Adaptive auto-regulation of androgen receptor provides a paradigm shifting rationale for bipolar androgen therapy (BAT) for castrate resistant human prostate cancer

Prostate

Volumn 72, Issue 14, 2012, Pages 1491-1505

  Isaacs, John T ^a,b   D'Antonio, Jason M ^a,b,c   Chen, Shuangling ^a   Antony, Lizamma ^a   Dalrymple, Susan P ^a   Ndikuyeze, Georges H ^a   Luo, Jun ^b   Denmeade, Samuel R ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AMERICAN UNIVERSITY   (United States)

Author keywords

androgen receptor; bipolar androgen therapy; Cdc6; Cdt1; DNA Licensing; Mcm; Orc; origin of replication; prostate cancer

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR;

ANDROGEN THERAPY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANDROGEN THERAPY; ARTICLE; CASTRATION; CASTRATION RESISTANT PROSTATE CANCER; CELL CULTURE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL SYNCHRONIZATION; CLINICAL ARTICLE; CONTROLLED STUDY; DNA REPLICATION ORIGIN; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; XENOGRAFT;

ANDROGEN ANTAGONISTS; ANDROGENS; ANILIDES; ANIMALS; CELL CYCLE; CELL DEATH; CELL LINE, TUMOR; DNA REPLICATION; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; METRIBOLONE; MICE; NEOPLASMS, HORMONE-DEPENDENT; NITRILES; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; TESTOSTERONE; TOSYL COMPOUNDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84865498990     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.22504     Document Type: Article

References (45)

