Activation of androgen receptor, lipogenesis, and oxidative stress converged by SREBP-1 is responsible for regulating growth and progression of prostate cancer cells

Molecular Cancer Research

Volumn 10, Issue 1, 2012, Pages 133-142

  Huang, Wen Chin ^a   Li, Xiangyan ^a   Liu, Jian ^b   Lin, Jentai ^c   Chung, Leland W K ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; FAT DROPLET; FATTY ACID SYNTHASE; NITRATE REDUCTASE (NADPH); REACTIVE OXYGEN METABOLITE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CASTRATION RESISTANT PROSTATE CANCER; CELL GROWTH; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DRUG MECHANISM; GENE OVEREXPRESSION; GENE SILENCING; GLEASON SCORE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID STORAGE; LIPOGENESIS; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION;

ANIMALS; CARCINOMA; CELL GROWTH PROCESSES; DISEASE PROGRESSION; HUMANS; LIPOGENESIS; MALE; MICE; MICE, NUDE; OXIDATIVE STRESS; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; RECEPTORS, ANDROGEN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTIONAL ACTIVATION; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84862908756     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0206     Document Type: Article

References (48)

1. Heinlein CA, Chang C. Androgen receptor in prostate cancer. Endocr Rev 2004;25:276-308. (Pubitemid 38501396)
2. Grossmann ME, Huang H, Tindall DJ. Androgen receptor signaling in androgen-refractory prostate cancer. J Natl Cancer Inst 2001;93:1687-97. (Pubitemid 33130257)
3. Ruizeveld de Winter JA, Janssen PJ, Sleddens HM, Verleun-Mooijman MC, Trapman J, Brinkmann AO, et al. Androgen receptor status in localized and locally progressive hormone refractory human prostate cancer. Am J Pathol 1994;144:735-46. (Pubitemid 24172062)
4. Leon CG, Locke JA, Adomat HH, Etinger SL, Twiddy AL, Neumann RD, et al. Alterations in cholesterol regulation contribute to the production of intratumoral androgens during progression to castration-resistant prostate cancer in a mouse xenograft model. Prostate 2010;70:390-400.
5. Huang WC, Zhau HE, Chung LW. Androgen receptor survival signaling is blocked by anti-{beta}2-microglobulin monoclonal antibody via a mitogen-activated protein kinase/lipogenic pathway in human prostate cancer cells. J Biol Chem 2010;285:7947-56.
6. Swinnen JV, Heemers H, van de Sande T, de Schrijver E, Brusselmans K, Heyns W, et al. Androgens, lipogenesis and prostate cancer. J Steroid Biochem Mol Biol 2004;92:273-9. (Pubitemid 40128248)
7. Di Vizio D, Solomon KR, Freeman MR. Cholesterol and cholesterol-rich membranes in prostate cancer: an update. Tumori 2008;94:633-9.
8. Cinar B, Mukhopadhyay NK, Meng G, Freeman MR. Phosphoinositide 3-kinase-independent non-genomic signals transit from the androgen receptor to Akt1 in membrane raft microdomains. J Biol Chem 2007;282:29584-93. (Pubitemid 350043392)
9. Freeman MR, Cinar B, Lu ML. Membrane rafts as potential sites of nongenomic hormonal signaling in prostate cancer. Trends Endocrinol Metab 2005;16:273-9. (Pubitemid 41058759)
10. Strom SS, Yamamura Y, Forman MR, Pettaway CA, Barrera SL, DiGiovanni J. Saturated fat intake predicts biochemical failure after prostatectomy. Int J Cancer 2008;122:2581-5. (Pubitemid 351590493)
11. Kolonel LN, Nomura AM, Cooney RV. Dietary fat and prostate cancer: current status. J Natl Cancer Inst 1999;91:414-28. (Pubitemid 29128277)
