miR-22 and miR-29a are members of the androgen receptor cistrome modulating LAMC1 and Mcl-1 in prostate cancer

Molecular Endocrinology

Volumn 29, Issue 7, 2015, Pages 1037-1054

  Pasqualini, Lorenza ^a   Bu, Huajie ^a,b   Puhr, Martin ^a   Narisu, Narisu ^c   Rainer, Johannes ^a,d   Schlick, Bettina ^a,e   Schäfer, Georg ^a,f   Angelova, Mihaela ^a   Trajanoski, Zlatko ^a   Börno, Stefan T ^g   Schweiger, Michal R ^g,h   Fuchsberger, Christian ^d,i   Klocker, Helmut ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d University of Lubeck   (Italy)

^e Oncotyrol Center for Personalized Cancer Medicine   (Austria)

^f MEDICAL UNIVERSITY OF INNSBRUCK   (Austria)

^g MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^h UNIVERSITY OF COLOGNE   (Germany)

ⁱ UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; LAMININ GAMMA1; MICRORNA 22; MICRORNA 29A; PROTEIN MCL 1; ANDROGEN; AR PROTEIN, HUMAN; LAMININ; MCL1 PROTEIN, HUMAN; MICRORNA; MIRN22 MICRORNA, HUMAN; MIRN29 MICRORNA, HUMAN;

ADVANCED CANCER; ARTICLE; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; EXPERIMENTAL MODEL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MALE; PRIMARY TUMOR; PRIORITY JOURNAL; PROSTATE CANCER; WILD TYPE; APOPTOSIS; BINDING SITE; CELL MOTION; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; PATHOLOGY; PROSTATE TUMOR; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANDROGENS; APOPTOSIS; BINDING SITES; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME; HUMANS; LAMININ; MALE; MICRORNAS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION;

EID: 84936119017     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1358     Document Type: Article

References (81)

