Androgen Deprivation-Induced Senescence Promotes Outgrowth of Androgen-Refractory Prostate Cancer Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Burton, Dominick G A ^a   Giribaldi, Maria G ^a,b   Munoz, Anisleidys ^a,b   Halvorsen, Katherine ^a   Patel, Asmita ^a   Jorda, Merce ^a   Perez Stable, Carlos ^a,c,d   Rai, Priyamvada ^a,d  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Miami   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUTLIN 3; PROTEIN BAX; PROTEIN P53;

ANDROGEN DEPRIVATION THERAPY; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER RESISTANCE; CARCINOGENESIS; CELL CLONING; CELL DEATH; CELL POPULATION; CELL STIMULATION; CELL STRAIN LAPC4; CELL STRAIN LNCAP; CELL SURVIVAL; CELLULAR SENESCENCE; DRUG RESISTANCE; PHENOTYPE; PROSTATE CANCER; SENESCENCE; TREATMENT RESPONSE;

ANDROGENS; BCL-2-ASSOCIATED X PROTEIN; CELL AGING; CELL DEATH; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; PROSTATIC NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84879526156     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068003     Document Type: Article

References (89)

1. Jenster G, (1999) The role of the androgen receptor in the development and progression of prostate cancer. Semin Oncol 26: 407-421.
2. Feldman BJ, Feldman D, (2001) The development of androgen-independent prostate cancer. Nature Reviews Cancer 1: 34-45.
3. Pienta KJ, Bradley D, (2006) Mechanisms underlying the development of androgen-independent prostate cancer. Clin Cancer Res 12: 1665-1671.
4. Linja MJ, Savinainen KJ, Saramaki OR, Tammela TL, Vessella RL, et al. (2001) Amplification and overexpression of androgen receptor gene in hormone-refractory prostate cancer. Cancer Research 61: 3550-3555.
5. Chmelar R, Buchanan G, Need EF, Tilley W, Greenberg NM, (2007) Androgen receptor coregulators and their involvement in the development and progression of prostate cancer. Int J Cancer 120: 719-733.
6. Dehm SM, Tindall DJ, (2006) Ligand-independent androgen receptor activity is activation function-2-independent and resistant to antiandrogens in androgen refractory prostate cancer cells. Journal of Biological Chemistry 281: 27882-27893.
7. Brooke GN, Parker MG, Bevan CL, (2008) Mechanisms of androgen receptor activation in advanced prostate cancer: differential co-activator recruitment and gene expression. Oncogene 27: 2941-2950.
8. Lu S, Tsai SY, Tsai MJ, (1999) Molecular mechanisms of androgen-independent growth of human prostate cancer LNCaP-AI cells. Endocrinology 140: 5054-5059.
9. Wen Y, Hu MC, Makino K, Spohn B, Bartholomeusz G, et al. (2000) HER-2/neu promotes androgen-independent survival and growth of prostate cancer cells through the Akt pathway. Cancer Research 60: 6841-6845.
10. Murillo H, Huang H, Schmidt LJ, Smith DI, Tindall DJ, (2001) Role of PI3K signaling in survival and progression of LNCaP prostate cancer cells to the androgen refractory state. Endocrinology 142: 4795-4805.
11. Zhang C, Wang L, Wu D, Chen H, Chen Z, et al. (2011) Definition of a FoxA1 Cistrome that is crucial for G1 to S-phase cell-cycle transit in castration-resistant prostate cancer. Cancer Research 71: 6738-6748.
12. Sharma A, Yeow WS, Ertel A, Coleman I, Clegg N, et al. (2010) The retinoblastoma tumor suppressor controls androgen signaling and human prostate cancer progression. J Clin Invest 120: 4478-4492.
13. Ettinger SL, Sobel R, Whitmore TG, Akbari M, Bradley DR, et al. (2004) Dysregulation of sterol response element-binding proteins and downstream effectors in prostate cancer during progression to androgen independence. Cancer Research 64: 2212-2221.
14. Montgomery RB, Mostaghel EA, Vessella R, Hess DL, Kalhorn TF, et al. (2008) Maintenance of intratumoral androgens in metastatic prostate cancer: a mechanism for castration-resistant tumor growth. Cancer Research 68: 4447-4454.
15. Harris WP, Mostaghel EA, Nelson PS, Montgomery B, (2009) Androgen deprivation therapy: progress in understanding mechanisms of resistance and optimizing androgen depletion. Nat Clin Pract Urol 6: 76-85.
16. Agus DB, Cordon-Cardo C, Fox W, Drobnjak M, Koff A, et al. (1999) Prostate cancer cell cycle regulators: response to androgen withdrawal and development of androgen independence. J Natl Cancer Inst 91: 1869-1876.
