Prolonged exposure to (R)-bicalutamide generates a LNCaP subclone with alteration of mitochondrial genome

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 314-324

  Pignatta, Sara ^a   Arienti, Chiara ^a   Zoli, Wainer ^a   Di Donato, Marzia ^b   Castoria, Gabriella ^b   Gabucci, Elisa ^c   Casadio, Valentina ^a   Falconi, Mirella ^c   De Giorgi, Ugo ^a   Silvestrini, Rosella ^a   Tesei, Anna ^a  

^a DEPARTMENT OF MEDICAL ONCOLOGY   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

(R) bicalutamide; Hormone resistance; Mitochondrial fission; MtDNA; Prostate cancer

Indexed keywords

BICALUTAMIDE; DYNAMIN I; DYNAMIN RELATED PROTEIN 1; MITOCHONDRIAL DNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CONTROLLED STUDY; DNA CONTENT; DRUG EXPOSURE; DRUG MECHANISM; GENE MUTATION; GENETIC TRANSCRIPTION; HORMONAL THERAPY; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MALE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL GENOME; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; RESPIRATORY CHAIN;

(R)-BICALUTAMIDE; HORMONE-RESISTANCE; MITOCHONDRIAL FISSION; MTDNA; PROSTATE CANCER;

ANDROGENS; ANILIDES; ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; CLONE CELLS; COS CELLS; DNA, MITOCHONDRIAL; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, MITOCHONDRIAL; GTP PHOSPHOHYDROLASES; HUMANS; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; NITRILES; PROSTATIC NEOPLASMS; TOSYL COMPOUNDS; TRANSCRIPTION, GENETIC;

EID: 84887370435     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.10.022     Document Type: Article

References (64)

