Jak2-Stat5a/b Signaling Induces Epithelial-to-Mesenchymal Transition and Stem-Like Cell Properties in Prostate Cancer

American Journal of Pathology

Volumn 185, Issue 9, 2015, Pages 2505-2522

  Talati, Pooja G ^a   Gu, Lei ^a   Ellsworth, Elyse M ^a   Girondo, Melanie A ^a   Trerotola, Marco ^a   Hoang, David T ^a   Leiby, Benjamin ^b   Dagvadorj, Ayush ^a   McCue, Peter A ^a   Lallas, Costas D ^a   Trabulsi, Edouard J ^a   Gomella, Leonard ^a   Aplin, Andrew E ^a   Languino, Lucia ^a,c   Fatatis, Alessandro ^d   Rui, Hallgeir ^a   Nevalainen, Marja T ^a,c,e  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c WISTAR INSTITUTE   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e Medical College of Wisconsin Cancer Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; FIBRONECTIN; JANUS KINASE 2; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; PROLACTIN; STAT5A PROTEIN; STAT5B PROTEIN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; CADHERIN; JAK2 PROTEIN, HUMAN; NUCLEAR PROTEIN; STAT5 PROTEIN; STAT5A PROTEIN, HUMAN; STAT5B PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN; TWIST RELATED PROTEIN 1; TWIST1 PROTEIN, HUMAN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; EX VIVO STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL CULTURE; TUMOR XENOGRAFT; ANIMAL; CANCER STEM CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; RECURRENT DISEASE;

ANIMALS; CADHERINS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; JANUS KINASE 2; MALE; MICE; NEOPLASTIC STEM CELLS; NUCLEAR PROTEINS; PROSTATIC NEOPLASMS; RECURRENCE; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEINS; TWIST-RELATED PROTEIN 1;

EID: 84941053082     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.04.026     Document Type: Article

References (88)

1. G.R. Mundy Metastasis to bone: causes, consequences and therapeutic opportunities Nat Rev Cancer 2 2002 584 593
2. K. Tomita, A. van Bokhoven, G.J. van Leenders, E.T. Ruijter, C.F. Jansen, M.J. Bussemakers, and J.A. Schalken Cadherin switching in human prostate cancer progression Cancer Res 60 2000 3650 3654
3. R. Kalluri, and R.A. Weinberg The basics of epithelial-mesenchymal transition J Clin Invest 119 2009 1420 1428
4. R.N. Kaplan, R.D. Riba, S. Zacharoulis, A.H. Bramley, L. Vincent, C. Costa, D.D. MacDonald, D.K. Jin, K. Shido, S.A. Kerns, Z. Zhu, D. Hicklin, Y. Wu, J.L. Port, N. Altorki, E.R. Port, D. Ruggero, S.V. Shmelkov, K.K. Jensen, S. Rafii, and D. Lyden VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche Nature 438 2005 820 827
5. H. Peinado, S. Lavotshkin, and D. Lyden The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts Semin Cancer Biol 21 2011 139 146
6. J.T. Erler, K.L. Bennewith, T.R. Cox, G. Lang, D. Bird, A. Koong, Q.T. Le, and A.J. Giaccia Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche Cancer Cell 15 2009 35 44
7. R.N. Kaplan, S. Rafii, and D. Lyden Preparing the "soil": the premetastatic niche Cancer Res 66 2006 11089 11093
8. P.S. Steeg Cancer biology: emissaries set up new sites Nature 438 2005 750 751
9. Y. Shiozawa, E.A. Pedersen, A.M. Havens, Y. Jung, A. Mishra, J. Joseph, J.K. Kim, L.R. Patel, C. Ying, A.M. Ziegler, M.J. Pienta, J. Song, J. Wang, R.D. Loberg, P.H. Krebsbach, K.J. Pienta, and R.S. Taichman Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow J Clin Invest 121 2011 1298 1312
10. K. Gravdal, O.J. Halvorsen, S.A. Haukaas, and L.A. Akslen A switch from E-cadherin to N-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer Clin Cancer Res 13 2007 7003 7011
