Loss of androgen-regulated MicroRNA 1 activates SRC and promotes prostate cancer bone metastasis

Molecular and Cellular Biology

Volumn 35, Issue 11, 2015, Pages 1940-1951

  Liu, Yen Nien ^a   Yin, JuanJuan ^b   Barrett, Ben ^b   Sheppard Tillman, Heather ^b   Li, Dongmei ^c   Casey, Orla M ^b   Fang, Lei ^b   Hynes, Paul G ^b   Ameri, Amir H ^b   Kelly, Kathleen ^b  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; MICRORNA 1; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR ZEB1; ANDROGEN; MICRORNA; MIRN1 MICRORNA, HUMAN; PROTEIN TYROSINE KINASE;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BONE METASTASIS; CANCER GROWTH; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DISTANT METASTASIS; DOWN REGULATION; ENZYME ACTIVITY; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LNCAP CELL LINE; MALE; MORBIDITY; MOUSE; NONHUMAN; ONCOGENE SRC; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; TUMOR INVASION; UPREGULATION; ANIMAL; BONE TUMOR; CASTRATION RESISTANT PROSTATE CANCER; GENE EXPRESSION REGULATION; GENETICS; NUDE MOUSE; PATHOLOGY; SECONDARY; TUMOR CELL LINE;

ANDROGENS; ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, NUDE; MICRORNAS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84929399755     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00008-15     Document Type: Article

References (46)

1. Roudier MP, True LD, Higano CS, Vesselle H, Ellis W, Lange P, Vessella RL. 2003. Phenotypic heterogeneity of end-stage prostate carcinoma metastatic to bone. Hum Pathol 34:646-653. http://dx.doi.org/10.1016/S0046-8177(03)00190-4.
2. 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. 2004. Androgen-independent prostate cancer is a heterogeneous group of diseases: lessons from a rapid autopsy program. Cancer Res 64:9209-9216. http://dx.doi.org/10.1158/0008-5472.CAN-04-2442.
3. Scher HI, Sawyers CL. 2005. Biology of progressive, castration-resistant prostate cancer: directed therapies targeting the androgen-receptor signaling axis. J Clin Oncol 23:8253-8261. http://dx.doi.org/10.1200/JCO.2005.03.4777.
4. Zong Y, Goldstein AS. 2013. Adaptation or selection-mechanisms of castration-resistant prostate cancer. Nat Rev Urol 10:90-98. http://dx.doi.org/10.1038/nrurol.2012.237.
5. Mendiratta P, Mostaghel E, Guinney J, Tewari AK, Porrello A, Barry WT, Nelson PS, Febbo PG. 2009. Genomic strategy for targeting therapy in castration-resistant prostate cancer. J Clin Oncol 27:2022-2029. http://dx.doi.org/10.1200/JCO.2008.17.2882.
6. Sharma NL, Massie CE, Ramos-Montoya A, Zecchini V, Scott HE, Lamb AD, MacArthur S, Stark R, Warren AY, Mills IG, Neal DE. 2013. The androgen receptor induces a distinct transcriptional program in castration-resistant prostate cancer in man. Cancer Cell 23:35-47. http://dx.doi.org/10.1016/j.ccr.2012.11.010.
7. Tomlins SA, Mehra R, Rhodes DR, Cao X, Wang L, Dhanasekaran SM, Kalyana-Sundaram S, Wei JT, Rubin MA, Pienta KJ, Shah RB, Chinnaiyan AM. 2007. Integrative molecular concept modeling of prostate cancer progression. Nat Genet 39:41-51. http://dx.doi.org/10.1038/ng1935.
8. Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J, Chen Z, Beroukhim R, Wang H, Lupien M, Wu T, Regan MM, Meyer CA, Carroll JS, Manrai AK, Janne OA, Balk SP, Mehra R, Han B, Chinnaiyan AM, Rubin MA, True L, Fiorentino M, Fiore C, Loda M, Kantoff PW, Liu XS, Brown M. 2009. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138:245-256. http://dx.doi.org/10.1016/j.cell.2009.04.056.