12. Yokomizo A, Shiota M, Kashiwagi E, Kuroiwa K, Tatsugami K, Inokuchi J, et al. Statins reduce the androgen sensitivity and cell proliferation by decreasing the androgen receptor protein in prostate cancer cells. Prostate 2011;71:298-304.
13. Solomon KR, Pelton K, Boucher K, Joo J, Tully C, Zurakowski D, et al. Ezetimibe is an inhibitor of tumor angiogenesis. Am J Pathol 2009;174:1017-26.
14. Murtola TJ, Visakorpi T, Lahtela J, Syvala H, Tammela T. Statins and prostate cancer prevention: where we are now, and future directions. Nat Clin Pract Urol 2008;5:376-87.
15. Shimano H. Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes. Prog Lipid Res 2001;40:439-52. (Pubitemid 32929966)
16. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997;89:331-40. (Pubitemid 27220877)
17. Jackson SM, Ericsson J, Metherall JE, Edwards PA. Role for sterol regulatory element binding protein in the regulation of farnesyl diphosphate synthase and in the control of cellular levels of cholesterol and triglyceride: evidence from sterol regulation-defective cells. J Lipid Res 1996;37:1712-21. (Pubitemid 26275382)
18. Wang X, Sato R, Brown MS, Hua X, Goldstein JL. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 1994;77:53-62.
19. Wang X, Briggs MR, Hua X, Yokoyama C, Goldstein JL, Brown MS. Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. II. Purification and characterization. J Biol Chem 1993;268:14497-504. (Pubitemid 23195581)
20. Briggs MR, Yokoyama C, Wang X, Brown MS, Goldstein JL. Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. I. Identification of the protein and delineation of its target nucleotide sequence. J Biol Chem 1993;268:14490-6. (Pubitemid 23195580)
21. Ericsson J, Jackson SM, Lee BC, Edwards PA. Sterol regulatory element binding protein binds to a cis element in the promoter of the farnesyl diphosphate synthase gene. Proc Natl Acad Sci U S A 1996;93:945-50. (Pubitemid 26041200)
22. Menendez JA, Decker JP, Lupu R. In support of fatty acid synthase (FAS) as a metabolic oncogene: extracellular acidosis acts in an epigenetic fashion activating FAS gene expression in cancer cells. J Cell Biochem 2005;94:1-4. (Pubitemid 41420319)
23. Ettinger SL, Sobel R, Whitmore TG, Akbari M, Bradley DR, Gleave ME, et al. Dysregulation of sterol response element-binding proteins and downstream effectors in prostate cancer during progression to androgen independence. Cancer Res 2004;64:2212-21. (Pubitemid 38339475)
24. Khandrika L, Kumar B, Koul S, Maroni P, Koul HK. Oxidative stress in prostate cancer. Cancer Lett 2009;282:125-36.
25. Clerkin JS, Naughton R, Quiney C, Cotter TG. Mechanisms of ROS modulated cell survival during carcinogenesis. Cancer Lett 2008;266:30-6.
26. Thalmann GN, Sikes RA, Wu TT, Degeorges A, Chang SM, Ozen M, et al. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis. Prostate 2000;44:91-103. (Pubitemid 30419183)
27. Huang WC, Havel JJ, Zhau HE, Qian WP, Lue HW, Chu CY, et al. {beta} 2-Microglobulin signaling blockade inhibited androgen receptor axis and caused apoptosis in human prostate cancer cells. Clin Cancer Res 2008;14:5341-7.
28. Wang H, Wang H, Xiong W, Chen Y, Ma Q, Ma J, et al. Evaluation on the phagocytosis of apoptotic spermatogenic cells by Sertoli cells in vitro through detecting lipid droplet formation by Oil Red O staining. Reproduction 2006;132:485-92.
29. Nomura T, Huang WC, Zhau HE, Wu D, Xie Z, Mimata H, et al. {beta}2-Microglobulin promotes the growth of human renal cell carcinoma through the activation of the protein kinase A, cyclic AMP-responsive element-binding protein, and vascular endothelial growth factor axis. Clin Cancer Res 2006;12:7294-305. (Pubitemid 46095401)
