Retinoic acid and androgen receptors combine to achieve tissue specific control of human prostatic transglutaminase expression: A novel regulatory network with broader significance

Nucleic Acids Research

Volumn 40, Issue 11, 2012, Pages 4825-4840

  Rivera Gonzalez, Guillermo C ^a   Droop, Alastair P ^a   Rippon, Helen J ^a   Tiemann, Katrin ^a   Pellacani, Davide ^a   Georgopoulos, Lindsay J ^a   Maitland, Norman J ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RETINOIC ACID; RETINOIC ACID RECEPTOR GAMMA;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; BTG1 GENE; CDCA7L GENE; CDK6 GENE; CONTROLLED STUDY; ENZYME REGULATION; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MAPPING; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; HORMONE ACTION; HORMONE RECEPTOR INTERACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SAMD3 GENE; TGM4 GENE; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANDROGENS; CELL LINE, TUMOR; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE REGULATORY NETWORKS; HUMANS; MALE; METRIBOLONE; PROMOTER REGIONS, GENETIC; PROSTATE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; RECEPTORS, RETINOIC ACID; TRANSCRIPTIONAL ACTIVATION; TRANSGLUTAMINASES; TRETINOIN;

EID: 84862222054     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks143     Document Type: Article

References (65)

1. Gudas, L.J. (1994) Retinoids and vertebrate development. J. Biol. Chem., 269, 15399-15402. (Pubitemid 24202115)
2. Dupe, V., Davenne, M., Brocard, J., Dolle, P., Mark, M., Dierich, A., Chambon, P. and Rijli, F.M. (1997) In vivo functional analysis of the Hoxa-1 3' retinoic acid response element (3'RARE). Development, 124, 399-410. (Pubitemid 27101674)
3. Kashyap, V., Gudas, L.J., Brenet, F., Funk, P., Viale, A. and Scandura, J.M. (2011) Epigenomic reorganization of the clustered Hox genes in embryonic stem cells induced by retinoic acid. J. Biol. Chem., 286, 3250-3260.
4. Akam, M. (1998) Hox genes in arthropod development and evolution. Biol. Bull., 195, 373-374. (Pubitemid 29049799)
5. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell, 78, 191-201. (Pubitemid 24241088)
6. Kastner, P., Mark, M., Ghyselinck, N., Krezel, W., Dupe, V., Grondona, J.M. and Chambon, P. (1997) Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development, 124, 313-326. (Pubitemid 27101666)
7. Dilworth, F.J. and Chambon, P. (2001) Nuclear receptors coordinate the activities of chromatin remodeling complexes and coactivators to facilitate initiation of transcription. Oncogene, 20, 3047-3054. (Pubitemid 32553559)
8. Bastien, J. and Rochette-Egly, C. (2004) Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene, 328, 1-16. (Pubitemid 38352876)
9. Rochette-Egly, C. and Chambon, P. (2001) F9 embryocarcinoma cells: a cell autonomous model to study the functional selectivity of RARs and RXRs in retinoid signaling. Histol. Histopathol., 16, 909-922. (Pubitemid 32700401)
10. Park, D.J., Chumakov, A.M., Vuong, P.T., Chih, D.Y., Gombart, A.F., Miller, W.H. Jr and Koeffler, H.P. (1999) CCAAT/enhancer binding protein epsilon is a potential retinoid target gene in acute promyelocytic leukemia treatment. J. Clin. Invest., 103, 1399-1408. (Pubitemid 29535496)
11. Donato, L.J., Suh, J.H. and Noy, N. (2007) Suppression of mammary carcinoma cell growth by retinoic acid: the cell cycle control gene Btg2 is a direct target for retinoic acid receptor signaling. Cancer Res., 67, 609-615. (Pubitemid 46192199)
12. Altucci, L., Rossin, A., Raffelsberger, W., Reitmair, A., Chomienne, C. and Gronemeyer, H. (2001) Retinoic acid-induced apoptosis in leukemia cells is mediated by paracrine action of tumor-selective death ligand TRAIL. Nat. Med., 7, 680-686. (Pubitemid 32588023)
13. Kellokumpu-Lehtinen, P., Santti, R.S. and Pelliniemi, L.J. (1981) Development of human fetal prostate in culture. Urol. Res., 9, 89-98. (Pubitemid 11155986)
14. Cunha, G.R. and Lung, B. (1978) The possible influence of temporal factors in androgenic responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice. J. Exp. Zool., 205, 181-193.
