Epithelial mesenchymal transition (EMT) in prostate growth and tumor progression

Translational Andrology and Urology

Volumn 2, Issue 3, 2013, Pages 202-211

  Grant, Campbell M ^a   Kyprianou, Natasha ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Adherens junctions; Androgens; Cell invasion; Embryonic growth; Moving front; Predictive markers; Therapeutic targeting

Indexed keywords

EID: 84901238857     PISSN: 22234683     EISSN: 22234691     Source Type: Journal    
DOI: 10.3978/j.issn.2223-4683.2013.09.04     Document Type: Review

References (85)

1. Siegel R, DeSantis C, Virgo K, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012;62:220-41.
2. Taichman RS, Loberg RD, Mehra R, et al. The evolving biology and treatment of prostate cancer. J Clin Invest 2007;117:2351-61.
3. Matuszak EA, Kyprianou N. Androgen regulation of epithelial-mesenchymal transition in prostate tumorigenesis. Expert Rev Endocrinol Metab 2011;6:469-482.
4. Schaeffer EM, Marchionni L, Huang Z, et al. Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 2008;27:7180-91.
5. Hayward SW, Cunha GR. The prostate: development and physiology. Radiol Clin North Am 2000;38:1-14.
6. Quigley CA, De Bellis A, Marschke KB, et al. Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 1995;16:271-321.
7. Friedlander TW, Ryan CJ. Targeting the androgen receptor. Urol Clin North Am 2012;39:453-64.
8. Chen CD, Welsbie DS, Tran C, et al. Molecular determinants of resistance to antiandrogen therapy. Nat Med 2004;10:33-9.
9. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer 2001;1:34-45.
10. Locke JA, Guns ES, Lubik AA, et al. Androgen levels increase by intratumoral de novo steroidogenesis during progression of castration-resistant prostate cancer. Cancer Res 2008;68:6407-15.
11. Culig Z, Hobisch A, Cronauer MV, et al. Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor. Cancer Res 1994;54:5474-8.
12. Stanbrough M, Bubley GJ, Ross K, et al. Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res 2006;66:2815-25.
13. Chang KH, Li R, Papari-Zareei M, et al. Dihydrotestosterone synthesis bypasses testosterone to drive castration-resistant prostate cancer. Proc Natl Acad Sci U S A 2011;108:13728-33.
14. Bhanalaph T, Varkarakis MJ, Murphy GP. Current status of bilateral adrenalectomy or advanced prostatic carcinoma. Ann Surg 1974;179:17-23.
15. de Bono JS, Logothetis CJ, Molina A, et al. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 2011;364:1995-2005.
16. Nishiyama T, Hashimoto Y, Takahashi K. The influence of androgen deprivation therapy on dihydrotestosterone levels in the prostatic tissue of patients with prostate cancer. Clin Cancer Res 2004;10:7121-6.
17. Tsao CK, Galsky MD, Small AC, et al. Targeting the androgen receptor signalling axis in castration-resistant prostate cancer (CRPC). BJU Int 2012;110:1580-8.
18. Logothetis CJ, Gallick GE, Maity SN, et al. Molecular classification of prostate cancer progression: foundation for marker-driven treatment of prostate cancer. Cancer Discov 2013;3:849-61.
19. Perry AS, Watson RW, Lawler M, et al. The epigenome as a therapeutic target in prostate cancer. Nat Rev Urol 2010;7:668-80.
20. Dehm SM, Schmidt LJ, Heemers HV, et al. Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res 2008;68:5469-77.
21. Watson PA, Chen YF, Balbas MD, et al. Constitutively active androgen receptor splice variants expressed in castration-resistant prostate cancer require full-length androgen receptor. Proc Natl Acad Sci U S A 2010;107:16759-65.
22. Colombel M, Symmans F, Gil S, et al. Detection of the apoptosis-suppressing oncoprotein bc1-2 in hormone-refractory human prostate cancers. Am J Pathol 1993;143:390-400.
23. Condeelis J, Singer RH, Segall JE. The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu Rev Cell Dev Biol 2005;21:695-718.
24. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-8.
25. Marker PC, Donjacour AA, Dahiya R, et al. Hormonal, cellular, and molecular control of prostatic development. Dev Biol 2003;253:165-74.
26. Prins GS, Putz O. Molecular signaling pathways that regulate prostate gland development. Differentiation 2008;76:641-59.
27. Rørth P. Collective cell migration. Annu Rev Cell Dev Biol 2009;25:407-29.
28. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia 2010;15:117-34.
29. Kokkinos MI, Wafai R, Wong MK, et al. Vimentin and epithelial-mesenchymal transition in human breast cancer-observations in vitro and in vivo. Cells Tissues Organs 2007;185:191-203.
30. Thiery JP, Acloque H, Huang RY, et al. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
31. Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 2009;28:151-66.
32. Wallerand H, Robert G, Pasticier G, et al. The epithelial-mesenchymal transition-inducing factor TWIST is an attractive target in advanced and/or metastatic bladder and prostate cancers. Urol Oncol 2010;28:473-9.
33. Barrallo-Gimeno A, Nieto MA. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005 ;132:3151-61.
34. Korpal M, Ell BJ, Buffa FM, et al. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nat Med 2011;17:1101-8.
35. Baritaki S, Chapman A, Yeung K, et al. Inhibition of epithelial to mesenchymal transition in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: pivotal roles of Snail repression and RKIP induction. Oncogene 2009;28:3573-85.
36. Nagaoka T, Karasawa H, Castro NP, et al. An evolving web of signaling networks regulated by Cripto-1. Growth Factors 2012;30:13-21.
37. Bianco C, Rangel MC, Castro NP, et al. Role of Cripto-1 in stem cell maintenance and malignant progression. Am J Pathol 2010;177:532-40.
38. Rangel MC, Karasawa H, Castro NP, et al. Role of Cripto-1 during epithelial-to-mesenchymal transition in development and cancer. Am J Pathol 2012;180:2188-200.
39. Wang H, Leav I, Ibaragi S, et al. SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer Res 2008;68:1625-30.
40. De Santa Barbara P, Bonneaud N, Boizet B, et al. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Müllerian hormone gene. Mol Cell Biol 1998;18:6653-65.
41. Wang H, McKnight NC, Zhang T, et al. SOX9 is expressed in normal prostate basal cells and regulates androgen receptor expression in prostate cancer cells. Cancer Res 2007;67:528-36.
42. Kulkarni AB, Huh CG, Becker D, et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 1993;90:770-4.
43. Sarraj MA, Escalona RM, Umbers A, et al. Fetal testis dysgenesis and compromised Leydig cell function in Tgfbr3 (beta glycan) knockout mice. Biol Reprod 2010;82:153-62.
44. Boutet A, De Frutos CA, Maxwell PH, et al. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J 2006;25:5603-13.
45. Combes AN, Wilhelm D, Davidson T, et al. Endothelial cell migration directs testis cord formation. Dev Biol 2009;326:112-20.
46. Alonso-Magdalena P, Brössner C, Reiner A, et al. A role for epithelial-mesenchymal transition in the etiology of benign prostatic hyperplasia. Proc Natl Acad Sci U S A 2009;106:2859-63.
47. Lu T, Lin WJ, Izumi K, et al. Targeting androgen receptor to suppress macrophage-induced EMT and benign prostatic hyperplasia (BPH) development. Mol Endocrinol 2012;26:1707-15.
48. Acloque H, Adams MS, Fishwick K, et al. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 2009;119:1438-49.
49. Ciruna B, Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell 2001;1:37-49.
50. Robinson DR, Zylstra CR, Williams BO. Wnt signaling and prostate cancer. Curr Drug Targets 2008;9:571-80.
51. Polette M, Mestdagt M, Bindels S, et al. Beta-catenin and ZO-1: shuttle molecules involved in tumor invasion-associated epithelial-mesenchymal transition processes. Cells Tissues Organs 2007;185:61-5.
52. Yang F, Li X, Sharma M, et al. Linking beta-catenin to androgen-signaling pathway. J Biol Chem 2002;277:11336-44.
53. Whitaker HC, Girling J, Warren AY, et al. Alterations in beta-catenin expression and localization in prostate cancer. Prostate 2008;68:1196-205.
54. Ivanović V, Todorović-Raković N, Demajo M, et al. Elevated plasma levels of transforming growth factor-beta 1 (TGF-beta 1) in patients with advanced breast cancer: association with disease progression. Eur J Cancer 2003;39:454-61.
55. Xie D, Gore C, Liu J, et al. Role of DAB2IP in modulating epithelial-to-mesenchymal transition and prostate cancer metastasis. Proc Natl Acad Sci U S A 2010;107:2485-90.
56. Massagué J. TGFbeta in Cancer. Cell 2008;134:215-30.