1. Abril J., de Heredia M.L., González L., Clèries R., Nadal M., Condom E., Aguiló F., Gómez-Zaera M., Nunes V. Altered expression of 12S/MT-RNR1, MT-CO2/COX2, and MT-ATP6 mitochondrial genes in prostate cancer. Prostate 2008, 68:1086-1096.
2. Albany C., Alva A.S., Aparicio A.M., Singal R., Yellapragada S., Sonpavde G., Hahn N.M. Epigenetics in prostate cancer. Prostate Cancer 2011, 2011:580318.
3. Amaral T.M., Macedo D., Fernandes I., Costa L. Castration-resistant prostate cancer: mechanisms, targets, and treatment. Prostate Cancer 2012, 2012:327253.
4. American Cancer Society, 2012. Cancer Facts & Figures 2012. American Cancer Society, Atlanta.
5. Arredouani M.S., Lu B., Bhasin M., Eljanne M., Yue W., Mosquera J.M., Bubley G.J., Li V., Rubin M.A., Libermann T.A., Sanda M.G. Identification of the transcription factor single-minded homologue 2 as a potential biomarker and immunotherapy target in prostate cancer. Clin. Cancer Res. 2009, 15:5794-5802.
6. Attard G., Sarker D., Reid A., Molife R., Parker C., de Bono J.S. Improving the outcome of patients with castration-resistant prostate cancer through rational drug development. Br. J. Cancer 2006, 95:767-774.
7. Barsoum M.J., Yuan H., Gerencser A.A., Liot G., Kushnareva Y., Gräber S., Kovacs I., Lee W.D., Waggoner J., Cui J., White A.D., Bossy B., Martinou J.C., Youle R.J., Lipton S.A., Ellisman M.H., Perkins G.A., Bossy-Wetzel E. Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 2006, 25:3900-3911.
8. Bossy-Wetzel E., Barsoum M.J., Godzik A., Schwarzenbacher R., Lipton S.A. Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr. Opin. Cell Biol. 2003, 15:706-716.
9. Castoria G., Lombardi M., Barone M.V., Bilancio A., Di Domenico M., Bottero D., Vitale F., Migliaccio A., Auricchio F. Androgen-stimulated DNA synthesis and cytoskeletal changes in fibroblasts by a nontranscriptional receptor action. J. Cell Biol. 2003, 161:547-556.
10. Castoria G., D'Amato L., Ciociola A., Giovannelli P., Giraldi T., Sepe L., Paolella G., Barone M.V., Migliaccio A., Auricchio F. Androgen-induced cell migration: role of androgen receptor/filamin A association. PLoS One 2011, 6:e17218.
11. Castoria G., Giovannelli P., Lombardi M., De Rosa C., Giraldi T., de Falco A., Barone M.V., Abbondanza C., Migliaccio A., Auricchio F. Tyrosine phosphorylation of estradiol receptor by Src regulates its hormone-dependent nuclear export and cell cycle progression in breast cancer cells. Oncogene 2012, 31:4868-4877.
12. Chan S.W., Chen J.Z. Measuring mtDNA damage using a supercoiling-sensitive qPCR approach. Methods Mol. Biol. 2009, 554:183-197.
13. Chang C.S., Kokontis J., Liao S.T. Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors. Proc. Natl. Acad. Sci. USA 1988, 85:7211-7215.
14. Chen J.Z., Gokden N., Greene G.F., Mukunyadzi P., Kadlubar F.F. Extensive somatic mitochondrial mutations in primary prostate cancer using laser capture microdissection. Cancer Res. 2002, 62:6470-6474.
15. Choudhary V., Kaddour-Djebbar I., Lakshmikanthan V., Ghazaly T., Thangjam G.S., Sreekumar A., Lewis R.W., Mills I.G., Bollag W.B., Kumar M.V. Novel role of androgens in mitochondrial fission and apoptosis. Mol. Cancer Res. 2011, 9:1067-1077.
16. Cook C.C., Kim A., Terao S., Gotoh A., Higuchi M. Consumption of oxygen: a mitochondrial-generated progression signal of advanced cancer. Cell Death Dis. 2012, 3:e258.
17. End D., Molina A., Todd M., Meyers M.L. Interactions of abiraterone, eplerenone, and prednisolone with wild-type and mutant androgen receptor: a rationale for increasing abiraterone exposure or combining with MDV3100. Cancer Res. 2013, 73:2926.
18. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 2001, 1:515-525.
19. Gnanapragasam V.J., Robson C.N., Leung H.Y., Neal D.E. Androgen receptor signalling in the prostate. BJU Int. 2000, 86:1001-1013.
20. Gottlieb B., Beitel L.K., Wu J.H., Trifiro M. The androgen receptor gene mutations database (ARDB): 2004 update. Hum. Mutat. 2004, 23:527-533.
21. Grasso C.S., Wu Y.M., Robinson D.R., Cao X., Dhanasekaran S.M., Khan A.P., Quist M.J., Jing X., Lonigro R.J., Brenner J.C., Asangani I.A., Ateeq B., Chun S.Y., Siddiqui J., Sam L., Anstett M., Mehra R., Prensner J.R., Palanisamy N., Ryslik G.A., Vandin F., Raphael B.J., Kunju L.P., Rhodes D.R., Pienta K.J., Chinnaiyan A.M., Tomlins S.A. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012, 487:239-243.
22. Han X.J., Tomizawa K., Fujimura A., Ohmori I., Nishiki T., Matsushita M., Matsui H. Regulation of mitochondrial dynamics and neurodegenerative diseases. Acta Med. Okayama 2011, 65:1-10.