1. Litvinov IV, De Marzo AM, Isaacs JT,. Is the Achilles' heel for prostate cancer therapy a gain of function in androgen receptor signaling? J Clin Endocrinol Metab 2003; 88: 2972-2982. (Pubitemid 36877458)
2. Vander Griend DJ, Litvinov I, Isaacs JT,. Androgen Receptor (AR) suppresses human prostate epithelial cell proliferation via AR/β-Catenin/ TCF-4 complex inhibition of c-Myc transcription. PLos-one 2012 (in press).
3. Bono JS, Logothetis CJ, Molina A, Fizazi K, North S, Chu L, Chi KN, Jones RJ, Goodman OB Jr, Saad F, Staffurth JN, Mainwaring P, Harland S, Flaig TW, Hutson TE, Cheng T, Patterson H, Hainsworth JD, Ryan CJ, Steinberg CN, Ellard SL, Fléchon A, Saleh M, Scholz M, Efstathiou E, Zivi A, Bianchini D, Loriot Y, Chieffo N, Kheoh T, Haqq CM, Scher HI, COU-AA-301 Investigators. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 2011; 364: 1995-2005.
4. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R, Rosenfeld MG, Sawyers CL,. Molecular determinants of resistance to antiandrogen therapy. Nat Med 2004; 10: 33-39. (Pubitemid 38524696)
5. Shah RB, Mehra R, Chinnaiyan AM, Shen R, Ghosh D, Zhou M, Macvicar GR, Varambally S, Harwood J, Bismar TA, Kim R, Rubin MA, Pienta KJ,. Androgen-independent prostate cancer is a heterogeneous group of diseases: Lessons from a rapid autopsy program. Cancer Res 2004; 64: 9209-9216. (Pubitemid 39665537)
6. Vander Griend DJ, D'Antonio J, Gurel B, Antony L, Demarzo AM, Isaacs JT,. Cell-autonomous intracellular androgen receptor signaling drives the growth of human prostate cancer initiating cells. Prostate 2010; 70: 90-99.
7. Zegarra-Moro OL, Schmidt LJ, Huang H, Tindall DJ,. Disruption of androgen receptor function inhibits proliferation of androgen-refractory prostate cancer cells. Cancer Res 2002; 62: 1008-1013. (Pubitemid 34160279)
8. Li TH, Zhao H, Peng Y, Beliakoff J, Brooks JD, Sun Z,. A promoting role of androgen receptor in androgen-sensitive and -insensitive prostate cancer cells. Nucleic Acids Res 2007; 35: 2767-2776. (Pubitemid 47073687)
9. Dehm SM, Schmidt LJ, Heemers HV, Vessella RL, Tindall DJ,. Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res 2008; 68: 5469-5477.
10. Snoek R, Cheng H, Margiotti K, Wafa LA, Wong CA, Wong EC, Fazli L, Nelson CC, Gleave ME, Rennie PS,. In vivo knockdown of the androgen receptor results in growth inhibition and regression of well-established, castration-resistant prostate tumors. Clin Cancer Res 2009; 15: 39-47.
11. Litvinov IV, Vander Griend DJ, Antony L, Dalrymple S, De Marzo AM, Drake CG, Isaacs JT,. Androgen receptor as a licensing factor for DNA replication in androgen-sensitive prostate cancer cells. Proc Natl Acad Sci U S A 2006; 103: 15085-15090. (Pubitemid 44583168)
12. Vander Griend DJ, Litvinov IV, Isaacs JT,. Stabilizing androgen receptor in mitosis inhibits prostate cancer proliferation. Cell Cycle 2007; 6: 647-651. (Pubitemid 46535673)
13. D'Antonio J, Vander Griend D, Isaacs J,. DNA licensing as a novel androgen receptor mediated therapeutic target for prostate cancer. Endocr Relat Cancer 2009; 16: 325-332.
14. Bell SP, Dutta A,. DNA replication in eukaryotic cells. Annu Rev Biochem 2002; 71: 333-374. (Pubitemid 34800224)
15. Tabancay AP, Forsburg SL,. Eukaryotic DNA replication in a chromatin context. Curr Top Dev Biol 2006; 76: 129-184. (Pubitemid 44760541)
16. Siddiqui K, Stillman B,. ATP-dependent assembly of human origin recognition complex. J Biol Chem 2007; 282: 32370-32383. (Pubitemid 350106415)
17. Blow JJ, Dutta A,. Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 2005; 6: 476-486. (Pubitemid 40780559)
18. Arias EE, Walter JC,. Strength in numbers: Preventing re-replication via multiple mechanisms in eukaryotic cells. Genes Dev 2007; 21: 497-518. (Pubitemid 46409465)
19. Mailand N, Diffley JF,. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 2005; 122: 915-926. (Pubitemid 41345208)
20. Fujita M,. Cdtlrevisited: Complex and tight regulation during the cell cycle and consequences of deregulation in mammalian cells. Cell Div 2006; 1: 22.
21. Bai VU, Cifuentes E, Menon M, Barrack ER, Reddy GP,. Androgen receptor regulates Cdc6 in synchronized LNCaP cells progressing from Gl to S phase. J Cell Physiol 2005; 204: 381-387. (Pubitemid 40934630)
22. Kemppainen JA, Lane MV, Sar M, Wilson EM,. Androgen receptor phosphorylation, turnover, nuclear transport, and transcriptional activation. Specificity for steroids and antihormones. J Biol Chem 1992; 267: 968-974.
23. Vander Gnend DJ, Karthaus WL, Dalrymple S, Meeker A, DeMarzo AM, Isaacs JT,. The role of CD133 in normal human prostate stem cells and malignant cancer-initiating cells. Cancer Res 2008; 68: 9703-9711.
24. D'Antonio JM, Vander Griend DJ, Antony L, Ndikuyeze G, Dalrymple SL, Koochekpour S, Isaacs JT,. Loss of androgen receptor-dependent growth suppression by prostate cancer cells can occur independently from acquiring oncogenic addiction to androgen receptor signaling. PLoS ONE 2010; 5: el1475.