57. Wendt MK, Allington TM, Schiemann WP. Mechanisms of the epithelial-mesenchymal transition by TGF-beta. Future Oncol 2009;5:1145-68.
58. Moses HL, Yang EY, Pietenpol JA. TGF-beta stimulation and inhibition of cell proliferation: new mechanistic insights. Cell 1990;63:245-7.
59. Cakouros D, Raices RM, Gronthos S, et al. Twist-ing cell fate: mechanistic insights into the role of twist in lineage specification/differentiation and tumorigenesis. J Cell Biochem 2010;110:1288-98.
60. Yang J, Mani SA, Donaher JL, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004;117:927-39.
61. Yuen HF, Chua CW, Chan YP, et al. Significance of TWIST and E-cadherin expression in the metastatic progression of prostatic cancer. Histopathology 2007;50:648-58.
62. Makrilia N, Kollias A, Manolopoulos L, et al. Cell adhesion molecules: role and clinical significance in cancer. Cancer Invest 2009;27:1023-37.
63. Gravdal K, Halvorsen OJ, Haukaas SA, et al. 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 2007;13:7003-11.
64. Tanaka H, Kono E, Tran CP, et al. Monoclonal antibody targeting of N-cadherin inhibits prostate cancer growth,metastasis and castration resistance. Nat Med 2010;16:1414-20.
65. Liu YN, Liu Y, Lee HJ, et al. Activated androgen receptor downregulates E-cadherin gene expression and promotes tumor metastasis. Mol Cell Biol 2008;28:7096-108.
66. Akhurst RJ, Derynck R. TGF-beta signaling in cancer-a double-edged sword. Trends Cell Biol 2001;11:S44-51.
67. Niu YN, Xia SJ. Stroma-epithelium crosstalk in prostate cancer. Asian J Androl 2009;11:28-35.
68. Pu H, Collazo J, Jones E, et al. Dysfunctional transforming growth factor-beta receptor II accelerates prostate tumorigenesis in the TRAMP mouse model. Cancer Res 2009;69:7366-74.
69. Yang F, Tuxhorn JA, Ressler SJ, et al. Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Cancer Res 2005;65:8887-95.
70. Zhu ML, Kyprianou N. Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J 2010;24:769-77.
71. Cano P, Godoy A, Escamilla R, et al. Stromal-epithelial cell interactions and androgen receptor-coregulator recruitment is altered in the tissue microenvironment of prostate cancer. Cancer Res 2007;67:511-9.
72. van der Poel HG. Androgen receptor and TGFbeta1/Smad signaling are mutually inhibitory in prostate cancer. Eur Urol 2005;48:1051-8.
73. Bierie B, Moses HL. TGF-beta and cancer. Cytokine Growth Factor Rev 2006;17:29-40.
74. Drake JM, Strohbehn G, Bair TB, et al. ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells. Mol Biol Cell 2009;20:2207-17.
75. Anose BM, LaGoo L, Schwendinger J. Characterization of androgen regulation of ZEB-1 and PSA in 22RV1 prostate cancer cells. Adv Exp Med Biol 2008;617:541-6.
76. Sun Y, Wang BE, Leong KG, et al. Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy. Cancer Res 2012;72:527-36.
77. Bolton EC, So AY, Chaivorapol C, et al. Cell-and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev 2007;21:2005-17.
78. Raimondi C, Gradilone A, Naso G, et al. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Res Treat 2011;130:449-55.
79. Armstrong AJ, Eisenberger MA, Halabi S, et al. Biomarkers in the management and treatment of men with metastatic castration-resistant prostate cancer. Eur Urol 2012;61:549-59.
80. Choudhury AD, Eeles R, Freedland SJ, et al. The role of genetic markers in the management of prostate cancer. Eur Urol 2012;62:577-87.
81. Bernard D, Pourtier-Manzanedo A, Gil J, et al. Myc confers androgen-independent prostate cancer cell growth. J Clin Invest 2003;112:1724-31.
82. Salagierski M, Schalken JA. Molecular diagnosis of prostate cancer: PCA3 and TMPRSS2:ERG gene fusion. J Urol 2012;187:795-801.
83. van Gils MP, Hessels D, van Hooij O, et al. The time-resolved fluorescence-based PCA3 test on urinary sediments after digital rectal examination; a Dutch multicenter validation of the diagnostic performance. Clin Cancer Res 2007;13:939-43.
84. Hamid AR, Pfeiffer MJ, Verhaegh GW, et al. Aldo-keto reductase family 1 member C3 (AKR1C3) is a biomarker and therapeutic target for castration-resistant prostate cancer. Mol Med 2013;18:1449-55.
85. Taylor BS, Schultz N, Hieronymus H, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22.