23. Hara T., Miyazaki J., Araki H., Yamaoka M., Kanzaki N., Kusaka M., Miyamoto M. Novel mutations of androgen receptor: a possible mechanism of bicalutamide withdrawal syndrome. Cancer Res. 2003, 63:149-153.
24. Harris W.P., Mostaghel E.A., Nelson P.S., Montgomery B. Androgen deprivation therapy: progress in understanding mechanisms of resistance and optimizing androgen depletion. Nat. Clin. Pract. Urol. 2009, 6:76-85.
25. Hesson L.B., Cooper W.N., Latif F. The role of RASSF1A methylation in cancer. Dis. Markers 2007, 23:73-87.
26. Higuchi M. Regulation of mitochondrial DNA content and cancer. Mitochondrion 2007, 7:53-57.
27. Higuchi M., Kudo T., Suzuki S., Evans T.T., Sasaki R., Wada Y., Shirakawa T., Sawyer J.R., Gotoh A. Mitochondrial DNA determines androgen dependence in prostate cancer cell lines. Oncogene 2006, 25:1437-1445.
28. Holzbeierlein J., Lal P., LaTulippe E., Smith A., Satagopan J., Zhang L., Ryan C., Smith S., Scher H., Scardino P., Reuter V., Gerald W.L. Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance. Am. J. Pathol. 2004, 164:217-227.
29. Lamont K.R., Tindall D.J. Minireview: alternative activation pathways for the androgen receptor in prostate cancer. Mol. Endocrinol. 2011, 25:897-907.
30. Lapointe J., Li C., Higgins J.P., van de Rijn M., Bair E., Montgomery K., Ferrari M., Egevad L., Rayford W., Bergerheim U., Ekman P., DeMarzo A.M., Tibshirani R., Botstein D., Brown P.O., Brooks J.D., Pollack J.R. Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc. Natl. Acad. Sci. USA 2004, 101:811-816.
31. LaTulippe E., Satagopan J., Smith A., Scher H., Scardino P., Reuter V., Gerald W.L. Comprehensive gene expression analysis of prostate cancer reveals distinct transcriptional programs associated with metastatic disease. Cancer Res. 2002, 62:4499-4506.
32. Lee D.J., Cha E.K., Dubin J.M., Beltran H., Chromecki T.F., Fajkovic H., Scherr D.S., Tagawa S.T., Shariat S.F. Novel therapeutics for the management of castration-resistant prostate cancer (CRPC). BJU Int. 2012, 109:968-985.
33. Li Y., Chan S.C., Brand L.J., Hwang T.H., Silverstein K.A., Dehm S.M. Androgen receptor splice variants mediate enzalutamide resistance in castration-resistant prostate cancer cell lines. Cancer Res. 2013, 73:483-489.
34. Linja M.J., Visakorpi T. Alterations of androgen receptor in prostate cancer. J. Steroid Biochem. Mol. Biol. 2004, 92:255-264.
35. Liu P., Ramachandran S., Ali Seyed M., Scharer C.D., Laycock N., Dalton W.B., Williams H., Karanam S., Datta M.W., Jaye D.L., Moreno C.S. Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res. 2006, 66:4011-4019.
36. Luo J.H. Gene expression alterations in human prostate cancer. Drugs Today (Barc) 2002, 38:713-719.
37. Magee J.A., Araki T., Patil S., Ehrig T., True L., Humphrey P.A., Catalona W.J., Watson M.A., Milbrandt J. Expression profiling reveals hepsin overexpression in prostate cancer. Cancer Res. 2001, 61:5692-5696.
38. Marques R.B., Dits N.F., Erkens-Schulze S., van Weerden W.M., Jenster G. Bypass mechanisms of the androgen receptor pathway in therapy-resistant prostate cancer cell models. PLoS One 2010, 5:e13500.
39. Meiers I., Shanks J.H., Bostwick D.G. Glutathione S-transferase pi (GSTP1) hypermethylation in prostate cancer: review 2007. Pathology 2007, 39:299-304.
40. Osanto S., Van Poppel H. Emerging novel therapies for advanced prostate cancer. Ther. Adv. Urol. 2012, 4:3-12.
41. Petros J.A., Baumann A.K., Ruiz-Pesini E., Amin M.B., Sun C.Q., Hall J., Lim S., Issa M.M., Flanders W.D., Hosseini S.H., Marshall F.F., Wallace D.C. MtDNA mutations increase tumorigenicity in prostate cancer. Proc. Natl. Acad. Sci. USA 2005, 102:719-724.
42. Prince F.P. Mitochondrial cristae diversity in human Leydig cells: a revised look at cristae morphology in these steroid-producing cells. Anat. Rec. 1999, 254:534-541.
43. Rhodes D.R., Kalyana-Sundaram S., Mahavisno V., Varambally R., Yu J., Briggs B.B., Barrette T.R., Anstet M.J., Kincead-Beal C., Kulkarni P., Varambally S., Ghosh D., Chinnaiyan A.M. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 2007, 9:166-180.
44. Richards J., Lim A.C., Hay C.W., Taylor A.E., Wingate A., Nowakowska K., Pezaro C., Carreira S., Goodall J., Arlt W., McEwan I.J., de Bono J.S., Attard G. Interactions of abiraterone, eplerenone, and prednisolone with wild-type and mutant androgen receptor: a rationale for increasing abiraterone exposure or combining with MDV3100. Cancer Res. 2012, 72:2176-2182.