25. Gao J, Arnold JT, Isaacs JT,. Conversion from a paracrine to an autocrine mechanism of androgen-stimulated growth during malignant transformation of prostatic epithelial cells. Cancer Res 2001; 61: 5038-5044. (Pubitemid 32681532)
26. Uzgare AR, Isaacs JT,. Enhanced redundancy in Akt and mitogen-activated protein kinase-induced survival of malignant versus normal prostate epithelial cells. Cancer Res 2004; 64: 6190-6199. (Pubitemid 39129421)
27. Prakash K, Pirozzi G, Elashoff M, Munger W, Waga I, Dhir R, Kakehi Y, Getzenberg RH,. Symptomatic and asymptomatic benign prostatic hyperplasia: Molecular differentiation by using microarrays. Proc Natl Acad Sci USA 2002; 99: 7598-7603. (Pubitemid 34568737)
28. Bova GS, Fox WM, Epstein JI,. Methods of radical prostatectomy specimen processing: A novel technique for harvesting fresh prostate cancer tissue and review of processing techniques. Mod Pathol 1993; 6: 201-207.
29. Liu W, Laitinen S, Vihinen M, Kowalski J, Yu G, Chen L, Ewing CM, Eisenberger MA, Carducci MA, Nelson WG, Yegnasubramanian S, Luo J, Wang Y, Xu J, Isaacs WB, Visakorpi T, Bova GS,. Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat Med 2009; 15: 559-565.
30. Dunn TA, Chen S, Faith DA, Hicks JL, Platz EA, Chen Y, Ewing CM, Sauvageot J, Isaacs WB, De Marzo AM, Luo J,. A novel role of myosin VI in human prostate cancer. Am J Pathol 2006; 169: 1843-1854. (Pubitemid 351182013)
31. Litvinov I, Antony L, Dalrymple SL, Becker R, Cheng L, Isaacs JT,. PC-3, but not DU145, human prostate cancer cells retain the coregulators required for rumor suppressor ability of androgen receptor. Prostate 2006; 66: 1329-1338. (Pubitemid 44384309)
32. Fujita M, Ishimi Y, Nakamura H, Kiyono T, Tsurumi T,. Nuclear organization of DNA replication initiation proteins in mammalian cells. J Biol Chem 2002; 277: 10354-10361. (Pubitemid 34968153)
33. Cifuentes E, Croxen R, Menon M, Barrack ER, Reddy GP,. Synchronized prostate cancer cells for studying androgen regulated events in cell cycle progression from Gl into S phase. J Cell Physiol 2003; 195: 337-345. (Pubitemid 36529862)
34. Hoehn W, Schroeder FH, Reimann JF, Joebsis AC, Hermanek P,. Human prostatic adenocarcinoma: Some characteristics of a serially transplantable line in nude mice (PC82). Prostate 1980; 1: 95-104. (Pubitemid 11016689)
35. Wainstein MA, He F, Robinson D, Kung HJ, Schwartz S, Giaconia JM, Edgehouse NL, Pretlow TP, Bodner DR, Kursh ED,. CWR22: Androgen-dependent xenograft model derived from a primary human prostatic carcinoma. Cancer Res 1994; 54: 6049-6052. (Pubitemid 24378626)
36. Koochekpour S, Maresh GA, Katner A, Parker-Johnson K, Lee TJ, Hebert FE, Kao YS, Skinner J, Rayford W,. Establishment and characterization of a primary androgen-responsive African-American prostate cancer cell line, E006AA. Prostate 2004; 60: 141-152. (Pubitemid 38758579)
37. Troyer DA, Tang Y, Bedolla R, Adhvaryu SG, Thompson IM, Abboud-Werner S, Sun LZ, Friedrichs WE, deGraffenried LA,. Characterization of PacMetUTl, a recently isolated human prostate cancer cell line. Prostate 2008; 68: 883-892. (Pubitemid 351845219)
38. Koivisto P, Kononen J, Palmberg C, Tammela T, Hyytinen E, Isola J, Trapman J, Cleutjens K, Noordzij A, Visakorpi T, Kallioniemi OP,. Androgen receptor gene amplification: A possible molecular mechanism for androgen deprivation therapy failure in prostate cancer. Cancer Res 1997; 57: 314-319. (Pubitemid 27036612)
39. Sedelaar JP, Isaacs JT,. Tissue culture media supplemented with 10% fetal calf bovine serum contains a castrate level of testosterone. Prostate 2009; 69: 1724-1729.
40. Berges RR, Vukanovic J, Epstein JL, CarMichel M, Cisek L, Johnson De, Veltri RW, Walsh PC, Isaacs JT,. Implication of cell kinetic changes during the progression of human prostatic cancer. Clin Cancer Res 1995; 1: 473-480.
41. Gerdes J, Becker MH, Key G, Cattoretti G,. Immunohistogical detection of tumour growth fraction (Ki-67 antigen) in formalin-fixed and routinely processed tissues. J Pathol 1992; 168: 85-86.
42. Delmolino LM, Saha P, Dutta A,. Multiple mechanisms regulate subcellular localization of human CDC6. J Biol Chem 2001; 276: 26947-26954.
43. Tatsumi Y, Ohta S, Kimura H, Tsurimoto T, Obuse C,. The ORC1 cycle in human cells I. Cell cycle-regulated oscillation on human ORC1. J Biol Chem 2003; 278: 41528-41534. (Pubitemid 37280982)
44. Hateboer, Wobst A, Otzen Petersen B, Le Cam L, Vigo E, Sardet C, Helin K,. Cell cycle-regulated expression of mammalian CDC6 is dependent on E2F. Mol Cell Biol 1998; 18: 6679-6697. (Pubitemid 28500556)
45. Haffner MC, Aryree MJ, Toubaji A, Esopi DM, Albadine R, Gurel B, Isaacs WB, Bova GS, Liu W, Xu J, Meeker AK, Netto G, De Marzo AM, Nelson WG, Yegnasurbramanian S,. Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet 2010; 42: 668-675.