1. Knudsen KE, Scher HI. Starving the addiction: new opportunities for durable suppression of AR signaling in prostate cancer. Clin Cancer Res. 2009;15(15):4792–4798.
2. Hodgson MC, Bowden WA, Agoulnik IU. Androgen receptor footprint on the way to prostate cancer progression. World J Urol. 2012;30(3):279–285.
3. Shen MM, Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev. 2010;24(18):1967–2000.
4. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer. 2001;1(1):34–45.
5. Waltering KK, Porkka KP, Jalava SE, et al. Androgen regulation of micro-RNAs in prostate cancer. Prostate. 2011;71(6):604–614.
6. Ribas J, Ni X, Haffner M, et al. miR-21: an androgen receptorregulated microRNA that promotes hormone-dependent and hormone- independent prostate cancer growth. Cancer Res. 2009; 69(18):7165–7169.
7. ChunJiao S, Huan C, ChaoYang X, GuoMei R. Uncovering the roles of miRNAs and their relationship with androgen receptor in prostate cancer. IUBMB Life. 2014;66(6):379–386.
8. Coppola V, De Maria R, Bonci D. MicroRNAs and prostate cancer. Endocr Relat Cancer. 2010;17(1):F1–F17.
9. Paone A, Galli R, Fabbri M. MicroRNAs as new characters in the plot between epigenetics and prostate cancer. Front Genet. 2011; 2:62.
10. Jerónimo C, Bastian PJ, Bjartell A, et al. Epigenetics in prostate cancer: biologic and clinical relevance. Eur Urol. 2011;60(4):753–766.
11. van Rooij E. The art of microRNA research. Circ Res. 2011;108(2): 219–234.
12. Chira P, Vareli K, Sainis I, Papandreou C, Briasoulis E. Alterations of MicroRNAs in solid cancers and their prognostic value. Cancers. 2010;2(2):1328–1353.
13. Gururajan M, Josson S, Chu GC, et al. miR-154* and miR-379 in the DLK1-DIO3 microRNA mega-cluster regulate epithelial to mesenchymal transition and bone metastasis of prostate cancer. Clin Cancer Res. 2014;20(24):6559–6569.
14. Josson S, Gururajan M, Hu P, et al. miR-409-3p/-5p promotes tumorigenesis, epithelial-to-mesenchymal transition, and bone metastasis of human prostate cancer. Clin Cancer Res. 2014;20(17): 4636–4646.
15. Di Leva G, Croce CM. Roles of small RNAs in tumor formation. Trends Mol Med. 2010;16(6):257–267.
16. Selth LA, Townley SL, Bert AG, et al. Circulating microRNAs predict biochemical recurrence in prostate cancer patients. Br J Cancer. 2013;109(3):641–650.
17. Schrauder MG, Strick R, Schulz-Wendtland R, et al. Circulating micro-RNAs as potential blood-based markers for early stage breast cancer detection. PLoS One. 2012;7(1):e29770.
18. Kim WT, Kim WJ. MicroRNAs in prostate cancer. Prostate Int. 2013;1(1):3–9.
19. Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL, Tammela TL, Visakorpi T. MicroRNA expression profiling in prostate cancer. Cancer Res. 2007;67(13):6130–6135.
20. Ozen M, Creighton CJ, Ozdemir M, Ittmann M. Widespread deregulation of microRNA expression in human prostate cancer. Oncogene. 2008;27(12):1788–1793.
21. Ambs S, Prueitt RL, Yi M, et al. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res. 2008;68(15):6162–6170.
22. DeVere White RW, Vinall RL, Tepper CG, Shi XB. MicroRNAs and their potential for translation in prostate cancer. Urol Oncol. 2009;27(3):307–311.
23. Tong AW, Fulgham P, Jay C, et al. MicroRNA profile analysis of human prostate cancers. Cancer Gene Ther. 2009;16(3):206–216.
24. Kogan I, Goldfinger N, Milyavsky M, et al. hTERT-immortalized prostate epithelial and stromal-derived cells: an authentic in vitro model for differentiation and carcinogenesis. Cancer Res. 2006; 66(7):3531–3540.
25. Madar S, Brosh R, Buganim Y, et al. Modulated expression of WFDC1 during carcinogenesis and cellular senescence. Carcinogenesis. 2009;30(1):20–27.
26. Wang Q, Carroll JS, Brown M. Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol Cell. 2005;19(5):631–642.
27. Bu H, Schweiger MR, Manke T, et al. Anterior gradient 2 and 3–two prototype androgen-responsive genes transcriptionally upregulated by androgens and by oestrogens in prostate cancer cells. FEBS J. 2013;280(5):1249–1266.
28. Cartharius K, Frech K, Grote K, et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics. 2005;21(13):2933–2942.
29. Martowicz A, Rainer J, Lelong J, Spizzo G, Gastl G, Untergasser G. EpCAM overexpression prolongs proliferative capacity of primary human breast epithelial cells and supports hyperplastic growth. Mol Cancer. 2013;12:56.