17. Khandrika L, Lieberman R, Koul S, Kumar B, Maroni P, et al. (2009) Hypoxia-associated p38 mitogen-activated protein kinase-mediated androgen receptor activation and increased HIF-1alpha levels contribute to emergence of an aggressive phenotype in prostate cancer. Oncogene 28: 1248-1260.
18. Craft N, Chhor C, Tran C, Belldegrun A, DeKernion J, et al. (1999) Evidence for clonal outgrowth of androgen-independent prostate cancer cells from androgen-dependent tumors through a two-step process. Cancer Research 59: 5030-5036.
19. Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, et al. (1996) Metastatic prostate cancer in a transgenic mouse. Cancer Research 56: 4096-4102.
20. Tso CL, McBride WH, Sun J, Patel B, Tsui KH, et al. (2000) Androgen deprivation induces selective outgrowth of aggressive hormone-refractory prostate cancer clones expressing distinct cellular and molecular properties not present in parental androgen-dependent cancer cells. Cancer J 6: 220-233.
21. Knudsen KE, Arden KC, Cavenee WK, (1998) Multiple G1 regulatory elements control the androgen-dependent proliferation of prostatic carcinoma cells. Journal of Biological Chemistry 273: 20213-20222.
22. Campisi J, d'Adda di Fagagna F, (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8: 729-740.
23. Pernicova Z, Slabakova E, Kharaishvili G, Bouchal J, Kral M, et al. (2011) Androgen depletion induces senescence in prostate cancer cells through down-regulation of Skp2. Neoplasia 13: 526-536.
24. Ewald JA, Desotelle JA, Church DR, Yang B, Huang W, et al. (2012) Androgen deprivation induces senescence characteristics in prostate cancer cells in vitro and in vivo. Prostate.
25. Halazonetis TD, Gorgoulis VG, Bartek J, (2008) An oncogene-induced DNA damage model for cancer development. Science 319: 1352-1355.
26. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637.
27. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642.
28. Rai P, Onder TT, Young JJ, McFaline JL, Pang B, et al. (2009) Continuous elimination of oxidized nucleotides is necessary to prevent rapid onset of cellular senescence. Proc Natl Acad Sci U S A 106: 169-174.
29. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, et al. (2003) Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9: 493-501.
30. Peacock SO, Fahrenholtz CD, Burnstein KL, (2012) Vav3 enhances androgen receptor splice variant activity and is critical for castration-resistant prostate cancer growth and survival. Mol Endocrinol 26: 1967-1979.
31. Dimri G, Lee X, Basile G, Acosta M, Scott G, et al. (1995) A Biomarker that Identifies Senescent Human Cells in Culture and in Aging Skin in vivo. Proceedings of the National Academy of Sciences 92: 9363-9367.
32. van Bokhoven A, Varella-Garcia M, Korch C, Johannes WU, Smith EE, et al. (2003) Molecular characterization of human prostate carcinoma cell lines. Prostate 57: 205-225.
33. Lu S, Tsai SY, Tsai MJ, (1997) Regulation of androgen-dependent prostatic cancer cell growth: androgen regulation of CDK2, CDK4, and CKI p16 genes. Cancer Research 57: 4511-4516.
34. Kokontis JM, Hay N, Liao S, (1998) Progression of LNCaP prostate tumor cells during androgen deprivation: hormone-independent growth, repression of proliferation by androgen, and role for p27Kip1 in androgen-induced cell cycle arrest. Mol Endocrinol 12: 941-953.
35. Hsieh T, Wu J, (1997) Differential expression and regulation of p53 in human prostatic cells. Int J Oncol 10: 1109-1112.
36. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS, (2010) The essence of senescence. Genes & Development 24: 2463-2479.
37. Pardee AB, (1974) A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci U S A 71: 1286-1290.
38. Sedelnikova OA, Horikawa I, Zimonjic DB, Popescu NC, Bonner WM, et al. (2004) Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat Cell Biol 6: 168-170.
39. Itahana K, Campisi J, Dimri G, (2004) Mechanisms of cellular senescence in human and mouse cells. Biogerontology 5: 1-10.
40. Beausejour CM, Krtolica A, Galimi F, Narita M, Lowe SW, et al. (2003) Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J 22: 4212-4222.
41. Herbig U, Jobling WA, Chen BP, Chen DJ, Sedivy JM, (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Molecular Cell 14: 501-513.
42. Cheng L, Sebo TJ, Cheville JC, Pisansky TM, Slezak J, et al. (1999) p53 protein overexpression is associated with increased cell proliferation in patients with locally recurrent prostate carcinoma after radiation therapy. Cancer 85: 1293-1299.
