Liver X Receptor activation downregulates AKT survival signaling in lipid rafts and induces apoptosis of prostate cancer cells

Oncogene

Volumn 29, Issue 18, 2010, Pages 2712-2723

  Pommier, A J C ^a,b,c   Alves, G ^a,b,c   Viennois, E ^a,b,c   Bernard, S ^b   Communal, Y ^d   Sion, B ^a   Marceau, G ^a,b,e   Damon, C ^a,b   Mouzat, K ^f   Caira, F ^a,b,c   Baron, S ^a,b,c   Lobaccaro, J M A ^a,b,c  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b CNRS   (France)

^c CRNH AUVERGNE   (France)

^d CENTRE JEAN PERRIN   (France)

^e UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^f NÎMES UNIVERSITY HOSPITAL   (France)

Author keywords

Apoptosis; Cholesterol; Lipid rafts; LXRs; Prostate

Indexed keywords

ABC TRANSPORTER G1; CELL NUCLEUS RECEPTOR; CHOLESTEROL; LIVER X RECEPTOR; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL CULTURE; CELL MEMBRANE; CELL SURVIVAL; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; LIPID RAFT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; RNA INTERFERENCE; UPREGULATION; XENOGRAFT;

ANIMALS; APOPTOSIS; ATP-BINDING CASSETTE TRANSPORTERS; CARBON-CARBON LIGASES; CELL LINE, TUMOR; CHOLESTEROL; DOWN-REGULATION; HYDROCARBONS, FLUORINATED; MALE; MEMBRANE MICRODOMAINS; MICE; MICE, NUDE; ORPHAN NUCLEAR RECEPTORS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SULFONAMIDES;

MUS MUSCULUS;

EID: 77952242043     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.30     Document Type: Article

References (52)