15. Seo, R., McGuire, M., Chung, M. and Bushman, W. (1997) Inhibition of prostate ductal morphogenesis by retinoic acid. J. Urol., 158, 931-935.
16. Peehl, D.M., Wong, S.T. and Stamey, T.A. (1993) Vitamin A regulates proliferation and differentiation of human prostatic epithelial cells. Prostate, 23, 69-78. (Pubitemid 23250086)
17. Lohnes, D., Mark, M., Mendelsohn, C., Dolle, P., Decimo, D., LeMeur, M., Dierich, A., Gorry, P. and Chambon, P. (1995) Developmental roles of the retinoic acid receptors. J. Steroid Biochem. Mol. Biol., 53, 475-486.
18. Stein, G.S., Zaidi, S.K., Stein, J.L., Lian, J.B., Van Wijnen, A.J., Montecino, M., Young, D.W., Javed, A., Pratap, J., Choi, J.Y. et al. (2009) Transcription-factor-mediated epigenetic control of cell fate and lineage commitment. Biochemistry and Cell Biology=Biochimie et Biologie Cellulaire, 87, 1-6.
19. Yu, Y., Xu, T., Hao, P. and Li, X. (2010) Association of tissue lineage and gene expression: conservatively and differentially expressed genes define common and special functions of tissues. BMC Bioinformatics, 11(Suppl 11), S1.
20. Cheng, W.S., Giandomenico, V., Pastan, I. and Essand, M. (2003) Characterization of the androgen-regulated prostate-specific T cell receptor gamma-chain alternate reading frame protein (TARP) promoter. Endocrinology, 144, 3433-3440. (Pubitemid 36904419)
21. Dubbink, H.J., Verkaik, N.S., Faber, P.W., Trapman, J., Schroder, F.H. and Romijn, J.C. (1996) Tissue specific and androgen-regulated expression of human prostate-specific transglutaminase. Biochem. J., 315(Pt 3), 901-908. (Pubitemid 26147620)
22. Cleutjens, K.B., Van der Korput, H.A., Van Eekelen, C.C., Van Rooij, H.C., Faber, P.W. and Trapman, J. (1997) 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., 11, 148-161. (Pubitemid 27057428)
23. Prescott, J.L., Blok, L. and Tindall, D.J. (1998) Isolation and androgen regulation of the human homeobox cDNA, NKX3.1. Prostate, 35, 71-80. (Pubitemid 28158640)
24. Watt, F., Martorana, A., Brookes, D.E., Ho, T., Kingsley, E., O'Keefe, D.S., Russell, P.J., Heston, W.D. and Molloy, P.L. (2001) A tissue-specific enhancer of the prostate-specific membrane antigen gene, FOLH1. Genomics, 73, 243-254. (Pubitemid 32463720)
25. Seitz, J., Keppler, C., Rausch, U. and Aumuller, G. (1990) Immunohistochemistry of secretory transglutaminase from rodent prostate. Histochemistry, 93, 525-530. (Pubitemid 20069766)
26. Cukierski, M.A., Sina, J.L., Prahalada, S. and Robertson, R.T. (1991) Effects of seminal vesicle and coagulating gland ablation on fertility in rats. Reprod. Toxicol., 5, 347-352.