11. H. Tanaka, E. Kono, C.P. Tran, H. Miyazaki, J. Yamashiro, T. Shimomura, L. Fazli, R. Wada, J. Huang, R.L. Vessella, J. An, S. Horvath, M. Gleave, M.B. Rettig, Z.A. Wainberg, and R.E. Reiter Monoclonal antibody targeting of N-cadherin inhibits prostate cancer growth, metastasis and castration resistance Nat Med 16 2010 1414 1420
12. J.R. Graff, E. Gabrielson, H. Fujii, S.B. Baylin, and J.G. Herman Methylation patterns of the E-cadherin 5' CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression J Biol Chem 275 2000 2727 2732
13. K. Yoshiura, Y. Kanai, A. Ochiai, Y. Shimoyama, T. Sugimura, and S. Hirohashi Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas Proc Natl Acad Sci U S A 92 1995 7416 7419
14. J. Yang, S.A. Mani, J.L. Donaher, S. Ramaswamy, R.A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R.A. Weinberg Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis Cell 117 2004 927 939
15. Q. Qin, Y. Xu, T. He, C. Qin, and J. Xu Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms Cell Res 22 2012 90 106
16. N.R. Alexander, N.L. Tran, H. Rekapally, C.E. Summers, C. Glackin, and R.L. Heimark N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1 Cancer Res 66 2006 3365 3369
17. H. Zheng, and Y. Kang Multilayer control of the EMT master regulators Oncogene 33 2014 1755 1763
18. W.K. Kwok, M.T. Ling, T.W. Lee, T.C. Lau, C. Zhou, X. Zhang, C.W. Chua, K.W. Chan, F.L. Chan, C. Glackin, Y.C. Wong, and X. Wang Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target Cancer Res 65 2005 5153 5162
19. M.B. Weiss, E.V. Abel, M.M. Mayberry, K.J. Basile, A.C. Berger, and A.E. Aplin TWIST1 is an ERK1/2 effector that promotes invasion and regulates MMP-1 expression in human melanoma cells Cancer Res 72 2012 6382 6392
20. S.A. Mikheeva, A.M. Mikheev, A. Petit, R. Beyer, R.G. Oxford, L. Khorasani, J.P. Maxwell, C.A. Glackin, H. Wakimoto, I. Gonzalez-Herrero, I. Sanchez-Garcia, J.R. Silber, P.J. Horner, and R.C. Rostomily TWIST1 promotes invasion through mesenchymal change in human glioblastoma Mol Cancer 9 2010 194
21. Z. Yang, X. Zhang, H. Gang, X. Li, Z. Li, T. Wang, J. Han, T. Luo, F. Wen, and X. Wu Up-regulation of gastric cancer cell invasion by Twist is accompanied by N-cadherin and fibronectin expression Biochem Biophys Res Commun 358 2007 925 930
22. W.H. Yang, H.Y. Lan, C.H. Huang, S.K. Tai, C.H. Tzeng, S.Y. Kao, K.J. Wu, M.C. Hung, and M.H. Yang RAC1 activation mediates Twist1-induced cancer cell migration Nat Cell Biol 14 2012 366 374
23. Y. Kang, and J. Massague Epithelial-mesenchymal transitions: twist in development and metastasis Cell 118 2004 277 279
24. M.A. Eckert, T.M. Lwin, A.T. Chang, J. Kim, E. Danis, L. Ohno-Machado, and J. Yang Twist1-induced invadopodia formation promotes tumor metastasis Cancer Cell 19 2011 372 386
25. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, M. Shipitsin, L.L. Campbell, K. Polyak, C. Brisken, J. Yang, and R.A. Weinberg The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
26. A.P. Morel, M. Lievre, C. Thomas, G. Hinkal, S. Ansieau, and A. Puisieux Generation of breast cancer stem cells through epithelial-mesenchymal transition PLoS One 3 2008 e2888
27. A.J. Armstrong, M.S. Marengo, S. Oltean, G. Kemeny, R.L. Bitting, J.D. Turnbull, C.I. Herold, P.K. Marcom, D.J. George, and M.A. Garcia-Blanco Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers Mol Cancer Res 9 2011 997 1007
