whereas palmitate has opposite effects. Cancer Res 60: 6353-6358.
30. van der Sanden MH, Houweling M, van Golde LM, Vaandrager AB (2003) Inhibition of phosphatidylcholine synthesis induces expression of the endoplasmic reticulum stress and apoptosis-related protein CCAAT/enhancer-binding protein-homologous protein (CHOP/GADD153). Biochem J 369: 643-650.
31. van der Sanden MH, Meems H, Houweling M, Helms JB, Vaandrager AB (2004) Induction of CCAAT/enhancer-binding protein (C/EBP)-homologous protein/growth arrest and DNA damage-inducible protein 153 expression during inhibition of phosphatidylcholine synthesis is mediated via activation of a C/EBP-activating transcription factor-responsive element. J Biol Chem 279: 52007-52015.
32. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
33. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, et al. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6: 1099-1108.
34. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, et al. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129: 1337-1349.
35. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, et al. (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109: 525-532.
36. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, et al. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12: 982-995.
37. Thomas KC, Sabnis AS, Johansen ME, Lanza DL, Moos PJ, et al. (2007) Transient receptor potential vanilloid 1 agonists cause endoplasmic reticulum stress and cell death in human lung cells. J Pharmacol Exp Ther 321: 830-838.
38. Qiao D, Im E, Qi W, Martinez JD (2002) Activator protein-1 and CCAAT/ enhancer-binding protein mediated GADD153 expression is involved in deoxycholic acid-induced apoptosis. Biochim Biophys Acta 1583: 108-116.
39. Scaglia N, Igal RA (2005) Stearoyl-CoA desaturase is involved in the control of proliferation, anchorage-independent growth, and survival in human transformed cells. J Biol Chem 280: 25339-25349.
40. Almaguel FG, Liu JW, Pacheco FJ, Casiano CA, De Leon M (2009) Activation and reversal of lipotoxicity in PC12 and rat cortical cells following exposure to palmitic acid. J Neurosci Res 87: 1207-1218.
41. Hardy S, El-Assaad W, Przybytkowski E, Joly E, Prentki M, et al. (2003) Saturated fatty acid-induced apoptosis in MDA-MB-231 breast cancer cells. A role for cardiolipin. J Biol Chem 278: 31861-31870.
42. Peter A, Weigert C, Staiger H, Rittig K, Cegan A, et al. (2008) Induction of stearoyl-CoA desaturase protects human arterial endothelial cells against lipotoxicity. Am J Physiol Endocrinol Metab 295: E339-349.
43. Wei Y, Wang D, Pagliassotti MJ (2007) Saturated fatty acid-mediated endoplasmic reticulum stress and apoptosis are augmented by trans-10, cis-12- conjugated linoleic acid in liver cells. Mol Cell Biochem 303: 105-113.
44. Vinciguerra M, Carrozzino F, Peyrou M, Carlone S, Montesano R, et al. (2009) Unsaturated fatty acids promote hepatoma proliferation and progression through downregulation of the tumor suppressor PTEN. J Hepatol 50: 1132-1141.
45. Hess D, Chisholm JW, Igal RA (2010) Inhibition of stearoylCoA desaturase activity blocks cell cycle progression and induces programmed cell death in lung cancer cells. PLoS One 5: e11394.
46. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Jr., et al. (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 100: 3077-3082.
47. Jackowski S (1996) Cell cycle regulation of membrane phospholipid metabolism. J Biol Chem 271: 20219-20222.
48. Siperstein MD (1984) Role of cholesterogenesis and isoprenoid synthesis in DNA replication and cell growth. J Lipid Res 25: 1462-1468.
49. Baburina I, Jackowski S (1998) Apoptosis triggered by 1-O-octadecyl-2-Omethyl- rac-glycero-3-phosphocholine is prevented by increased expression of CTP:phosphocholine cytidylyltransferase. J Biol Chem 273: 2169-2173.
50. Cui Z, Houweling M, Chen MH, Record M, Chap H, et al. (1996) A genetic defect in phosphatidylcholine biosynthesis triggers apoptosis in Chinese hamster ovary cells. J Biol Chem 271: 14668-14671.
51. Yeung BH, Kwan BW, He QY, Lee AS, Liu J, et al. (2008) Glucose-regulated protein 78 as a novel effector of BRCA1 for inhibiting stress-induced apoptosis. Oncogene 27: 6782-6789.
52. Jiang CC, Chen LH, Gillespie S, Wang YF, Kiejda KA, et al. (2007) Inhibition of MEK sensitizes human melanoma cells to endoplasmic reticulum stressinduced apoptosis. Cancer Res 67: 9750-9761.
53. Jiang CC, Mao ZG, Avery-Kiejda KA, Wade M, Hersey P, et al. (2009) Glucose-regulated protein 78 antagonizes cisplatin and adriamycin in human melanoma cells. Carcinogenesis 30: 197-204.
54. Pyrko P, Schonthal AH, Hofman FM, Chen TC, Lee AS (2007) The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res 67: 9809-9816.
55. Karaskov E, Scott C, Zhang L, Teodoro T, Ravazzola M, et al. (2006) Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147: 3398-3407.
56. Ou L, Wu Y, Ip C, Meng X, Hsu YC, et al. (2008) Apoptosis induced by t10,c12-conjugated linoleic acid is mediated by an atypical endoplasmic reticulum stress response. J Lipid Res 49: 985-994.
57. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
58. Lin JH, Li H, Zhang Y, Ron D, Walter P (2009) Divergent effects of PERK and IRE1 signaling on cell viability. PLoS One 4: e4170.
59. Jiang HY, Wek RC (2005) Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 280: 14189-14202.
60. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21: 1249-1259.
61. Rasheva VI, Domingos PM (2009) Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 14: 996-1007.
62. Koltun DO, Parkhill EQ, Vasilevich NI, Glushkov AI, Zilbershtein TM, et al. (2009) Novel, potent, selective, and metabolically stable stearoyl-CoA desaturase (SCD) inhibitors. Bioorg Med Chem Lett 19: 2048-2052.
63. Leger S, Black WC, Deschenes D, Dolman S, Falgueyret JP, et al. (2010) Synthesis and biological activity of a potent and orally bioavailable SCD inhibitor (MF-438). Bioorg Med Chem Lett 20: 499-502.