27. Mukherjee, D.C., Agrawal, A.K., Manjunath, R. and Mukherjee, A.B. (1983) Suppression of epididymal sperm antigenicity in the rabbit by uteroglobin and transglutaminase in vitro. Science, 219, 989-991. (Pubitemid 13189534)
28. Davies, G., Ablin, R.J., Mason, M.D. and Jiang, W.G. (2007) Expression of the prostate transglutaminase (TGase-4) in prostate cancer cells and its impact on the invasiveness of prostate cancer. J. Exp. Ther. Oncol., 6, 257-264. (Pubitemid 46789726)
29. Dubbink, H.J., Cleutjens, K.B., Van der Korput, H.A., Trapman, J. and Romijn, J.C. (1999) An Sp1 binding site is essential for basal activity of the human prostate-specific transglutaminase gene (TGM4) promoter. Gene, 240, 261-267.
30. Thomas, M.A., Hodgson, M.C., Loermans, S.D., Hooper, J., Endersby, R. and Bentel, J.M. (2006) Transcriptional regulation of the homeobox gene NKX3.1 by all-trans retinoic acid in prostate cancer cells. J. Cell Biochem., 99, 1409-1419.
31. Jiang, A.L., Zhang, P.J., Chen, W.W., Liu, W.W., Yu, C.X., Hu, X.Y., Zhang, X.Q. and Zhang, J.Y. (2006) Effects of 9-cis retinoic acid on human homeobox gene NKX3.1 expression in prostate cancer cell line LNCaP. Asian J. Androl., 8, 435-441.
32. Cussenot, O., Berthon, P., Berger, R., Mowszowicz, I., Faille, A., Hojman, F., Teillac, P., Le Duc, A. and Calvo, F. (1991) Immortalization of human adult normal prostatic epithelial cells by liposomes containing large T-SV40 gene. J. Urol., 146, 881-886.
33. Massie, C.E., Lynch, A., Ramos-Montoya, A., Boren, J., Stark, R., Fazli, L., Warren, A., Scott, H., Madhu, B., Sharma, N. et al. (2011) The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J., 30, 2719-2733.
34. Barbosa-Morais, N.L., Dunning, M.J., Samarajiwa, S.A., Darot, J.F., Ritchie, M.E., Lynch, A.G. and Tavare, S. (2010) A re-annotation pipeline for Illumina BeadArrays: improving the interpretation of gene expression data. Nucleic Acids Res., 38, e17.
35. Ross-Innes, C.S., Stark, R., Holmes, K.A., Schmidt, D., Spyrou, C., Russell, R., Massie, C.E., Vowler, S.L., Eldridge, M. and Carroll, J.S. (2010) Cooperative interaction between retinoic acid receptor-alpha and estrogen receptor in breast cancer. Genes Dev., 24, 171-182.
36. Hua, S., Kittler, R. and White, K.P. (2009) Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Cell, 137, 1259-1271.
37. Yu, J., Mani, R.S., Cao, Q., Brenner, C.J., Cao, X., Wang, X., Wu, L., Li, J., Hu, M., Gong, Y. et al. (2010) An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell, 17, 443-454.
38. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-837. (Pubitemid 46802390)
39. Li, M.T., Richter, F., Chang, C., Irwin, R.J. and Huang, H. (2002) Androgen and retinoic acid interaction in LNCaP cells, effects on cell proliferation and expression of retinoic acid receptors and epidermal growth factor receptor. BMC Cancer, 2, 16.
40. Schug, T.T., Berry, D.C., Shaw, N.S., Travis, S.N. and Noy, N. (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell, 129, 723-733. (Pubitemid 46802374)
41. Berthon, P., Waller, A.S., Villette, J.M., Loridon, L., Cussenot, O. and Maitland, N.J. (1997) Androgens are not a direct requirement for the proliferation of human prostatic epithelium in vitro. Int. J. Cancer, 73, 910-916. (Pubitemid 127483050)
42. Masiello, D., Cheng, S., Bubley, G.J., Lu, M.L. and Balk, S.P. (2002) Bicalutamide functions as an androgen receptor antagonist by assembly of a transcriptionally inactive receptor. J. Biol Chem., 277, 26321-26326. (Pubitemid 34967123)
43. Fong, C.J., Sutkowski, D.M., Braun, E.J., Bauer, K.D., Sherwood, E.R., Lee, C. and Kozlowski, J.M. (1993) Effect of retinoic acid on the proliferation and secretory activity of androgen-responsive prostatic carcinoma cells. J. Urol., 149, 1190-1194. (Pubitemid 23133813)
44. Astrom, A., Pettersson, U., Krust, A., Chambon, P. and Voorhees, J.J. (1990) Retinoic acid and synthetic analogs differentially activate retinoic acid receptor dependent transcription. Biochem. Biophys. Res. Commun., 173, 339-345.
