Differential regulation of metabolic pathways by androgen receptor (AR) and its constitutively active splice variant, AR-V7, in prostate cancer cells

Oncotarget

Volumn 6, Issue 31, 2015, Pages 31997-32012

  Shafi, Ayesha A ^a   Putluri, Vasanta ^a   Arnold, James M ^a   Tsouko, Efrosini ^b   Maity, Suman ^a   Roberts, Justin M ^a   Coarfa, Cristian ^a   Frigo, Daniel E ^b,c   Putluri, Nagireddy ^a   Sreekumar, Arun ^a   Weigel, Nancy L ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b University of Houston   (United States)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

Androgen receptor; LNCaP; Metabolism; Prostate cancer; Splice variant

Indexed keywords

ANDROGEN RECEPTOR; ANDROGEN RECEPTOR 7; GLUTAMATE DEHYDROGENASE; UNCLASSIFIED DRUG; AR PROTEIN, HUMAN; MESSENGER RNA;

AMINO ACID METABOLISM; ARTICLE; CARBOXYLATION; CARCINOGENESIS; CASTRATION RESISTANT PROSTATE CANCER; CELL GROWTH; CELL MIGRATION; CITRIC ACID CYCLE; CONTROLLED STUDY; FATTY ACID SYNTHESIS; GENE EXPRESSION; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LIPID STORAGE; MALE; METABOLIC REGULATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEADY STATE; ALTERNATIVE RNA SPLICING; APOPTOSIS; CELL MOTION; CELL PROLIFERATION; DRUG RESISTANCE; ENZYME IMMUNOASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METABOLOMICS; MIDDLE AGED; PATHOLOGY; PROSTATE TUMOR; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ALTERNATIVE SPLICING; APOPTOSIS; BLOTTING, WESTERN; CELL MOVEMENT; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MIDDLE AGED; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 84945535659     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5585     Document Type: Article

References (51)