45. Scheller K., Sekeris C.E. The effects of steroid hormones on the transcription of genes encoding enzymes of oxidative phosphorylation. Exp. Physiol. 2003, 88:129-140.
46. Shi X.B., Ma A.H., Xia L., Kung H.J., de Vere White R.W. Functional analysis of 44 mutant androgen receptors from human prostate cancer. Cancer Res. 2002, 62:1496-1502.
47. Shutt T.E., Shadel G.S. A compendium of human mitochondrial gene expression machinery with links to disease. Environ. Mol. Mutagen. 2010, 51:360-379.
48. Simonnet H., Alazard N., Pfeiffer K., Gallou C., Béroud C., Demont J., Bouvier R., Schägger H., Godinot C. Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma. Carcinogenesis 2002, 23:759-768.
49. Singh D., Febbo P.G., Ross K., Jackson D.G., Manola J., Ladd C., Tamayo P., Renshaw A.A., D'Amico A.V., Richie J.P., Lander E.S., Loda M., Kantoff P.W., Golub T.R., Sellers W.R. Gene expression correlates of clinical prostate cancer behavior. Cancer Cell 2002, 1:203-209.
50. Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica D., Warren J.T., Bokesch H., Kenney S., Boyd M.R. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst. 1990, 82:1107-1112.
51. Taylor E.B., Rutter J. Mitochondrial quality control by the ubiquitin-proteasome system. Biochem. Soc. Trans. 2011, 39:1509-1513.
52. Taylor B.S., Schultz N., Hieronymus H., Gopalan A., Xiao Y., Carver B.S., Arora V.K., Kaushik P., Cerami E., Reva B., Antipin Y., Mitsiades N., Landers T., Dolgalev I., Major J.E., Wilson M., Socci N.D., Lash A.E., Heguy A., Eastham J.A., Scher H.I., Reuter V.E., Scardino P.T., Sander C., Sawyers C.L., Gerald W.L. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010, 18:11-22.
53. Tesei A., Leonetti C., Di Donato M., Gabucci E., Porru M., Varchi G., Guerrini A., Amadori D., Arienti C., Pignatta S., Paganelli G., Caraglia M., Castoria G., Zoli W. Effect of small molecules modulating androgen receptor (SARMs) in human prostate cancer models. PLoS One 2013, 8:e62657.
54. Tilley W.D., Buchanan G., Hickey T.E., Bentel J.M. Mutations in the androgen receptor gene are associated with progression of human prostate cancer to androgen independence. Clin. Cancer Res. 1996, 2:277-285.
55. Tomlins S.A., Mehra R., Rhodes D.R., Cao X., Wang L., Dhanasekaran S.M., Kalyana-Sundaram S., Wei J.T., Rubin M.A., Pienta K.J., Shah R.B., Chinnaiyan A.M. Integrative molecular concept modeling of prostate cancer progression. Nat. Genet. 2007, 39:41-51.
56. Vanaja D.K., Cheville J.C., Iturria S.J., Young C.Y. Transcriptional silencing of zinc finger protein 185 identified by expression profiling is associated with prostate cancer progression. Cancer Res. 2003, 63:3877-3882.
57. Varambally S., Yu J., Laxman B., Rhodes D.R., Mehra R., Tomlins S.A., Shah R.B., Chandran U., Monzon F.A., Becich M.J., Wei J.T., Pienta K.J., Ghosh D., Rubin M.A., Chinnaiyan A.M. Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 2005, 8:393-406.
58. Veldscholte J., Ris-Stalpers C., Kuiper G.G., Jenster G., Berrevoets C., Claassen E., van Rooij H.C., Trapman J., Brinkmann A.O., Mulder E. A mutation in the ligand binding domain of the androgen receptor of human LNCaP cells affects steroid binding characteristics and response to anti-androgens. Biochem. Biophys. Res. Commun. 1990, 173:534-540.
59. Verrijdt G., Schoenmakers E., Haelens A., Peeters B., Verhoeven G., Rombauts W., Claessens F. Change of specificity mutations in androgen-selective enhancers. Evidence for a role of differential DNA binding by the androgen receptor. J. Biol. Chem. 2000, 275:12298-12305.
60. Wallace T.A., Prueitt R.L., Yi M., Howe T.M., Gillespie J.W., Yfantis H.G., Stephens R.M., Caporaso N.E., Loffredo C.A., Ambs S. Tumor immunobiological differences in prostate cancer between African-American and European-American men. Cancer Res. 2008, 68:927-936.
61. Wang Y., Yu Q., Cho A.H., Rondeau G., Welsh J., Adamson E., Mercola D., McClelland M. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 2005, 7:748-760.
62. Welsh J.B., Sapinoso L.M., Su A.I., Kern S.G., Wang-Rodriguez J., Moskaluk C.A., Frierson H.F., Hampton G.M. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res. 2001, 61:5974-5978.
63. Wheater, P.R., Joung, B., Lowe, J.S., Stevens, A., Heath, J.W., 2007. Le ghiandole endocrine, Istologia e anatomia microscopica. Elsevier, Milan, Edizione V, pp. 328-346.
64. Yu Y.P., Landsittel D., Jing L., Nelson J., Ren B., Liu L., McDonald C., Thomas R., Dhir R., Finkelstein S., Michalopoulos G., Becich M., Luo J.H. Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J. Clin. Oncol. 2004, 22:2790-2799.