43. Navone NM, Troncoso P, Pisters LL, Goodrow TL, Palmer JL, et al. (1993) p53 protein accumulation and gene mutation in the progression of human prostate carcinoma. J Natl Cancer Inst 85: 1657-1669.
44. Aprikian AG, Sarkis AS, Fair WR, Zhang ZF, Fuks Z, et al. (1994) Immunohistochemical determination of p53 protein nuclear accumulation in prostatic adenocarcinoma. J Urol 151: 1276-1280.
45. Toussaint O, Remacle J, Dierick JF, Pascal T, Frippiat C, et al. (2002) From the Hayflick mosaic to the mosaics of ageing. Role of stress-induced premature senescence in human ageing. Int J Biochem Cell Biol 34: 1415-1429.
46. Chen JH, Ozanne SE, Hales CN, (2005) Heterogeneity in premature senescence by oxidative stress correlates with differential DNA damage during the cell cycle. DNA Repair (Amst) 4: 1140-1148.
47. Serrano M, Blasco MA, (2001) Putting the stress on senescence. Curr Opin Cell Biol 13: 748-753.
48. Gordon V, Bhadel S, Wunderlich W, Zhang J, Ficarro SB, et al. (2010) CDK9 regulates AR promoter selectivity and cell growth through serine 81 phosphorylation. Mol Endocrinol 24: 2267-2280.
49. Gurtner A, Starace G, Norelli G, Piaggio G, Sacchi A, et al. (2010) Mutant p53-induced up-regulation of mitogen-activated protein kinase kinase 3 contributes to gain of function. Journal of Biological Chemistry 285: 14160-14169.
50. Morton JP, Timpson P, Karim SA, Ridgway RA, Athineos D, et al. (2010) Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc Natl Acad Sci U S A 107: 246-251.
51. Rieber M, Strasberg Rieber M, (2009) DN-R175H p53 mutation is more effective than p53 interference in inducing epithelial disorganization and activation of proliferation signals in human carcinoma cells: role of E-cadherin. Int J Cancer 125: 1604-1612.
52. Di Como CJ, Gaiddon C, Prives C, (1999) p73 function is inhibited by tumor-derived p53 mutants in mammalian cells. Mol Cell Biol 19: 1438-1449.
53. Yu EY, Gulati R, Telesca D, Jiang P, Tam S, et al. (2010) Duration of first off-treatment interval is prognostic for time to castration resistance and death in men with biochemical relapse of prostate cancer treated on a prospective trial of intermittent androgen deprivation. J Clin Oncol 28: 2668-2673.
54. Wang E, (1995) Senescent human fibroblasts resist programmed cell death, and failure to suppress bcl2 is involved. Cancer Research 55: 2284-2292.
55. Marcotte R, Lacelle C, Wang E, (2004) Senescent fibroblasts resist apoptosis by downregulating caspase-3. Mech Ageing Dev 125: 777-783.
56. Hampel B, Malisan F, Niederegger H, Testi R, Jansen-Durr P, (2004) Differential regulation of apoptotic cell death in senescent human cells. Exp Gerontol 39: 1713-1721.
57. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, et al. (2008) Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6: 2853-2868.
58. Seaton A, Scullin P, Maxwell PJ, Wilson C, Pettigrew J, et al. (2008) Interleukin-8 signaling promotes androgen-independent proliferation of prostate cancer cells via induction of androgen receptor expression and activation. Carcinogenesis 29: 1148-1156.
59. Singh RK, Lokeshwar BL, (2011) The IL-8-Regulated Chemokine Receptor CXCR7 Stimulates EGFR Signaling to Promote Prostate Cancer Growth. Cancer Research 71: 3268-3277.
60. Araki S, Omori Y, Lyn D, Singh RK, Meinbach DM, et al. (2007) Interleukin-8 is a molecular determinant of androgen independence and progression in prostate cancer. Cancer Research 67: 6854-6862.
61. Acosta JC, O'Loghlen A, Banito A, Raguz S, Gil J, (2008) Control of senescence by CXCR2 and its ligands. Cell Cycle 7: 2956-2959.
62. Wilson C, Wilson T, Johnston PG, Longley DB, Waugh DJ, (2008) Interleukin-8 signaling attenuates TRAIL- and chemotherapy-induced apoptosis through transcriptional regulation of c-FLIP in prostate cancer cells. Mol Cancer Ther 7: 2649-2661.
63. Zhang M, Latham DE, Delaney MA, Chakravarti A, (2005) Survivin mediates resistance to antiandrogen therapy in prostate cancer. Oncogene 24: 2474-2482.
64. Kishi H, Igawa M, Kikuno N, Yoshino T, Urakami S, et al. (2004) Expression of the survivin gene in prostate cancer: correlation with clinicopathological characteristics, proliferative activity and apoptosis. J Urol 171: 1855-1860.
