SREBP-2 promotes stem cell-like properties and metastasis by transcriptional activation of c-Myc in prostate cancer

Oncotarget

Volumn 7, Issue 11, 2016, Pages 12869-12884

  Li, Xiangyan ^a   Wu, Jason Boyang ^a   Li, Qinlong ^a,b   Shigemura, Katsumi ^c   Chung, Leland W K ^a   Huang, Wen Chin ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

c Myc; Metastasis; Prostate cancer; SREBP 2; Stemness

Indexed keywords

MYC PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; MYC PROTEIN, HUMAN; SREBF2 PROTEIN, HUMAN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CELL INVASION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE SILENCING; HUMAN; MALE; METASTASIS; MOUSE; NONHUMAN; ONCOGENE C MYC; OUTCOME ASSESSMENT; PHENOTYPE; PROMOTER REGION; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; STEM CELL; TRANSCRIPTION INITIATION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; BIOSYNTHESIS; CANCER STEM CELL; CELL MOTION; DISEASE FREE SURVIVAL; DRUG SCREENING; GENE EXPRESSION REGULATION; METABOLISM; MIDDLE AGED; MORTALITY; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; SCID MOUSE; TUMOR INVASION;

ADULT; AGED; ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; DISEASE-FREE SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRANSCRIPTIONAL ACTIVATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962909443     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7331     Document Type: Article