1. Shafi AA, Yen AE, Weigel NL. Androgen receptors in hormone-dependent and castration-resistant prostate cancer. Pharmacol Ther 2013;140:223-38.
2. Koochekpour S. Androgen receptor signaling and mutations in prostate cancer. Asian Journal of Andrology 2010;12:639-57.
3. Gelmann EP. Molecular biology of the androgen receptor. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 2002;20:3001-15.
4. Nyquist MD, Dehm SM. Interplay between genomic alterations and androgen receptor signaling during prostate cancer development and progression. Horm Cancer 2013;4:61-9.
5. Sprenger CC, Plymate SR. The link between androgen receptor splice variants and castration-resistant prostate cancer. Horm Cancer 2014;5:207-17.
6. Guo Z, Yang X, Sun F, Jiang R, Linn DE, Chen H, Chen H, Kong X, Melamed J, Tepper CG, Kung HJ, Brodie AM, Edwards J, et al. A novel androgen receptor splice variant is up-regulated during prostate cancer progression and promotes androgen depletion-resistant growth. Cancer Res 2009;69:2305-13.
7. Hu R, Dunn TA, Wei S, Isharwal S, Veltri RW, Humphreys E, Han M, Partin AW, Vessella RL, Isaaca WB, Bova GS, Luo J. Ligand-independent androgen receptor variants derived from splicing of cryptic exons signify hormonerefractory prostate cancer. Cancer Res 2009;69:16-22.
8. Efstathiou E, Titus M, Wen S, Hoang A, Karlou M, Ashe R, Tu SM, Aparicio A, Troncoso P, Mohler J, Logothetis CJ. Molecular characterization of enzalutamide-treated bone metastatic castration-resistant prostate cancer. European Urology 2015;67:53-60.
9. Antonarakis ES, Lu C, Wang H, Luber B, Nakazawa M, Roeser JC, Chen Y, Mohammad TA, Chen Y, Fedor HL, Lotan TL, Zhen Q, De Marzo AM, et al. ARV7 and resistance to enzalutamide and abiraterone in prostate cancer. The New England Journal of Medicine 2014;371:1028-38.
10. Hu R, Lu C, Mostaghel EA, Yegnasubramanian S, Gurel M, Tannahill C, Edwards J, Isaacs WB, Nelson PS, Bluemn E, Plymate SR, Luo J. Distinct transcriptional programs mediated by the ligand-dependent full-length androgen receptor and its splice variants in castration-resistant prostate cancer. Cancer Res 2012;72:3457-62.
11. Krause WC, Shafi AA, Nakka M, Weigel NL. Androgen receptor and its splice variant, AR-V7, differentially regulate FOXA1 sensitive genes in LNCaP prostate cancer cells. Int J Biochem Cell Biol 2014;54:49-59.
12. Hu R, Isaacs WB, Luo J. A snapshot of the expression signature of androgen receptor splicing variants and their distinctive transcriptional activities. Prostate 2011;71:1656-67.
13. Massie CE, Lynch A, Ramos-Montoya A, Boren J, Stark R, Fazli L, Warren A, Scott H, Madhu B, Sharm N, Bon H, Zecchini V, Smith DM, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. The EMBO Journal 2011;30:2719-33.
14. Sharma NL, Massie CE, Ramos-Montoya A, Zecchini V, Scott HE, Lamb AD, MacArthur S, Stark R, Warren AY, Mills IG, Neal DE. The androgen receptor induces a distinct transcriptional program in castration-resistant prostate cancer in man. Cancer Cell 2013;23:35-47.
15. Barfeld SJ, Itkonen HM, Urbanucci A, Mills IG. Androgenregulated metabolism and biosynthesis in prostate cancer. Endocrine-Related Cancer 2014;21:T57-66.
16. Tennakoon JB, Shi Y, Han JJ, Tsouko E, White MA, Burns AR, Zhang A, Xia X, Ilkayeva OR, Xin L, Ittmann M, Rick FG, Schally AV, et al. Androgens regulate prostate cancer cell growth via an AMPK-PGC-1a-mediated metabolic switch. Oncogene 2014;33:5251-61.
17. Sreekumar A, Poisson LM, Rajendiran TM, Khan AP, Cao Q, Yu J, Laxman B, Mehra R, Lonigro RJ, Li Y, Nyati MK, Ahsan A, Kalyana-Sundaram S, et al. Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 2009;457:910-4.
18. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
19. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
20. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
21. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008;7:11-20.
22. Dakubo GD, Parr RL, Costello LC, Franklin RB, Thayer RE. Altered metabolism and mitochondrial genome in prostate cancer. J Clin Pathol 2006;59:10-6.
23. Ertel A, Tsirigos A, Whitaker-Menezes D, Birbe RC, Pavlides S, Martinez-Outschoorn UE, Pestell RG, Howell A, Sotgia F, Lisanti MP. Is cancer a metabolic rebellion against host aging? In the quest for immortality, tumor cells try to save themselves by boosting mitochondrial metabolism. Cell Cycle 2012;11:253-63.
24. Hensley CT, Wasti AT, DeBerardinis RJ. Glutamine and cancer: cell biology, physiology, and clinical opportunities. J Clin Invest 2013;123:3678-84.
25. Fuchs BC, Bode BP. Stressing out over survival: glutamine as an apoptotic modulator. J Surg Res 2006;131:26-40.
26. EAGLE H. The specific amino acid requirements of a human carcinoma cell (Stain HeLa) in tissue culture. J Exp Med 1955;102:37-48.
27. Wise DR, Thompson CB. Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci 2010;35:427-33.
28. DeBerardinis RJ, Cheng T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 2010;29:313-24.