30. Huang WC, Xie Z, Konaka H, Sodek J, Zhau HE, Chung LW. Human osteocalcin and bone sialoprotein mediating osteomimicry of prostate cancer cells: role of cAMP-dependent protein kinase a signaling pathway. Cancer Res 2005;65:2303-13. (Pubitemid 40490140)
31. Magana MM, Osborne TF. Two tandem binding sites for sterol regulatory element binding proteins are required for sterol regulation of fatty-acid synthase promoter. J Biol Chem 1996;271:32689-94. (Pubitemid 27008692)
32. Baron A, Migita T, Tang D, Loda M. Fatty acid synthase: a metabolic oncogene in prostate cancer? J Cell Biochem 2004;91:47-53.
33. Lu JP, Monardo L, Bryskin I, Hou ZF, Trachtenberg J, Wilson BC, et al. Androgens induce oxidative stress and radiation resistance in prostate cancer cells though NADPH oxidase. Prostate Cancer Prostatic Dis 2010;13:39-46.
34. Kumar B, Koul S, Khandrika L, MeachamRB, Koul HK. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res 2008;68:1777-85. (Pubitemid 351416563)
35. Brar SS, Corbin Z, Kennedy TP, Hemendinger R, Thornton L, Bommarius B, et al. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am J Physiol Cell Physiol 2003;285:C353-69. (Pubitemid 36917850)
36. Li L, Ittmann MM, Ayala G, Tsai MJ, Amato RJ, Wheeler TM, et al. The emerging role of the PI3-K-Akt pathway in prostate cancer progression. Prostate Cancer Prostatic Dis 2005;8:108-18. (Pubitemid 43118073)
37. Shiota M, Yokomizo A, Tada Y, Inokuchi J, Kashiwagi E, Masubuchi D, et al. Castration resistance of prostate cancer cells caused by castration- induced oxidative stress through Twist1 and androgen receptor overexpression. Oncogene 2010;29:237-50.
38. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
39. Yamashita T, Honda M, Takatori H, Nishino R, Minato H, Takamura H, et al. Activation of lipogenic pathway correlates with cell proliferation and poor prognosis in hepatocellular carcinoma. J Hepatol 2009;50:100-10.
40. Swinnen JV, Brusselmans K, Verhoeven G. Increased lipogenesis in cancer cells: new players, novel targets. Curr Opin Clin Nutr Metab Care 2006;9:358-65. (Pubitemid 44101970)
41. Blanchetot C, Boonstra J. The ROS-NOX connection in cancer and angiogenesis. Crit Rev Eukaryot Gene Expr 2008;18:35-45. (Pubitemid 350259933)
42. Lim SD, Sun C, Lambeth JD, Marshall F, Amin M, Chung L, et al. Increased Nox1 and hydrogen peroxide in prostate cancer. Prostate 2005;62:200-7. (Pubitemid 40096784)
43. Sikka SC. Role of oxidative stress response elements and antioxidants in prostate cancer pathobiology and chemoprevention-a mechanistic approach. Curr Med Chem 2003;10:2679-92. (Pubitemid 37456038)
44. Okamoto M, Kawai K, Reznikoff CA, Oyasu R. Transformation in vitro of a nontumorigenic rat urothelial cell line by hydrogen peroxide. Cancer Res 1996;56:4649-53. (Pubitemid 26338065)
45. Dreher D, Junod AF. Role of oxygen free radicals in cancer development. Eur J Cancer 1996;32A:30-8.
46. Sauer H, Diedershagen H, Hescheler J, Wartenberg M. Calcium-dependence of hydrogen peroxide-induced c-fos expression and growth stimulation of multicellular prostate tumor spheroids. FEBS Lett 1997;419:201-5. (Pubitemid 28010810)
47. Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, et al. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci U S A 2004;101:16419-24. (Pubitemid 39557728)
48. Dong-Yun S, Yu-Ru D, Shan-Lin L, Ya-Dong Z, Lian W. Redox stress regulates cell proliferation and apoptosis of human hepatoma through Akt protein phosphorylation. FEBS Lett. 2003;542:60-4.