Comprehensive study of gene and microRNA expression related to epithelial-mesenchymal transition in prostate cancer

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Katz, Betina ^a   Reis, Sabrina T ^a   Viana, Nayara I ^a   Morais, Denis R ^a   Moura, Caio M ^a   Dip, Nelson ^a   Silva, Iran A ^a   Iscaife, Alexandre ^a   Srougi, Miguel ^a   Leite, Katia R M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 183; MICRORNA 200; MICRORNA 200B; MICRORNA 203; MICRORNA 205; MICRORNA 21; MICRORNA 29B; MICRORNA 30A; MICRORNA 373; MICRORNA 495; MICRORNA 9; PROSTATE SPECIFIC ANTIGEN; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; CADHERIN; NUCLEAR PROTEIN; TUMOR MARKER; TWIST1 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CANCER GENETICS; CANCER GROWTH; CANCER LOCALIZATION; CANCER PATIENT; CANCER RECURRENCE; CANCER STAGING; CANCER SURVIVAL; CONTROLLED STUDY; DISEASE ACTIVITY; DU145 CELL LINE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE LOCATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GLEASON SCORE; HIGH RISK PATIENT; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LNCAP CELL LINE; MAJOR CLINICAL STUDY; MALE; METASTASIS POTENTIAL; MULTIGENE FAMILY; PC3 CELL LINE; PHENOTYPE; PREOPERATIVE EVALUATION; PRIMARY TUMOR; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROSTATECTOMY; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; RECURRENCE RISK; TWIST1 GENE; VIMENTIN GENE; BLOOD; DISEASE FREE SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PROSTATE TUMOR; REAL TIME POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; TUMOR CELL LINE; TUMOR RECURRENCE;

AGED; BIOMARKERS, TUMOR; CADHERINS; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; NUCLEAR PROTEINS; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; TWIST TRANSCRIPTION FACTOR; VIMENTIN;

EID: 84915823319     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113700     Document Type: Article

References (63)

1. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63: 11-30.
2. Quinn DI, Henshall SM, Haynes AM, Brenner PC, Kooner R, et al. (2001) Prognostic significance of pathologic features in localized prostate cancer treated with radical prostatectomy: implications for staging systems and predictive models. J Clin Oncol 19: 3692-3705.
3. Mackinnon AC, Yan BC, Joseph LJ, Al-Ahmadie HA (2009) Molecular biology underlying the clinical heterogeneity of prostate cancer: an update. Arch Pathol Lab Med 133: 1033-1040.
4. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
5. Huber MA, Kraut N, Beug H (2005) Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 17: 548-558.
6. Halbleib JM, Nelson WJ (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-3214.
7. Moreno-Bueno G, Cubillo E, Sarrio D, Peinado H, Rodriguez-Pinilla SM, et al. (2006) Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelial-mesenchymal transition. Cancer Res 66: 9543-9556.
8. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, et al. (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2: 84-89.
9. Tomita K, van Bokhoven A, van Leenders GJ, Ruijter ET, Jansen CF, et al. (2000) Cadherin switching in human prostate cancer progression. Cancer Res 60: 3650-3654.
10. Putzke AP, Ventura AP, Bailey AM, Akture C, Opoku-Ansah J, et al. (2011) Metastatic progression of prostate cancer and e-cadherin regulation by zeb1 and SRC family kinases. Am J Pathol 179: 400-410.
11. Graham TR, Zhau HE, Odero-Marah VA, Osunkoya AO, Kimbro KS, et al. (2008) Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 68: 2479-2488.
12. Behnsawy HM, Miyake H, Harada K, Fujisawa M (2013) Expression patterns of epithelial-mesenchymal transition markers in localized prostate cancer: significance in clinicopathological outcomes following radical prostatectomy. BJU Int 111: 30-37.
13. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
14. Bendoraite A, Knouf EC, Garg KS, Parkin RK, Kroh EM, et al. (2010) Regulation of miR-200 family microRNAs and ZEB transcription factors in ovarian cancer: evidence supporting a mesothelial-to-epithelial transition. Gynecol Oncol 116: 117-125.
15. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601.
16. Korpal M, Lee ES, Hu G, Kang Y (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283: 14910-14914.
17. Park SM, Gaur AB, Lengyel E, Peter ME (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907.
18. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, et al. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9: 582-589.
19. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, et al. (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68: 7846-7854.
20. Ru P, Steele R, Newhall P, Phillips NJ, Toth K, et al. (2012) miRNA-29b suppresses prostate cancer metastasis by regulating epithelial-mesenchymal transition signaling. Mol Cancer Ther 11: 1166-1173.
21. Zhang J, Zhang H, Liu J, Tu X, Zang Y, et al. (2012) miR-30 inhibits TGF-beta1-induced epithelial-to-mesenchymal transition in hepatocyte by targeting Snail1. Biochem Biophys Res Commun 417: 1100-1105.
22. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, et al. (2011) miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10: 4256-4271.
23. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, et al. (2013) MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 32: 296-306.
24. Epstein JI, Allsbrook WC, Jr., Amin MB, Egevad LL, Committee IG (2005) The 2005 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma. Am J Surg Pathol 29: 1228-1242.
25. Kong D, Li Y, Wang Z, Banerjee S, Ahmad A, et al. (2009) miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 27: 1712-1721.
26. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, et al. (2008) Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68: 6162-6170.
27. Paterson EL, Kolesnikoff N, Gregory PA, Bert AG, Khew-Goodall Y, et al. (2008) The microRNA-200 family regulates epithelial to mesenchymal transition. ScientificWorldJournal 8: 901-904.
28. Williams LV, Veliceasa D, Vinokour E, Volpert OV (2013) miR-200b inhibits prostate cancer EMT, growth and metastasis. PLoS One 8: e83991.
29. Kurashige J, Kamohara H, Watanabe M, Hiyoshi Y, Iwatsuki M, et al. (2012) MicroRNA-200b regulates cell proliferation, invasion, and migration by directly targeting ZEB2 in gastric carcinoma. Ann Surg Oncol 19 Suppl 3: S656-664.
30. Marchini S, Cavalieri D, Fruscio R, Calura E, Garavaglia D, et al. (2011) Association between miR-200c and the survival of patients with stage I epithelial ovarian cancer: a retrospective study of two independent tumour tissue collections. Lancet Oncol 12: 273-285.
31. Nam EJ, Yoon H, Kim SW, Kim H, Kim YT, et al. (2008) MicroRNA expression profiles in serous ovarian carcinoma. Clin Cancer Res 14: 2690-2695.
32. Hu X, Macdonald DM, Huettner PC, Feng Z, El Naqa IM, et al. (2009) A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer. Gynecol Oncol 114: 457-464.
33. Barron N, Keenan J, Gammell P, Martinez VG, Freeman A, et al. (2012) Biochemical relapse following radical prostatectomy and miR-200a levels in prostate cancer. Prostate 72: 1193-1199.