1. Adam RM, Mukhopadhyay NK, Kim J, Di Vizio D, Cinar B, Boucher K et al. (2007). Cholesterol sensitivity of endogenous and myristoylated Akt. Cancer Res 67: 6238-6246.
2. Ahmed NN, Grimes HL, Bellacosa A, Chan TO, Tsichlis PN. (1997). Transduction of interleukin-2 antiapoptotic and proliferative signals via Akt protein kinase. Proc Natl Acad Sci USA 94: 3627-3632.
3. Beckers A, Organe S, Timmermans L, Scheys K, Peeters A, Brussel-mans K et al. (2007). Chemical inhibition of acetyl-CoA carboxylase induces growth arrest and cytotoxicity selectively in cancer cells. Cancer Res 67: 8180-8187.
4. Bravi F, Scotti L, Bosetti C, Talamini R, Negri E, Montella M et al. (2006). Self-reported history of hypercholesterolaemia and gallstones and the risk of prostate cancer. Ann Oncol 17: 1014-1017.
5. Brusselmans K, De Schrijver E, Verhoeven G, Swinnen JV. (2005). RNA interference-mediated silencing of the acetyl-CoA-carboxy-lase-alpha gene induces growth inhibition and apoptosis of prostate cancer cells. Cancer Res 65: 6719-6725.
6. Brusselmans K, Timmermans L, Van de Sande T, Van Veldhoven PP, Guan G, Shechter I et al. (2007). Squalene synthase, a determinant of Raft-associated cholesterol and modulator of cancer cell proliferation. J Biol Chem 282: 18777-18785.
7. Carson JP, Kulik G, Weber MJ. (1999). Antiapoptotic signaling in LNCaP prostate cancer cells: a survival signaling pathway independent of phosphatidylinositol 3-kinase and Akt/protein kinase B. Cancer Res 59: 1449-1453.
8. Choe SS, Choi AH, Lee JW, Kim KH, Chung JJ, Park J et al. (2007). Chronic activation of liver X receptor induces\{beta\}-cell apoptosis through hyperactivation of lipogenesis. Diabetes 56: 1534-1543.
9. Chuu CP, Hiipakka RA, Kokontis JM, Fukuchi J, Chen RY, Liao S. (2006). Inhibition of tumor growth and progression of LNCaP prostate cancer cells in athymic mice by androgen and liver X receptor agonist. Cancer Res 66: 6482-6486.
10. Demierre MF, Higgins PD, Gruber SB, Hawk E, Lippman SM. (2005). Statins and cancer prevention. Nat Rev Cancer 5: 930-942.
11. Dwyer JR, Sever N, Carlson M, Nelson SF, Beachy PA, Parhami F. (2007). Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J Biol Chem 282: 8959-8968.
12. Fan L, Pepicelli CV, Dibble CC, Catbagan W, Zarycki JL, Laciak R et al. (2004). Hedgehog signaling promotes prostate xenograft tumor growth. Endocrinology 145: 3961-3970.
13. Frankel DJ, Pfeiffer JR, Surviladze Z, Johnson AE, Oliver JM, Wilson BS et al. (2006). Revealing the topography of cellular membrane domains by combined atomic force microscopy/fluorescence imaging. Biophys J 90: 2404-2413.
14. Freeman MR, Solomon KR. (2004). Cholesterol and prostate cancer. J Cell Biochem 91: 54-69.
15. Fukuchi J, Kokontis JM, Hiipakka RA, Chuu CP, Liao S. (2004a). Antiproliferative effect of liver X receptor agonists on LNCaP human prostate cancer cells. Cancer Res 64: 7686-7689.
16. Fukuchi J, Hiipakka RA, Kokontis JM, Hsu S, Ko AL, Fitzgerald ML et al. (2004b). Androgenic suppression of ATP-binding cassette transporter A1 expression in LNCaP human prostate cancer cells. Cancer Res 64: 7682-7685.
17. Grizard G, Sion B, Bauchart DD, Boucher D. (2000). Separation and quantification of cholesterol and major phospholipid classes in human semen by high-performance liquid chromatography and light-scattering detection. J Chromatogr B Biomed Sci Appl 740: 101-107.
18. Hill MM, Feng J, Hemmings BA. (2002). Identification of a plasma membrane Raft-associated PKB Ser473 kinase activity that is distinct from ILK and PDK1. Curr Biol 12: 1251-1255.
19. Karhadkar SS, Bova GS, Abdallah N, Dhara S, Gardner D, Maitra A et al. (2004). Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 431: 707-712.
20. Karpen HE, Bukowski JT, Hughes T, Gratton JP, Sessa WC, Gailani MR. (2001). The sonic hedgehog receptor patched associates with caveolin-1 in cholesterol-rich microdomains of the plasma membrane. J Biol Chem 276: 19503-19511.
21. Kim HJ, Andersson LC, Bouton D, Warner M, Gustafsson JA. (2009). Stromal growth and epithelial cell proliferation in ventral prostates of liver X receptor knockout mice. Proc Natl Acad Sci USA 106: 558-563.
22. Laffitte BA, Chao LC, Li J, Walczak R, Hummasti S, Joseph SB et al. (2003). Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc Natl Acad Sci USA 100: 5419-5424.
23. Lawrence JC, Saslowsky DE, Edwardson JM, Henderson RM. (2003). Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy. Biophys J 84: 1827-1832.
24. Li YC, Park MJ, Ye SK, Kim CW, Kim YN. (2006). Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents. Am J Pathol 168: 1107-1118 (quiz 1404-5).