28. A.T. Collins, P.A. Berry, C. Hyde, M.J. Stower, and N.J. Maitland Prospective identification of tumorigenic prostate cancer stem cells Cancer Res 65 2005 10946 10951
29. G. Gu, J. Yuan, M. Wills, and S. Kasper Prostate cancer cells with stem cell characteristics reconstitute the original human tumor in vivo Cancer Res 67 2007 4807 4815
30. R.U. Lukacs, S. Memarzadeh, H. Wu, and O.N. Witte Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation Cell Stem Cell 7 2010 682 693
31. J.J. Jacobs, K. Kieboom, S. Marino, R.A. DePinho, and M. van Lohuizen The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus Nature 397 1999 164 168
32. N.E. Sharpless, and R.A. DePinho The INK4A/ARF locus and its two gene products Curr Opin Genet Dev 9 1999 22 30
33. I.K. Park, S.J. Morrison, and M.F. Clarke Bmi1, stem cells, and senescence regulation J Clin Invest 113 2004 175 179
34. M.H. Yang, D.S. Hsu, H.W. Wang, H.J. Wang, H.Y. Lan, W.H. Yang, C.H. Huang, S.Y. Kao, C.H. Tzeng, S.K. Tai, S.Y. Chang, O.K. Lee, and K.J. Wu Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition Nat Cell Biol 12 2010 982 992
35. D. Kong, S. Banerjee, A. Ahmad, Y. Li, Z. Wang, S. Sethi, and F.H. Sarkar Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells PLoS One 5 2010 e12445
36. L.B. Song, J. Li, W.T. Liao, Y. Feng, C.P. Yu, L.J. Hu, Q.L. Kong, L.H. Xu, X. Zhang, W.L. Liu, M.Z. Li, L. Zhang, T.B. Kang, L.W. Fu, W.L. Huang, Y.F. Xia, S.W. Tsao, M. Li, V. Band, H. Band, Q.H. Shi, Y.X. Zeng, and M.S. Zeng The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells J Clin Invest 119 2009 3626 3636
37. T.J. Ahonen, J. Xie, M.J. LeBaron, J. Zhu, M. Nurmi, K. Alanen, H. Rui, and M.T. Nevalainen Inhibition of transcription factor Stat5 induces cell death of human prostate cancer cells J Biol Chem 278 2003 27287 27292
38. L. Gu, Z. Liao, D.T. Hoang, A. Dagvadorj, S. Gupta, S. Blackmon, E. Ellsworth, P. Talati, B. Leiby, M. Zinda, C.D. Lallas, E.J. Trabulsi, P. McCue, L. Gomella, D. Huszar, and M.T. Nevalainen Pharmacologic inhibition of Jak2-Stat5 signaling by Jak2 inhibitor AZD1480 potently suppresses growth of both primary and castrate-resistant prostate cancer Clin Cancer Res 19 2013 5658 5674
39. L. Gu, A. Dagvadorj, J. Lutz, B. Leiby, G. Bonuccelli, M.P. Lisanti, S. Addya, P. Fortina, A. Dasgupta, T. Hyslop, L. Bubendorf, and M.T. Nevalainen Transcription factor Stat3 stimulates metastatic behavior of human prostate cancer cells in vivo, whereas Stat5b has a preferential role in the promotion of prostate cancer cell viability and tumor growth Am J Pathol 176 2010 1959 1972
40. A. Dagvadorj, S. Collins, J.B. Jomain, J. Abdulghani, J. Karras, T. Zellweger, H. Li, M. Nurmi, K. Alanen, T. Mirtti, T. Visakorpi, L. Bubendorf, V. Goffin, and M.T. Nevalainen Autocrine prolactin promotes prostate cancer cell growth via Janus kinase-2-signal transducer and activator of transcription-5a/b signaling pathway Endocrinology 148 2007 3089 3101
41. A. Dagvadorj, R.A. Kirken, B. Leiby, J. Karras, and M.T. Nevalainen Transcription factor signal transducer and activator of transcription 5 promotes growth of human prostate cancer cells in vivo Clin Cancer Res 14 2008 1317 1324
42. A.V. Kazansky, D.M. Spencer, and N.M. Greenberg Activation of signal transducer and activator of transcription 5 is required for progression of autochthonous prostate cancer: evidence from the transgenic adenocarcinoma of the mouse prostate system Cancer Res 63 2003 8757 8762