34. Vernon AE, LaBonne C (2004) Tumor metastasis: a new twist on epithelial-mesenchymal transitions. Curr Biol 14: R719-721.
35. Xu G, Wu J, Zhou L, Chen B, Sun Z, et al. (2010) Characterization of the small RNA transcriptomes of androgen dependent and independent prostate cancer cell line by deep sequencing. PLoS One 5: e15519.
36. Zhu ML, Kyprianou N (2010) Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J 24: 769-777.
37. Liu YN, Liu Y, Lee HJ, Hsu YH, Chen JH (2008) Activated androgen receptor downregulates E-cadherin gene expression and promotes tumor metastasis. Mol Cell Biol 28: 7096-7108.
38. Sun Y, Wang BE, Leong KG, Yue P, Li L, et al. (2012) Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy. Cancer Res 72: 527-536.
39. Hudson RS, Yi M, Esposito D, Watkins SK, Hurwitz AA, et al. (2012) MicroRNA-1 is a candidate tumor suppressor and prognostic marker in human prostate cancer. Nucleic Acids Res 40: 3689-3703.
40. Kojima S, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, et al. (2012) Tumour suppressors miR-1 and miR-133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br J Cancer 106: 405-413.
41. Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL, Tammela TL, et al. (2007) MicroRNA expression profiling in prostate cancer. Cancer Res 67: 6130-6135.
42. Carlsson J, Davidsson S, Helenius G, Karlsson M, Lubovac Z, et al. (2011) A miRNA expression signature that separates between normal and malignant prostate tissues. Cancer Cell Int 11: 14.
43. Kao CJ, Martiniez A, Shi XB, Yang J, Evans CP, et al. (2013) miR-30 as a tumor suppressor connects EGF/Src signal to ERG and EMT. Oncogene.
44. Kumarswamy R, Mudduluru G, Ceppi P, Muppala S, Kozlowski M, et al. (2012) MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int J Cancer 130: 2044-2053.
45. Cheng CW, Wang HW, Chang CW, Chu HW, Chen CY, et al. (2012) MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer. Breast Cancer Res Treat 134: 1081-1093.
46. Wang W, Lin H, Zhou L, Zhu Q, Gao S, et al. (2013) MicroRNA-30a-3p inhibits tumor proliferation, invasiveness and metastasis and is downregulated in hepatocellular carcinoma. Eur J Surg Oncol.
47. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939.
48. Kwok WK, Ling MT, Lee TW, Lau TC, Zhou C, et al. (2005) Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res 65: 5153-5162.
49. Yuen HF, Chua CW, Chan YP, Wong YC, Wang X, et al. (2007) Significance of TWIST and E-cadherin expression in the metastatic progression of prostatic cancer. Histopathology 50: 648-658.
50. Eide T, Ramberg H, Glackin C, Tindall D, Tasken KA (2013) TWIST1, A novel androgen-regulated gene, is a target for NKX3-1 in prostate cancer cells. Cancer Cell Int 13: 4.
51. Bethel CR, Faith D, Li X, Guan B, Hicks JL, et al. (2006) Decreased NKX3.1 protein expression in focal prostatic atrophy, prostatic intraepithelial neoplasia, and adenocarcinoma: association with gleason score and chromosome 8p deletion. Cancer Res 66: 10683-10690.
52. Iwata T, Schultz D, Hicks J, Hubbard GK, Mutton LN, et al. (2010) MYC overexpression induces prostatic intraepithelial neoplasia and loss of Nkx3.1 in mouse luminal epithelial cells. PLoS One 5: e9427.
53. Casas E, Kim J, Bendesky A, Ohno-Machado L, Wolfe CJ, et al. (2011) Snail2 is an essential mediator of Twist1-induced epithelial mesenchymal transition and metastasis. Cancer Res 71: 245-254.
54. Liu Y, Zhao J, Zhang PY, Zhang Y, Sun SY, et al. (2012) MicroRNA-10b targets E-cadherin and modulates breast cancer metastasis. Med Sci Monit 18: BR299-308.
55. Ma L, Teruya-Feldstein J, Weinberg RA (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688.
56. Ueno K, Hirata H, Shahryari V, Deng G, Tanaka Y, et al. (2013) microRNA-183 is an oncogene targeting Dkk-3 and SMAD4 in prostate cancer. Br J Cancer 108: 1659-1667.
57. Sarver AL, Li L, Subramanian S (2010) MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res 70: 9570-9580.
58. Weeraratne SD, Amani V, Teider N, Pierre-Francois J, Winter D, et al. (2012) Pleiotropic effects of miR-183, 96, 182 converge to regulate cell survival, proliferation and migration in medulloblastoma. Acta Neuropathol 123: 539-552.
59. Qu Y, Li WC, Hellem MR, Rostad K, Popa M, et al. (2013) MiR-182 and miR-203 induce mesenchymal to epithelial transition and self-sufficiency of growth signals via repressing SNAI2 in prostate cells. Int J Cancer 133: 544-555.
60. Li XL, Hara T, Choi Y, Subramanian M, Francis P, et al. (2014) A p21-ZEB1 complex inhibits epithelial-mesenchymal transition through the microRNA 183-96-182 cluster. Mol Cell Biol 34: 533-550.
61. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, et al. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495.
62. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, et al. (2010) Integrative genomic profiling of human prostate cancer. Cancer Cell 18: 11-22.
63. Ding Z, Wu CJ, Chu GC, Xiao Y, Ho D, et al. (2011) SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 470: 269-273.