65. Signoretti S, Pires MM, Lindauer M, Horner JW, Grisanzio C, et al. (2005) p63 regulates commitment to the prostate cell lineage. Proc Natl Acad Sci U S A 102: 11355-11360.
66. Su X, Paris M, Gi YJ, Tsai KY, Cho MS, et al. (2009) TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 5: 64-75.
67. Keyes WM, Wu Y, Vogel H, Guo X, Lowe SW, et al. (2005) p63 deficiency activates a program of cellular senescence and leads to accelerated aging. Genes & Development 19: 1986-1999.
68. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, et al. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303: 844-848.
69. Gorgoulis VG, Halazonetis TD, (2010) Oncogene-induced senescence: the bright and dark side of the response. Curr Opin Cell Biol 22: 816-827.
70. Campisi J, (2010) Cellular senescence: putting the paradoxes in perspective. Curr Opin Genet Dev 21: 107-112.
71. Nelson G, Wordsworth J, Wang C, Jurk D, Lawless C, et al. (2012) A senescent cell bystander effect: senescence-induced senescence. Aging Cell 11: 345-349.
72. Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, et al. (2011) Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 479: 547-551.
73. Tsai KK, Stuart J, Chuang YY, Little JB, Yuan ZM, (2009) Low-dose radiation-induced senescent stromal fibroblasts render nearby breast cancer cells radioresistant. Radiat Res 172: 306-313.
74. Liu D, Hornsby PJ, (2007) Senescent human fibroblasts increase the early growth of xenograft tumors via matrix metalloproteinase secretion. Cancer Research 67: 3117-3126.
75. Krtolica A, Parrinello S, Lockett S, Desprez PY, Campisi J, (2001) Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc Natl Acad Sci U S A 98: 12072-12077.
76. Davalos AR, Coppe JP, Campisi J, Desprez PY, (2010) Senescent cells as a source of inflammatory factors for tumor progression. Cancer Metastasis Rev 29: 273-283.
77. Yang G, Rosen DG, Zhang Z, Bast RC Jr, Mills GB, et al. (2006) The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. Proc Natl Acad Sci U S A 103: 16472-16477.
78. Pazolli E, Luo X, Brehm S, Carbery K, Chung JJ, et al. (2009) Senescent stromal-derived osteopontin promotes preneoplastic cell growth. Cancer Research 69: 1230-1239.
79. Bavik C, Coleman I, Dean JP, Knudsen B, Plymate S, et al. (2006) The gene expression program of prostate fibroblast senescence modulates neoplastic epithelial cell proliferation through paracrine mechanisms. Cancer Research 66: 794-802.
80. Dean JP, Nelson PS, (2008) Profiling influences of senescent and aged fibroblasts on prostate carcinogenesis. Br J Cancer 98: 245-249.
81. Tokar EJ, Ancrile BB, Cunha GR, Webber MM, (2005) Stem/progenitor and intermediate cell types and the origin of human prostate cancer. Differentiation 73: 463-473.
82. English HF, Santen RJ, Isaacs JT, (1987) Response of glandular versus basal rat ventral prostatic epithelial cells to androgen withdrawal and replacement. Prostate 11: 229-242.
83. Koster MI, Kim S, Mills AA, DeMayo FJ, Roop DR, (2004) p63 is the molecular switch for initiation of an epithelial stratification program. Genes & Development 18: 126-131.
84. Rebbaa A, Zheng X, Chou PM, Mirkin BL, (2003) Caspase inhibition switches doxorubicin-induced apoptosis to senescence. Oncogene 22: 2805-2811.
85. Seluanov A, Gorbunova V, Falcovitz A, Sigal A, Milyavsky M, et al. (2001) Change of the death pathway in senescent human fibroblasts in response to DNA damage is caused by an inability to stabilize p53. Mol Cell Biol 21: 1552-1564.
86. Mirochnik Y, Veliceasa D, Williams L, Maxwell K, Yemelyanov A, et al. (2012) Androgen receptor drives cellular senescence. PLoS ONE 7: e31052.
87. Burchardt M, Burchardt T, Shabsigh A, Ghafar M, Chen MW, et al. (2001) Reduction of wild type p53 function confers a hormone resistant phenotype on LNCaP prostate cancer cells. Prostate 48: 225-230.
88. Tovar C, Higgins B, Kolinsky K, Xia M, Packman K, et al. (2011) MDM2 antagonists boost antitumor effect of androgen withdrawal: implications for therapy of prostate cancer. Mol Cancer 10: 49.
89. Mu Z, Hachem P, Hensley H, Stoyanova R, Kwon HW, et al. (2008) Antisense MDM2 enhances the response of androgen insensitive human prostate cancer cells to androgen deprivation in vitro and in vivo. Prostate 68: 599-609.