43. T. Mirtti, B.E. Leiby, J. Abdulghani, E. Aaltonen, M. Pavela, A. Mamtani, K. Alanen, L. Egevad, T. Granfors, A. Josefsson, P. Stattin, A. Bergh, and M.T. Nevalainen Nuclear Stat5a/b predicts early recurrence and prostate cancer-specific death in patients treated by radical prostatectomy Hum Pathol 44 2013 310 319
44. L. Gu, P. Vogiatzi, M. Puhr, A. Dagvadorj, J. Lutz, A. Ryder, S. Addya, P. Fortina, C. Cooper, B. Leiby, A. Dasgupta, T. Hyslop, L. Bubendorf, K. Alanen, T. Mirtti, and M.T. Nevalainen Stat5 promotes metastatic behavior of human prostate cancer cells in vitro and in vivo Endocr Relat Cancer 17 2010 481 493
45. H. Li, T.J. Ahonen, K. Alanen, J. Xie, M.J. LeBaron, T.G. Pretlow, E.L. Ealley, Y. Zhang, M. Nurmi, B. Singh, P.M. Martikainen, and M.T. Nevalainen Activation of signal transducer and activator of transcription 5 in human prostate cancer is associated with high histological grade Cancer Res 64 2004 4774 4782
46. B.R. Haddad, L. Gu, T. Mirtti, A. Dagvadorj, P. Vogiatzi, D.T. Hoang, R. Bajaj, B. Leiby, E. Ellsworth, S. Blackmon, C. Ruiz, M. Curtis, P. Fortina, A. Ertel, C. Liu, H. Rui, T. Visakorpi, L. Bubendorf, C.D. Lallas, E.J. Trabulsi, P. McCue, L. Gomella, and M.T. Nevalainen STAT5A/B gene locus undergoes amplification during human prostate cancer progression Am J Pathol 182 2013 2264 2275
47. H. Li, Y. Zhang, A. Glass, T. Zellweger, E. Gehan, L. Bubendorf, E.P. Gelmann, and M.T. Nevalainen Activation of signal transducer and activator of transcription-5 in prostate cancer predicts early recurrence Clin Cancer Res 11 2005 5863 5868
48. C. Thomas, A. Zoubeidi, H. Kuruma, L. Fazli, F. Lamoureux, E. Beraldi, B.P. Monia, A.R. MacLeod, J.W. Thuroff, and M.E. Gleave Transcription factor Stat5 knockdown enhances androgen receptor degradation and delays castration-resistant prostate cancer progression in vivo Mol Cancer Ther 10 2011 347 359
49. D.T. Hoang, L. Gu, Z. Liao, F. Shen, P.G. Talati, M. Koptyra, S.H. Tan, E. Ellsworth, S. Gupta, H. Montie, A. Dagvadorj, S. Savolainen, B. Leiby, T. Mirtti, D.E. Merry, and M.T. Nevalainen Inhibition of Stat5a/b enhances proteasomal degradation of androgen receptor liganded by antiandrogens in prostate cancer Mol Cancer Ther 14 2014 1 14
50. J.E. Darnell Jr. STATs and gene regulation Science 277 1997 1630 1635
51. D.E. Levy, and J.E. Darnell Jr. Stats: transcriptional control and biological impact Nat Rev Mol Cell Biol 3 2002 651 662
52. H. Rui, R.A. Kirken, and W.L. Farrar Activation of receptor-associated tyrosine kinase JAK2 by prolactin J Biol Chem 269 1994 5364 5368
53. H. Rui, J.J. Lebrun, R.A. Kirken, P.A. Kelly, and W.L. Farrar JAK2 activation and cell proliferation induced by antibody-mediated prolactin receptor dimerization Endocrinology 135 1994 1299 1306
54. G.S. Campbell, L.S. Argetsinger, J.N. Ihle, P.A. Kelly, J.A. Rillema, and C. Carter-Su Activation of JAK2 tyrosine kinase by prolactin receptors in Nb2 cells and mouse mammary gland explants Proc Natl Acad Sci U S A 91 1994 5232 5236
55. E. Soldaini, S. John, S. Moro, J. Bollenbacher, U. Schindler, and W.J. Leonard DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites Mol Cell Biol 20 2000 389 401
56. C.M. Horvath, Z. Wen, and J.E. Darnell Jr. A STAT protein domain that determines DNA sequence recognition suggests a novel DNA-binding domain Genes Dev 9 1995 984 994