9. Maugeri-Sacca M, Coppola V, De Maria R, Bonci D. 2013. Functional role of microRNAs in prostate cancer and therapeutic opportunities. Crit Rev Oncog 18:303-315. http://dx.doi.org/10.1615/CritRevOncog.2013007206.
10. Wang XD, Reeves K, Luo FR, Xu LA, Lee F, Clark E, Huang F. 2007. Identification of candidate predictive and surrogate molecular markers for dasatinib in prostate cancer: rationale for patient selection and efficacy monitoring. Genome Biol 8:R255. http://dx.doi.org/10.1186/gb-2007-8-11-r255.
11. Guo Z, Dai B, Jiang T, Xu K, Xie Y, Kim O, Nesheiwat I, Kong X, Melamed J, Handratta VD, Njar VC, Brodie AM, Yu LR, Veenstra TD, Chen H, Qiu Y. 2006. Regulation of androgen receptor activity by tyrosine phosphorylation. Cancer Cell 10:309-319. http://dx.doi.org/10.1016/j.ccr.2006.08.021.
12. Yeatman TJ. 2004. A renaissance for SRC. Nat Rev Cancer 4:470-480. http://dx.doi.org/10.1038/nrc1366.
13. Bromann PA, Korkaya H, Courtneidge SA. 2004. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23:7957-7968. http://dx.doi.org/10.1038/sj.onc.1208079.
14. Tatarov O, Mitchell TJ, Seywright M, Leung HY, Brunton VG, Edwards J. 2009. SRC family kinase activity is up-regulated in hormone-refractory prostate cancer. Clin Cancer Res 15:3540-3549. http://dx.doi.org/10.1158/1078-0432.CCR-08-1857.
15. Tatarov O, Edwards J. 2007. The role of SRC family kinases in prostate cancer. Transl Oncogenomics 2:67-77.
16. Liu Y, Karaca M, Zhang Z, Gioeli D, Earp HS, Whang YE. 2010. Dasatinib inhibits site-specific tyrosine phosphorylation of androgen receptor by Ack1 and Src kinases. Oncogene 29:3208-3216. http://dx.doi.org/10.1038/onc.2010.103.
17. Carver BS, Chapinski C, Wongvipat J, Hieronymus H, Chen Y, Chandarlapaty S, Arora VK, Le C, Koutcher J, Scher H, Scardino PT, Rosen N, Sawyers CL. 2011. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 19:575-586. http://dx.doi.org/10.1016/j.ccr.2011.04.008.
18. Kinkade CW, Castillo-Martin M, Puzio-Kuter A, Yan J, Foster TH, Gao H, Sun Y, Ouyang X, Gerald WL, Cordon-Cardo C, Abate-Shen C. 2008. Targeting AKT/mTOR and ERK MAPK signaling inhibits hormone-refractory prostate cancer in a preclinical mouse model. J Clin Invest 118:3051-3064. http://dx.doi.org/10.1172/JCI34764.
19. Mulholland DJ, Tran LM, Li Y, Cai H, Morim A, Wang S, Plaisier S, Garraway IP, Huang J, Graeber TG, Wu H. 2011. Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 19:792-804. http://dx.doi.org/10.1016/j.ccr.2011.05.006.
20. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L, Yi M, Stephens RM, Seng V, Sheppard-Tillman H, Martin P, Kelly K. 2013. MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 32:296-306. http://dx.doi.org/10.1038/onc.2012.58.
21. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, Croce CM. 2008. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68:6162-6170. http://dx.doi.org/10.1158/0008-5472.CAN-08-0144.
22. Hudson RS, Yi M, Esposito D, Watkins SK, Hurwitz AA, Yfantis HG, Lee DH, Borin JF, Naslund MJ, Alexander RB, Dorsey TH, Stephens RM, Croce CM, Ambs S. 2012. MicroRNA-1 is a candidate tumor suppressor and prognostic marker in human prostate cancer. Nucleic Acids Res 40:3689-3703. http://dx.doi.org/10.1093/nar/gkr1222.
23. Martens-Uzunova ES, Jalava SE, Dits NF, van Leenders GJ, Moller S, Trapman J, Bangma CH, Litman T, Visakorpi T, Jenster G. 2012. Diagnostic and prognostic signatures from the small non-coding RNA transcriptome in prostate cancer. Oncogene 31:978-991. http://dx.doi.org/10.1038/onc.2011.304.