30. Hoefer J, Kern J, Ofer P, et al. SOCS2 correlates with malignancy and exerts growth-promoting effects in prostate cancer. Endocr Relat Cancer. 2014;21(2):175–187.
31. Rainer J, Lelong J, Bindreither D, et al. Research resource: transcriptional response to glucocorticoids in childhood acute lymphoblastic leukemia. Mol Endocrinol. 2012;26(1):178–193.
32. Jian Ye, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012;13(134).
33. Puhr M, Santer FR, Neuwirt H, et al. Down-regulation of suppressor of cytokine signaling-3 causes prostate cancer cell death through activation of the extrinsic and intrinsic apoptosis pathways. Cancer Res. 2009;69(18):7375–7384.
34. Bu H, Bormann S, Schäfer G, et al. The anterior gradient 2 (AGR2) gene is overexpressed in prostate cancer and may be useful as a urine sediment marker for prostate cancer detection. Prostate. 2011; 71(6):575–587.
35. Puhr M, Hoefer J, Schäfer G, et al. Epithelial-to-mesenchymal transition leads to docetaxel resistance in prostate cancer and is mediated by reduced expression of miR-200c and miR-205. Am J Pathol. 2012;181(6):2188–2201.
36. Börno ST, Fischer A, Kerick M, et al. Genome-wide DNA methylation events in TMPRSS2-ERG fusion-negative prostate cancers implicate an EZH2-dependent mechanism with miR-26a hypermethylation. Cancer Discov. 2012;2(11):1024–1035.
37. Leng N, Dawson JA, Thomson JA, et al. EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics. 2013;29(8):1035–1043.
38. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
39. Sun C, Dobi A, Mohamed A, Li H, et al. TMPRSS2-ERG fusion, a common genomic alteration in prostate cancer activates C-MYC and abrogates prostate epithelial differentiation. Oncogene. 2008; 27(40):5348–5353.
40. Cleutjens KB, van der Korput HA, van Eekelen CC, van Rooij HC, Faber PW, Trapman J. An androgen response element in a far upstream enhancer region is essential for high, androgen-regulated activity of the prostate-specific antigen promoter. Mol Endocrinol. 1997;11(2):148–161.
41. Makkonen H, Kauhanen M, Paakinaho V, Jääskeläinen T, Palvimo JJ. Long-range activation of FKBP51 transcription by the androgen receptor via distal intronic enhancers. Nucleic Acids Res. 2009; 37(12):4135–4148.
42. Prescott J, Jariwala U, Jia L, et al. Androgen receptor-mediated repression of novel target genes. Prostate. 2007;67(13):1371–1383.
43. Massie CE, Lynch A, Ramos-Montoya A, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011;30(13):2719–2733.
44. Chen Y, Clegg NJ, Scher HI. Antiandrogens and androgen depleting therapies in prostate cancer: new agents for an established target. Lancet Oncol. 2009;10(10):981–991.
45. Cancer Genome Atlas Research Network, Weinstein JN, Collisson EA, Mills GB, et al. The cancer genome atlas pan-cancer analysis project. Nat Genet. 2013;45(10):1113–1120.
46. Zhou Y, Bolton EC, Jones JO. Androgens and androgen receptor signaling in prostate tumorigenesis. J Mol Endocrinol. 2015;54(1): R15–R29.
47. Li Y, Kong D, Ahmad A, Bao B, Dyson G, Sarkar FH. Epigenetic deregulation of miR-29a and miR-1256 by isoflavone contributes to the inhibition of prostate cancer cell growth and invasion. Epigenetics. 2012;7(8):940–949.
48. Givant-Horwitz V, Davidson B, Reich R. Laminin-induced signaling in tumor cells. Cancer Lett. 2005;223(1):1–10.
49. Hamilton MP, Rajapakshe K, Hartig SM, et al. Identification of a pan-cancer oncogenic microRNA superfamily anchored by a central core seed motif. Nat Commun. 2013;4:2730.
50. Chen ZL, Haegeli V, Yu H, Strickland S. Cortical deficiency of laminin _1 impairs the AKT/GSK-3_ signaling pathway and leads to defects in neurite outgrowth and neuronal migration. Dev Biol. 2009;327(1):158–168.
51. Song L, Coppola D, Livingston S, Cress D, Haura EB. Mcl-1 regulates survival and sensitivity to diverse apoptotic stimuli in human non-small cell lung cancer cells. Cancer Biol Ther. 2005;4(3):267–276.
52. Quinn BA, Dash R, Azab B, et al. Targeting Mcl-1 for the therapy of cancer. Expert Opin Investig Drugs. 2011;20(10):1397–1411.
53. Jackson RS 2nd, Placzek W, Fernandez A, et al. Sabutoclax, a Mcl-1 antagonist, inhibits tumorigenesis in transgenic mouse and human xenograft models of prostate cancer. Neoplasia. 2012;14(7):656–665.
54. Son JK, Varadarajan S, Bratton SB. TRAIL-activated stress kinases suppress apoptosis through transcriptional upregulation of MCL- 1. Cell Death Differ. 2010;17(8):1288–1301.