57. M.T. Nevalainen, E.M. Valve, P.M. Ingleton, M. Nurmi, P.M. Martikainen, and P.L. Harkonen Prolactin and prolactin receptors are expressed and functioning in human prostate J Clin Invest 99 1997 618 627
58. E. Weiss-Messer, O. Merom, A. Adi, R. Karry, M. Bidosee, R. Ber, A. Kaploun, A. Stein, and R.J. Barkey Growth hormone (GH) receptors in prostate cancer: gene expression in human tissues and cell lines and characterization, GH signaling and androgen receptor regulation in LNCaP cells Mol Cell Endocrinol 220 2004 109 123
59. L. Feldman, Y. Wang, J.S. Rhim, N. Bhattacharya, M. Loda, and A.J. Sytkowski Erythropoietin stimulates growth and STAT5 phosphorylation in human prostate epithelial and prostate cancer cells Prostate 66 2006 135 145
60. A.W. Grasso, D. Wen, C.M. Miller, J.S. Rhim, T.G. Pretlow, and H.J. Kung ErbB kinases and NDF signaling in human prostate cancer cells Oncogene 15 1997 2705 2716
61. A. Dagvadorj, S.H. Tan, Z. Liao, J. Xie, M. Nurmi, K. Alanen, H. Rui, T. Mirtti, and M.T. Nevalainen N-terminal truncation of Stat5a/b circumvents PIAS3-mediated transcriptional inhibition of Stat5 in prostate cancer cells Int J Biochem Cell Biol 42 2010 2037 2046
62. F.L. Graham, and L. Prevec Manipulation of adenovirus vectors Methods Mol Biol 7 1991 109 128
63. M.B. Weiss, E.V. Abel, N. Dadpey, and A.E. Aplin FOXD3 modulates migration through direct transcriptional repression of TWIST1 in melanoma Mol Cancer Res 12 2014 1314 1323
64. M. Hedvat, D. Huszar, A. Herrmann, J.M. Gozgit, A. Schroeder, A. Sheehy, R. Buettner, D. Proia, C.M. Kowolik, H. Xin, B. Armstrong, G. Bebernitz, S. Weng, L. Wang, M. Ye, K. McEachern, H. Chen, D. Morosini, K. Bell, M. Alimzhanov, S. Ioannidis, P. McCoon, Z.A. Cao, H. Yu, R. Jove, and M. Zinda The JAK2 inhibitor AZD1480 potently blocks Stat3 signaling and oncogenesis in solid tumors Cancer Cell 16 2009 487 497
65. J. Abdulghani, L. Gu, A. Dagvadorj, J. Lutz, B. Leiby, G. Bonuccelli, M.P. Lisanti, T. Zellweger, K. Alanen, T. Mirtti, T. Visakorpi, L. Bubendorf, and M.T. Nevalainen Stat3 promotes metastatic progression of prostate cancer Am J Pathol 172 2008 1717 1728
66. A. Dubrovska, S. Kim, R.J. Salamone, J.R. Walker, S.M. Maira, C. Garcia-Echeverria, P.G. Schultz, and V.A. Reddy 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 106 2009 268 273
67. I.V. Litvinov, D.J. Vander Griend, Y. Xu, L. Antony, S.L. Dalrymple, and J.T. Isaacs Low-calcium serum-free defined medium selects for growth of normal prostatic epithelial stem cells Cancer Res 66 2006 8598 8607
68. D.A. Lawson, and O.N. Witte Stem cells in prostate cancer initiation and progression J Clin Invest 117 2007 2044 2050
69. M.T. Nevalainen, E.M. Valve, S.I. Makela, M. Blauer, P.J. Tuohimaa, and P.L. Harkonen Estrogen and prolactin regulation of rat dorsal and lateral prostate in organ culture Endocrinology 129 1991 612 622
70. M.T. Nevalainen, E.M. Valve, T. Ahonen, A. Yagi, J. Paranko, and P.L. Harkonen Androgen-dependent expression of prolactin in rat prostate epithelium in vivo and in organ culture FASEB J 11 1997 1297 1307
71. T.J. Ahonen, P.L. Harkonen, J. Laine, H. Rui, P.M. Martikainen, and M.T. Nevalainen Prolactin is a survival factor for androgen-deprived rat dorsal and lateral prostate epithelium in organ culture Endocrinology 140 1999 5412 5421
72. T.J. Ahonen, P.L. Harkonen, H. Rui, and M.T. Nevalainen PRL signal transduction in the epithelial compartment of rat prostate maintained as long-term organ cultures in vitro Endocrinology 143 2002 228 238