References (44)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2013. CA. 2013; 63:11-30.
2. Hurt EM, Kawasaki BT, Klarmann GJ, Thomas SB and Farrar WL. CD44+ CD24(-) prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br J Cancer. 2008; 98:756-765.
3. Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, Calhoun-Davis T, Li H, Palapattu GS, Pang S, Lin K, Huang J, Ivanov I, Li W, Suraneni MV and Tang DG. The PSA(-/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell. 2012; 10:556-569.
4. Domingo-Domenech J, Vidal SJ, Rodriguez-Bravo V, Castillo-Martin M, Quinn SA, Rodriguez-Barrueco R, Bonal DM, Charytonowicz E, Gladoun N, de la Iglesia-Vicente J, Petrylak DP, Benson MC, Silva JM and Cordon-Cardo C. Suppression of acquired docetaxel resistance in prostate cancer through depletion of notch-and hedgehog-dependent tumor-initiating cells. Cancer Cell. 2012; 22:373-388.
5. Dubrovska A, Kim S, Salamone RJ, Walker JR, Maira SM, Garcia-Echeverria C, Schultz PG and Reddy VA. The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci U S A. 2009; 106:268-273.
6. Zhou Z, Flesken-Nikitin A and Nikitin AY. Prostate cancer associated with p53 and Rb deficiency arises from the stem/progenitor cell-enriched proximal region of prostatic ducts. Cancer Res. 2007; 67:5683-5690.
7. Rajasekhar VK, Studer L, Gerald W, Socci ND and Scher HI. Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-kappaB signalling. Nat Commun. 2011; 2:162.
8. Gurel B, Iwata T, Koh CM, Jenkins RB, Lan F, Van Dang C, Hicks JL, Morgan J, Cornish TC, Sutcliffe S, Isaacs WB, Luo J and De Marzo AM. Nuclear MYC protein overexpression is an early alteration in human prostate carcinogenesis. Mod Pathol. 2008; 21:1156-1167.
9. Li T, Su Y, Mei Y, Leng Q, Leng B, Liu Z, Stass SA and Jiang F. ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Laboratory investigation; a journal of technical methods and pathology. 2010; 90:234-244.
10. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly JG, Chandra D, Zhou J, Claypool K, Coghlan L and Tang DG. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene. 2006; 25:1696-1708.
11. Jeter CR, Liu B, Liu X, Chen X, Liu C, Calhoun-Davis T, Repass J, Zaehres H, Shen JJ and Tang DG. NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene. 2011; 30:3833-3845.
12. Rybak AP and Tang D. SOX2 plays a critical role in EGFR-mediated self-renewal of human prostate cancer stem-like cells. Cell Signal. 2013; 25:2734-2742.
13. Taylor RA, Toivanen R and Risbridger GP. Stem cells in prostate cancer: treating the root of the problem. Endocrine-related cancer. 2010; 17:R273-285.
14. Chen X, Rycaj K, Liu X and Tang DG. New insights into prostate cancer stem cells. Cell cycle. 2013; 12:579-586.
15. Amemiya-Kudo M, Shimano H, Hasty AH, Yahagi N, Yoshikawa T, Matsuzaka T, Okazaki H, Tamura Y, Iizuka Y, Ohashi K, Osuga J, Harada K, Gotoda T, Sato R, Kimura S, Ishibashi S, et al. Transcriptional activities of nuclear SREBP-1a,-1c, and-2 to different target promoters of lipogenic and cholesterogenic genes. J Lipid Res. 2002; 43:1220-1235.
16. Shimano H. Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes. Prog Lipid Res. 2001; 40:439-452.
17. Brown MS and Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 1997; 89:331-340.
18. Ettinger SL, Sobel R, Whitmore TG, Akbari M, Bradley DR, Gleave ME and Nelson CC. Dysregulation of sterol response element-binding proteins and downstream effectors in prostate cancer during progression to androgen independence. Cancer Res. 2004; 64:2212-2221.
19. Huang WC, Li X, Liu J, Lin J and Chung LW. Activation of androgen receptor, lipogenesis, and oxidative stress converged by SREBP-1 is responsible for regulating growth and progression of prostate cancer cells. Mol Cancer Res. 2012; 10:133-142.
20. Shin G, Kang TW, Yang S, Baek SJ, Jeong YS and Kim SY. GENT: gene expression database of normal and tumor tissues. Cancer Inform. 2011; 10:149-157.
21. Li H and Tang DG. Prostate cancer stem cells and their potential roles in metastasis. Journal of surgical oncology. 2011; 103:558-562.
22. Ni J, Cozzi P, Hao J, Duan W, Graham P, Kearsley J and Li Y. Cancer stem cells in prostate cancer chemoresistance. Current cancer drug targets. 2014; 14:225-240.
23. Krycer JR, Sharpe LJ, Luu W and Brown AJ. The Akt-SREBP nexus: cell signaling meets lipid metabolism. Trends Endocrinol Metab. 2010; 21:268-276.
24. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, Griffiths JR, Chung YL and Schulze A. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab. 2008; 8:224-236.
25. Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA, Balderas E, Guertin DA, Madden KL, Carpenter AE, Finck BN and Sabatini DM. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell. 2011; 146:408-420.
26. Freed-Pastor WA, Mizuno H, Zhao X, Langerod A, Moon SH, Rodriguez-Barrueco R, Barsotti A, Chicas A, Li W, Polotskaia A, Bissell MJ, Osborne TF, Tian B, Lowe SW, Silva JM, Borresen-Dale AL, et al. Mutant p53 disrupts mammary tissue architecture via the mevalonate pathway. Cell. 2012; 148:244-258.
27. Sorrentino G, Ruggeri N, Specchia V, Cordenonsi M, Mano M, Dupont S, Manfrin A, Ingallina E, Sommaggio R, Piazza S, Rosato A, Piccolo S and Del Sal G. Metabolic control of YAP and TAZ by the mevalonate pathway. Nat Cell Biol. 2014; 16:357-366.
28. van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Lippitt JM, Guzman-Ramirez N, Hamdy FC, Eaton CL, Thalmann GN, Cecchini MG, Pelger RC and van der Pluijm G. High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res. 2010; 70:5163-5173.
29. Vita M and Henriksson M. The Myc oncoprotein as a therapeutic target for human cancer. Semin Cancer Biol. 2006; 16:318-330.
30. Ellwood-Yen K, Graeber TG, Wongvipat J, Iruela-Arispe ML, Zhang J, Matusik R, Thomas GV and Sawyers CL. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell. 2003; 4:223-238.
31. Hawksworth D, Ravindranath L, Chen Y, Furusato B, Sesterhenn IA, McLeod DG, Srivastava S and Petrovics G. Overexpression of C-MYC oncogene in prostate cancer predicts biochemical recurrence. Prostate Cancer Prostatic Dis. 2010; 13:311-315.
32. Bernard D, Pourtier-Manzanedo A, Gil J and Beach DH. Myc confers androgen-independent prostate cancer cell growth. J Clin Invest. 2003; 112:1724-1731.
33. Civenni G, Malek A, Albino D, Garcia-Escudero R, Napoli S, Di Marco S, Pinton S, Sarti M, Carbone GM and Catapano CV. RNAi-mediated silencing of Myc transcription inhibits stem-like cell maintenance and tumorigenicity in prostate cancer. Cancer Res. 2013; 73:6816-6827.
34. Zhau HE, Odero-Marah V, Lue HW, Nomura T, Wang R, Chu G, Liu ZR, Zhou BP, Huang WC and Chung LW. Epithelial to mesenchymal transition (EMT) in human prostate cancer: lessons learned from ARCaP model. Clinical & experimental metastasis. 2008; 25:601-610.
35. Ginestier C, Monville F, Wicinski J, Cabaud O, Cervera N, Josselin E, Finetti P, Guille A, Larderet G, Viens P, Sebti S, Bertucci F, Birnbaum D and Charafe-Jauffret E. Mevalonate metabolism regulates Basal breast cancer stem cells and is a potential therapeutic target. Stem Cells. 2012; 30:1327-1337.
36. Thalmann GN, Sikes RA, Wu TT, Degeorges A, Chang SM, Ozen M, Pathak S and Chung LW. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis. Prostate. 2000; 44(2):91-103 Jul 101;144.
37. Xu J, Wang R, Xie ZH, Odero-Marah V, Pathak S, Multani A, Chung LW and Zhau HE. Prostate cancer metastasis: role of the host microenvironment in promoting epithelial to mesenchymal transition and increased bone and adrenal gland metastasis. Prostate. 2006; 66:1664-1673.
38. Craft N, Chhor C, Tran C, Belldegrun A, DeKernion J, Witte ON, Said J, Reiter RE and Sawyers CL. Evidence for clonal outgrowth of androgen-independent prostate cancer cells from androgen-dependent tumors through a two-step process. Cancer Res. 1999; 59:5030-5036.
39. Li X, Chen YT, Josson S, Mukhopadhyay NK, Kim J, Freeman MR and Huang WC. MicroRNA-185 and 342 Inhibit Tumorigenicity and Induce Apoptosis through Blockade of the SREBP Metabolic Pathway in Prostate Cancer Cells. PLoS One. 2013; 8:e70987.
40. Li X, Chen YT, Hu P and Huang WC. Fatostatin displays high antitumor activity in prostate cancer by blocking SREBP-regulated metabolic pathways and androgen receptor signaling. Mol Cancer Ther. 2014; 13:855-866.
41. Huang WC, Zhau HE and Chung LW. Androgen receptor survival signaling is blocked by anti-beta2-microglobulin monoclonal antibody via a MAPK/lipogenic pathway in human prostate cancer cells. J Biol Chem. 2010; 285:7947-7956.
42. Kuser-Abali G, Alptekin A and Cinar B. Overexpression of MYC and EZH2 cooperates to epigenetically silence MST1 expression. Epigenetics. 2014; 9:634-643.
43. Prensner JR, Iyer MK, Sahu A, Asangani IA, Cao Q, Patel L, Vergara IA, Davicioni E, Erho N, Ghadessi M, Jenkins RB, Triche TJ, Malik R, Bedenis R, McGregor N, Ma T, et al. The long noncoding RNA SChLAP1 promotes aggressive prostate cancer and antagonizes the SWI/SNF complex. Nat Genet. 2013; 45:1392-1398.
44. Li X, Wu JB, Chung LW and Huang WC. Anti-cancer efficacy of SREBP inhibitor, alone or in combination with docetaxel, in prostate cancer harboring p53 mutations. Oncotarget. 2015; 6:41018-41032. doi: 10.18632/oncotarget.5879.