29. Khan AP, Poisson LM, Bhat VB, Fermin D, Zhao R, Kalyana-Sundaram S, Michailidis G, Nesvizhskii AI, Omenn GS, Chinnaiyan AM, Sreekumar A. Quantitative proteomic profiling of prostate cancer reveals a role for miR-128 in prostate cancer. Mol Cell Proteomics 2010;9:298-312.
30. Putluri N, Shojaie A, Vasu VT, Nalluri S, Vareed SK, Putluri V, Vivekanandan-Giri A, Byun J, Pennathur S, Sana TR, Fischer SM, Palapattu GS, Creighton CJ, et al. Metabolomic profiling reveals a role for androgen in activating amino acid metabolism and methylation in prostate cancer cells. PLoS ONE 2011;6:e21417.
31. Koike K, Urata Y, Goto S. Cloning and nucleotide sequence of the cDNA encoding human 2-oxoglutarate dehydrogenase (lipoamide). Proc Natl Acad Sci USA 1992;89:1963-7.
32. Lindbladh C, Rault M, Hagglund C, Small WC, Mosbach K, Bülow L, Evans C, Srere PA. Preparation and kinetic characterization of a fusion protein of yeast mitochondrial citrate synthase and malate dehydrogenase. Biochemistry 1994;33:11692-8.
33. Deberardinis RJ, Sayed N, Ditsworth D, Thompson CB. Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 2008;18:54-61.
34. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 2007;104:19345-50.
35. Brand K. Glutamine and glucose metabolism during thymocyte proliferation. Pathways of glutamine and glutamate metabolism. Biochem J 1985;228:353-61.
36. Michaelidis TM, Tzimagiorgis G, Moschonas NK, Papamatheakis J. The human glutamate dehydrogenase gene family: gene organization and structural characterization. Genomics 1993;16:150-60.
37. Zha S, Ferdinandusse S, Hicks JL, Denis S, Dunn TA, Wanders RJ, Luo J, De Marzo AM, Isaacs WB. Peroxisomal branched chain fatty acid beta-oxidation pathway is upregulated in prostate cancer. Prostate 2005;63:316-23.
38. Oyama N, Miller TR, Dehdashti F, Siegel BA, Fischer KC, Michalski JM, Kibel AS, Andriole GL, Picus J, Welch MJ. 11C-acetate PET imaging of prostate cancer: detection of recurrent disease at PSA relapse. J Nucl Med 2003;44:549-55.
39. Swinnen JV, Veldhoven PP Van, Esquenet M, Heyns W, Verhoeven G. Androgens markedly stimulate the accumulation of neutral lipids in the human prostatic adenocarcinoma cell line LNCaP. Endocrinology 1996;137:4468-74.
40. Swinnen JV, Esquenet M, Goossens K, Heyns W, Verhoeven G. Androgens stimulate fatty acid synthase in the human prostate cancer cell line LNCaP. Cancer Research 1997;57:1086-90.
41. Saha AK, Ruderman NB. Malonyl-CoA and AMP-activated protein kinase: an expanding partnership. Mol Cell Biochem 2003;253:65-70.
42. Martin DB, Vagelos PR. The mechanism of tricarboxylic acid cycle regulation of fatty acid synthesis. The Journal of Biological Chemistry 1962;237:1787-92.
43. Zhang X, Morrissey C, Sun S, Ketchandji M, Nelson PS, True LD, Vakar-Lopez F, Vessella RL, Plymate SR. Androgen receptor variants occur frequently in castration resistant prostate cancer metastases. PloS One 2011;6:e27970.
44. Hörnberg E, Ylitalo EB, Crnalic S, Antti H, Stattin P, Widmark A, Bergh A, Wikström P. Expression of androgen receptor splice variants in prostate cancer bone metastases is associated with castration-resistance and short survival. PloS One 2011;6:e19059.
45. Jacque N, Ronchetti AM, Larrue C, Meunier G, Birsen R, Willems L, Saland E,Decroocq J, Trovati Maciel T, Lambert M, Poulain L, Hospital MA, Sujobert P, et al. Targeting glutaminolysis has anti-leukemic activity in acute myeloid leukemia and synergizes with BCL-2 inhibition. Blood 2015; 126:1346-56.
46. Gross MI, Demo SD, Dennison JB, Chen L, ChernovRogan T, Goyal B, Janes JR, Laidig GJ, Lewis ER, Li J, Mackinnon AL, Parlati F, Rodriguez ML, et al. Antitumor activity of the glutaminase inhibitor CB-839 in triplenegative breast cancer. Mol Cancer Ther 2014;13:890-901.
47. Agoulnik IU, Vaid A, Nakka M, Alvarado M, Bingman WE, Erdem H, Frolov A, Smith CL, Ayala GE, Ittmann MM, Weigel NL. Androgens modulate expression of transcription intermediary factor 2, an androgen receptor coactivator whose expression level correlates with early biochemical recurrence in prostate cancer. Cancer Research 2006;66:10594-602.
48. Nazareth LV, Weigel NL. Activation of the human androgen receptor through a protein kinase A signaling pathway. The Journal of Biological Chemistry 1996;271:19900-7.
49. Shafi AA, Cox MB, Weigel NL. Androgen receptor splice variants are resistant to inhibitors of Hsp90 and FKBP52, which alter androgen receptor activity and expression. Steroids 2013;78:548-54.
50. Kim J-SS, Roberts JM, Bingman WE, Shao L, Wang J, Ittmann MM, Weigel NL. The prostate cancer TMPRSS2:ERG fusion synergizes with the vitamin D receptor (VDR) to induce CYP24A1 expression-limiting VDR signaling. Endocrinology 2014;155:3262-73.
51. Stashi E, Lanz RB, Mao J, Michailidis G, Zhu B, Kettner NM, Putluri N, Reineke EL, Reineke LC, Dasgupta S, Dean A, Stevenson CR, Sivasubramanian N, et al. SRC-2 is an essential coactivator for orchestrating metabolism and circadian rhythm. Cell Reports 2014;6:633-45.