73. M.T. Nevalainen, P.L. Harkonen, E.M. Valve, W. Ping, M. Nurmi, and P.M. Martikainen Hormone regulation of human prostate in organ culture Cancer Res 53 1993 5199 5207
74. A. Dagvadorj, S.H. Tan, Z. Liao, L.R. Cavalli, B.R. Haddad, and M.T. Nevalainen Androgen-regulated and highly tumorigenic human prostate cancer cell line established from a transplantable primary CWR22 tumor Clin Cancer Res 14 2008 6062 6072
75. S.H. Tan, A. Dagvadorj, F. Shen, L. Gu, Z. Liao, J. Abdulghani, Y. Zhang, E.P. Gelmann, T. Zellweger, Z. Culig, T. Visakorpi, L. Bubendorf, R.A. Kirken, J. Karras, and M.T. Nevalainen Transcription factor Stat5 synergizes with androgen receptor in prostate cancer cells Cancer Res 68 2008 236 248
76. A.S. Sultan, J. Xie, M.J. LeBaron, E.L. Ealley, M.T. Nevalainen, and H. Rui Stat5 promotes homotypic adhesion and inhibits invasive characteristics of human breast cancer cells Oncogene 24 2005 746 760
77. K.S. McCarty Jr., L.S. Miller, E.B. Cox, J. Konrath, and K.S. McCarty Sr. Estrogen receptor analyses: correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies Arch Pathol Lab Med 109 1985 716 721
78. X. Liu, G.W. Robinson, F. Gouilleux, B. Groner, and L. Hennighausen Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue Proc Natl Acad Sci U S A 92 1995 8831 8835
79. M. Schmitt-Ney, W. Doppler, R.K. Ball, and B. Groner Beta-casein gene promoter activity is regulated by the hormone-mediated relief of transcriptional repression and a mammary-gland-specific nuclear factor Mol Cell Biol 11 1991 3745 3755
80. F.E. Utama, M.J. LeBaron, L.M. Neilson, A.S. Sultan, A.F. Parlow, K.U. Wagner, and H. Rui Human prolactin receptors are insensitive to mouse prolactin: implications for xenotransplant modeling of human breast cancer in mice J Endocrinol 188 2006 589 601
81. M.L. Zhu, and N. Kyprianou Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells FASEB J 24 2010 769 777
82. Y. Sun, B.E. Wang, K.G. Leong, P. Yue, L. Li, S. Jhunjhunwala, D. Chen, K. Seo, Z. Modrusan, W.Q. Gao, J. Settleman, and L. Johnson Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy Cancer Res 72 2012 527 536
83. M. Shiota, A. Yokomizo, Y. Tada, J. Inokuchi, E. Kashiwagi, D. Masubuchi, M. Eto, T. Uchiumi, and S. Naito Castration resistance of prostate cancer cells caused by castration-induced oxidative stress through Twist1 and androgen receptor overexpression Oncogene 29 2010 237 250
84. T. Eide, H. Ramberg, C. Glackin, D. Tindall, and K.A. Tasken TWIST1, a novel androgen-regulated gene, is a target for NKX3-1 in prostate cancer cells Cancer Cell Int 13 2013 4 10
85. G.Z. Cheng, W.Z. Zhang, M. Sun, Q. Wang, D. Coppola, M. Mansour, L.M. Xu, C. Costanzo, J.Q. Cheng, and L.H. Wang Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function J Biol Chem 283 2008 14665 14673
86. H.W. Lo, S.C. Hsu, W. Xia, X. Cao, J.Y. Shih, Y. Wei, J.L. Abbruzzese, G.N. Hortobagyi, and M.C. Hung Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression Cancer Res 67 2007 9066 9076
87. C. Fan, L. He, A. Kapoor, A. Gillis, A.P. Rybak, J.C. Cutz, and D. Tang Bmi1 promotes prostate tumorigenesis via inhibiting p16(INK4A) and p14(ARF) expression Biochim Biophys Acta 1782 2008 642 648
88. V. Rouet, R.L. Bogorad, C. Kayser, K. Kessal, C. Genestie, A. Bardier, D.R. Grattan, B. Kelder, J.J. Kopchick, P.A. Kelly, and V. Goffin Local prolactin is a target to prevent expansion of basal/stem cells in prostate tumors Proc Natl Acad Sci U S A 107 2010 15199 15204