25. Liao Y, Grobholz R, Abel U, Trojan L, Michel MS, Angel P et al. (2003). Increase of AKT/PKB expression correlates with gleason pattern in human prostate cancer. Int J Cancer 107: 676-680.
26. Magura L, Blanchard R, Hope B, Beal JR, Schwartz GG, Sahmoun AE. (2008). Hypercholesterolemia and prostate cancer: a hospital-based case-control study. Cancer Causes Control 19: 1259-1266.
27. Meng ZX, Nie J, Ling JJ, Sun JX, Zhu YX, Gao L et al. (2009). Activation of liver X receptors inhibits pancreatic islet beta cell proliferation through cell cycle arrest. Diabetologia 52: 125-135.
28. Mo H, Elson CE. (2004). Studies of the isoprenoid-mediated inhibition of mevalonate synthesis applied to cancer chemotherapy and chemoprevention. Exp Biol Med (Maywood) 229: 567-585.
29. Mouzat K, Volat F, Baron S, Alves G, Pommier AJ, Volle DH et al. (2009). Absence of nuclear receptors for oxysterols liver X receptor induces ovarian hyperstimulation syndrome in mice. Endocrinology 150: 3369-3375.
30. Murtola TJ, Visakorpi T, Lahtela J, Syvala H, Tammela T. (2008). Statins and prostate cancer prevention: where we are now, and future directions. Nat Clin Pract Urol 5: 376-387.
31. Pizer ES, Pflug BR, Bova GS, Han WF, Udan MS, Nelson JB. (2001). Increased fatty acid synthase as a therapeutic target in androgen-independent prostate cancer progression. Prostate 47: 102-110.
32. Poynter JN, Gruber SB, Higgins PD, Almog R, Bonner JD, Rennert HS et al. (2005). Statins and the risk of colorectal cancer. N Engl J Med 352: 2184-2192.
33. Rossi S, Graner E, Febbo P, Weinstein L, Bhattacharya N, Onody T et al. (2003). Fatty acid synthase expression defines distinct molecular signatures in prostate cancer. Mol Cancer Res 1: 707-715.
34. Rusinol AE, Thewke D, Liu J, Freeman N, Panini SR, Sinensky MS. (2004). AKT/protein kinase B regulation of BCL family members during oxysterol-induced apoptosis. J Biol Chem 279: 1392-1399.
35. Sanchez P, Hernandez AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A et al. (2004). Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci USA 101: 12561-12566.
36. Sekine Y, Furuya Y, Nishii M, Koike H, Matsui H, Suzuki K. (2008). Simvastatin inhibits the proliferation of human prostate cancer PC-3 cells via down-regulation of the insulin-like growth factor 1 receptor. Biochem Biophys Res Commun 372: 356-361.
37. Shannon J, Tewoderos S, Garzotto M, Beer TM, Derenick R, Palma A et al. (2005). Statins and prostate cancer risk: a case-control study. Am J Epidemiol 162: 318-325.
38. Simons K, Toomre D. (2000). Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39.
39. Solomon KR, Rudd CE, Finberg RW. (1996). The association between glycosylphosphatidylinositol-anchored proteins and het-erotrimeric G protein alpha subunits in lymphocytes. Proc Natl Acad Sci USA 93: 6053-6058.
40. Swinnen JV, Roskams T, Joniau S, Van Poppel H, Oyen R, Baert L 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.
41. Swyer G. (1942). The cholesterol content of normal and enlarged prostates. Cancer Res 2: 372-375.
42. Tontonoz P, Mangelsdorf DJ. (2003). Liver X receptor signaling pathways in cardiovascular disease. Mol Endocrinol 17: 985-993.
43. Ukomadu C, Dutta A. (2003). Inhibition of cdk2 activating phosphorylation by mevastatin. J Biol Chem 278: 4840-4846.
44. Umekita Y, Hiipakka RA, Kokontis JM, Liao S. (1996). Human prostate tumor growth in athymic mice: inhibition by andro-gens and stimulation by finasteride. Proc Natl Acad Sci USA 93: 11802-11807.
45. Volle DH, Lobaccaro JM. (2007). Role of the nuclear receptors for oxysterols LXRs in steroidogenic tissues: beyond the 'foie gras', the steroids and sex? Mol Cell Endocrinol 265-266: 183-189.
46. Walczak R, Joseph SB, Laffitte BA, Castrillo A, Pei L, Tontonoz P. (2004). Transcription of the vascular endothelial growth factor gene in macrophages is regulated by liver X receptors. J Biol Chem 279: 9905-9911.
47. Wessel D, Flugge UI. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143.
48. White C. (1909). On the occurence of crystals in tumours. J Pathol Bacteriol 13: 3-10.
49. Yang G, Truong LD, Timme TL, Ren C, Wheeler TM, Park SH et al. (1998). Elevated expression of caveolin is associated with prostate and breast cancer. Clin Cancer Res 4: 1873-1880.
50. Yang L, Sinensky MS. (2000). 25-Hydroxycholesterol activates a cytochrome c release-mediated caspase cascade. Biochem Biophys Res Commun 278: 557-563.
51. Yuan XJ, Whang YE. (2002). PTEN sensitizes prostate cancer cells to death receptor-mediated and drug-induced apoptosis through a FADD-dependent pathway. Oncogene 21: 319-327.
52. Zhuang L, Kim J, Adam RM, Solomon KR, Freeman MR. (2005). Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. J Clin Invest 115: 959-968.