24. Yin J, Pollock C, Tracy K, Chock M, Martin P, Oberst M, Kelly K. 2007. Activation of the RalGEF/Ral pathway promotes prostate cancer metastasis to bone. Mol Cell Biol 27:7538-7550. http://dx.doi.org/10.1128/MCB.00955-07.
25. Yin JJ, Zhang L, Munasinghe J, Linnoila RI, Kelly K. 2010. Cediranib/AZD2171 inhibits bone and brain metastasis in a preclinical model of advanced prostate cancer. Cancer Res 70:8662-8673. http://dx.doi.org/10.1158/0008-5472.CAN-10-1435.
26. Gumerlock PH, Poonamallee UR, Meyers FJ, DeVere White RW. 1991. Activated ras alleles in human carcinoma of the prostate are rare. Cancer Res 51:1632-1637.
27. Wang XS, Shankar S, Dhanasekaran SM, Ateeq B, Sasaki AT, Jing X, Robinson D, Cao Q, Prensner JR, Yocum AK, Wang R, Fries DF, Han B, Asangani IA, Cao X, Li Y, Omenn GS, Pflueger D, Gopalan A, Reuter VE, Kahoud ER, Cantley LC, Rubin MA, Palanisamy N, Varambally S, Chinnaiyan AM. 2011. Characterization of KRAS rearrangements in metastatic prostate cancer. Cancer Discov 1:35-43. http://dx.doi.org/10.1158/2159-8274.CD-10-0022.
28. Aytes A, Mitrofanova A, Kinkade CW, Lefebvre C, Lei M, Phelan V, LeKaye HC, Koutcher JA, Cardiff RD, Califano A, Shen MM, Abate-Shen C. 2013. ETV4 promotes metastasis in response to activation of PI3-kinase and Ras signaling in a mouse model of advanced prostate cancer. Proc Natl Acad Sci U S A 110:E3506-E3515. http://dx.doi.org/10.1073/pnas.1303558110.
29. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, Socci ND, Lash AE, Heguy A, Eastham JA, Scher HI, Reuter VE, Scardino PT, Sander C, Sawyers CL, Gerald WL. 2010. Integrative genomic profiling of human prostate cancer. Cancer Cell 18:11-22. http://dx.doi.org/10.1016/j.ccr.2010.05.026.
30. Mulholland DJ, Kobayashi N, Ruscetti M, Zhi A, Tran LM, Huang J, Gleave M, Wu H. 2012. Pten loss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate cancer stem/progenitor cells. Cancer Res 72:1878-1889. http://dx.doi.org/10.1158/0008-5472.CAN-11-3132.
31. Day CP, Carter J, Bonomi C, Esposito D, Crise B, Ortiz-Conde B, Hollingshead M, Merlino G. 2009. Lentivirus-mediated bifunctional cell labeling for in vivo melanoma study. Pigment Cell Melanoma Res 22:283-295. http://dx.doi.org/10.1111/j.1755-148X.2009.00545.x.
32. Liu YN, Abou-Kheir W, Yin JJ, Fang L, Hynes P, Casey O, Hu D, Wan Y, Seng V, Sheppard-Tillman H, Martin P, Kelly K. 2012. Critical and reciprocal regulation of KLF4 and SLUG in transforming growth factor beta-initiated prostate cancer epithelial-mesenchymal transition. Mol Cell Biol 32:941-953. http://dx.doi.org/10.1128/MCB.06306-11.
33. Hieronymus H, Lamb J, Ross KN, Peng XP, Clement C, Rodina A, Nieto M, Du J, Stegmaier K, Raj SM, Maloney KN, Clardy J, Hahn WC, Chiosis G, Golub TR. 2006. Gene expression signature-based chemical genomic prediction identifies a novel class of HSP90 pathway modulators. Cancer Cell 10:321-330. http://dx.doi.org/10.1016/j.ccr.2006.09.005.
34. Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, Olson JA, Jr, Marks JR, Dressman HK, West M, Nevins JR. 2006. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 439:353-357. http://dx.doi.org/10.1038/nature04296.
35. Katz B, Reis ST, Viana NI, Morais DR, Moura CM, Dip N, Silva IA, Iscaife A, Srougi M, Leite KR. 2014. Comprehensive study of gene and microRNA expression related to epithelial-mesenchymal transition in prostate cancer. PLoS One 9:e113700. http://dx.doi.org/10.1371/journal.pone.0113700.
36. Araujo J, Logothetis C. 2009. Targeting Src signaling in metastatic bone disease. Int J Cancer 124:1-6. http://dx.doi.org/10.1002/ijc.23998.
37. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R, Rosenfeld MG, Sawyers CL. 2004. Molecular determinants of resistance to antiandrogen therapy. Nat Med 10:33-39. http://dx.doi.org/10.1038/nm972.
38. Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, Majumder S, Liu CG, Volinia S, Croce CM, Schmittgen TD, Ghoshal K, Jacob ST. 2008. Methylation mediated silencing of microRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res 68:5049-5058. http://dx.doi.org/10.1158/0008-5472.CAN-07-6655.
39. Leone V, D'Angelo D, Rubio I, de Freitas PM, Federico A, Colamaio M, Pallante P, Medeiros-Neto G, Fusco A. 2011. MiR-1 is a tumor suppressor in thyroid carcinogenesis targeting CCND2, CXCR4, and SDF-1alpha. J Clin Endocrinol Metab 96:E1388-E1398. http://dx.doi.org/10.1210/jc.2011-0345.
40. Navon R, Wang H, Steinfeld I, Tsalenko A, Ben-Dor A, Yakhini Z. 2009. Novel rank-based statistical methods reveal microRNAs with differential expression in multiple cancer types. PLoS One 4:e8003. http://dx.doi.org/10.1371/journal.pone.0008003.
41. Majid S, Dar AA, Saini S, Arora S, Shahryari V, Zaman MS, Chang I, Yamamura S, Tanaka Y, Deng G, Dahiya R. 2012. miR-23b represses proto-oncogene Src kinase and functions as methylation-silenced tumor suppressor with diagnostic and prognostic significance in prostate cancer. Cancer Res 72:6435-6446. http://dx.doi.org/10.1158/0008-5472.CAN-12-2181.
42. Zhang XH, Jin X, Malladi S, Zou Y, Wen YH, Brogi E, Smid M, Foekens JA, Massague J. 2013. Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma. Cell 154:1060-1073. http://dx.doi.org/10.1016/j.cell.2013.07.036.
43. Mukherji D, Eichholz A, De Bono JS. 2012. Management of metastatic castration-resistant prostate cancer: recent advances. Drugs 72:1011-1028. http://dx.doi.org/10.2165/11633360-000000000-00000.
44. Saylor PJ, Armstrong AJ, Fizazi K, Freedland S, Saad F, Smith MR, Tombal B, Pienta K. 2013. New and emerging therapies for bone metastases in genitourinary cancers. Eur Urol 63:309-320. http://dx.doi.org/10.1016/j.eururo.2012.10.007.
45. Montero JC, Seoane S, Ocana A, Pandiella A. 2011. Inhibition of SRC family kinases and receptor tyrosine kinases by dasatinib: possible combinations in solid tumors. Clin Cancer Res 17:5546-5552. http://dx.doi.org/10.1158/1078-0432.CCR-10-2616.
46. Araujo JC, Trudel GC, Saad F, Armstrong AJ, Yu EY, Bellmunt J, Wilding G, McCaffrey J, Serrano SV, Matveev VB, Efstathiou E, Oudard S, Morris MJ, Sizer B, Goebell PJ, Heidenreich A, de Bono JS, Begbie S, Hong JH, Richardet E, Gallardo E, Paliwal P, Durham S, Cheng S, Logothetis CJ. 2013. Docetaxel and dasatinib or placebo in men with metastatic castration-resistant prostate cancer (READY): a randomised, double-blind phase 3 trial. Lancet Oncol 14:1307-0316. http://dx.doi.org/10.1016/S1470-2045(13)70479-0.