55. Yancey D, Nelson KC, Baiz D, et al. BAD dephosphorylation and decreased expression of MCL-1 induce rapid apoptosis in prostate cancer cells. PLoS One. 2013;8(9):e74561.
56. Ottman R, Nguyen C, Lorch R, Chakrabarti R. MicroRNA expressions associated with progression of prostate cancer cells to antiandrogen therapy resistance. Mol Cancer. 2014;13(1).
57. Jalava SE, Urbanucci A, Latonen L, et al. Androgen-regulated miR-32 targets BTG2 and is overexpressed in castration-resistant prostate cancer. Oncogene. 2012;31(41):4460–4471.
58. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell. 2008;133(2):217–222.
59. Patel JB, Appaiah HN, Burnett RM, et al. Control of EVI-1 oncogene expression in metastatic breast cancer cells through microRNA miR- 22. Oncogene. 2011;30(11):1290–1301.
60. Tan G, Shi Y, Wu ZH. MicroRNA-22 promotes cell survival upon UV radiation by repressing PTEN. Biochem Biophys Res Commun. 2012;417(1):546–551.
61. Cui Y, Su WY, Xing J, et al. MiR-29a inhibits cell proliferation and induces cell cycle arrest through the downregulation of p42.3 in human gastric cancer. PLoS One. 2011;6(10):e25872.
62. Gebeshuber CA, Zatloukal K, Martinez J. miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep. 2009;10(4):400–405.
63. Olive V, Bennett MJ, Walker JC, et al. miR-19 is a key oncogenic component of mir-17- 92. Genes Dev. 2009;23(24):2839–2849.
64. Hwang HW, Wentzel EA, Mendell JT. Cell-cell contact globally activates microRNA biogenesis. Proc Natl Acad Sci USA. 2009; 106(17):7016–7021.
65. Musumeci M, Coppola V, Addario A, et al. Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene. 2011;30(41):4231–4242.
66. Gu L, Frommel SC, Oakes CC, et al. BAZ2A (TIP5) is involved in epigenetic alterations in prostate cancer and its overexpression predicts disease recurrence. Nat Genet. 2015;47(1):22–30.
67. Mori M, Triboulet R, Mohseni M, et al. Hippo signaling regulates microprocessor and links cell-density-dependent miRNA biogenesis to cancer. Cell. 2014;156(5):893–906.
68. Schaefer A, Jung M, Miller K, et al. Suitable reference genes for relative quantification of miRNA expression in prostate cancer. Exp Mol Med. 2010;42(11):749.
69. Mott JL, Kobayashi S, Bronk SF, Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene. 2007;26(42):6133–6140.
70. Nishikawa R, Goto Y, Kojima S, et al. Tumor-suppressive microRNA- 29s inhibit cancer cell migration and invasion via targeting LAMC1 in prostate cancer. Int J Oncol. 2014;45(1):401–410.
71. Smyth N, Vatansever HS, Murray P, et al. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol. 1999;144(1):151–160.
72. Piovan C, Palmieri D, Di Leva G, et al. Oncosuppressive role of p53-induced miR-205 in triple negative breast cancer. Mol Oncol. 2012;6(4):458–472.
73. Sprenger CC, Drivdahl RH, Woodke LB, et al. Senescence-induced alterations of laminin chain expression modulate tumorigenicity of prostate cancer cells. Neoplasia. 2008;10(12):1350–1361.
74. Wuillème-Toumi S, Robillard N, Gomez P, et al. Mcl-1 is overexpressed in multiple myeloma and associated with relapse and shorter survival. Leukemia. 2005;19(7):1248–1252.
75. Boiani M, Daniel C, Liu X, Hogarty MD, Marnett LJ. The stress protein BAG3 stabilizes Mcl-1 protein and promotes survival of cancer cells and resistance to antagonist ABT-737. J Biol Chem. 2013;288(10):6980–6990.
76. Adler HL, McCurdy MA, Kattan MW, Timme TL, Scardino PT, Thompson TC. Elevated levels of circulating interleukin-6 and transforming growth factor-_ 1 in patients with metastatic prostatic carcinoma. J Urol. 1999;161(1):182–187.
77. Cavarretta IT, Neuwirt H, Untergasser G, et al. The antiapoptotic effect of IL-6 autocrine loop in a cellular model of advanced prostate cancer is mediated by Mcl-1. Oncogene. 2007;26(20):2822–2832.
78. Santer FR, Erb HH, Oh SJ, et al. Mechanistic rationale for MCL1 inhibition during androgen deprivation therapy. Oncotarget. 2015; 6(8):6105–6122.
79. Koehler BC, Scherr AL, Lorenz S, et al. Beyond cell death - antiapoptotic Bcl-2 proteins regulate migration and invasion of colorectal cancer cells in vitro. PLoS One. 2013;8(10):e76446.
80. Kroiss A, Vincent S, Decaussin-Petrucci M, et al. Androgen-regulated microRNA-135a decreases prostate cancer cell migration and invasion through downregulating ROCK1 and ROCK 2. Oncogene. 2015;34(22):2846–2855.
81. Williams LV, Veliceasa D, Vinokour E, Volpert OV. miR-200b inhibits prostate cancer EMT, growth and metastasis. PLoS One. 2013;8(12):e83991.