45. Nakayama, T., Watanabe, M., Yamanaka, M., Hirokawa, Y., Suzuki, H., Ito, H., Yatani, R. and Shiraishi, T. (2001) The role of epigenetic modifications in retinoic acid receptor beta2 gene expression in human prostate cancers. Lab Invest., 81, 1049-1057. (Pubitemid 32645980)
46. Aboseif, S.R., Dahiya, R., Narayan, P. and Cunha, G.R. (1997) Effect of retinoic acid on prostatic development. Prostate, 31, 161-167. (Pubitemid 27225199)
47. Pang, S., Dannull, J., Kaboo, R., Xie, Y., Tso, C.L., Michel, K., deKernion, J.B. and Belldegrun, A.S. (1997) Identification of a positive regulatory element responsible for tissue-specific expression of prostate-specific antigen. Cancer Res., 57, 495-499. (Pubitemid 27081670)
48. Vezina, C.M., Allgeier, S.H., Fritz, W.A., Moore, R.W., Strerath, M., Bushman, W. and Peterson, R.E. (2008) Retinoic acid induces prostatic bud formation. Dev. Dyn., 237, 1321-1333. (Pubitemid 351668816)
49. Dubbink, H.J., Hoedemaeker, R.F., Van der Kwast, T.H., Schroder, F.H. and Romijn, J.C. (1999) Human prostate-specific transglutaminase: a new prostatic marker with a unique distribution pattern. Lab Invest., 79, 141-150. (Pubitemid 29110645)
50. Young, C.Y., Murtha, P.E., Andrews, P.E., Lindzey, J.K. and Tindall, D.J. (1994) Antagonism of androgen action in prostate tumor cells by retinoic acid. Prostate, 25, 39-45. (Pubitemid 24230913)
51. Chuang, K.H., Lee, Y.F., Lin, W.J., Chu, C.Y., Altuwaijri, S., Wan, Y.J. and Chang, C. (2005) 9-cis-retinoic acid inhibits androgen receptor activity through activation of retinoid X receptor. Mol. Endocrinol., 19, 1200-1212. (Pubitemid 40594119)
52. Ubels, J.L., Wertz, J.T., Ingersoll, K.E., Jackson, R.S. 2nd and Aupperlee, M.D. (2002) Down-regulation of androgen receptor expression and inhibition of lacrimal gland cell proliferation by retinoic acid. Exp. Eye Res., 75, 561-571. (Pubitemid 35435611)
53. Schuur, E.R., Henderson, G.A., Kmetec, L.A., Miller, J.D., Lamparski, H.G. and Henderson, D.R. (1996) Prostate-specific antigen expression is regulated by an upstream enhancer. J. Biol. Chem., 271, 7043-7051. (Pubitemid 26104139)
54. Noss, K.R., Wolfe, S.A. and Grimes, S.R. (2002) Upregulation of prostate specific membrane antigen/folate hydrolase transcription by an enhancer. Gene, 285, 247-256. (Pubitemid 34246341)
55. Dilworth, F.J., Fromental-Ramain, C., Yamamoto, K. and Chambon, P. (2000) ATP-driven chromatin remodeling activity and histone acetyltransferases act sequentially during transactivation by RAR/RXR In vitro. Mol. Cell, 6, 1049-1058.
56. Kimura, K., Markowski, M., Bowen, C. and Gelmann, E.P. (2001) Androgen blocks apoptosis of hormone-dependent prostate cancer cells. Cancer Res., 61, 5611-5618. (Pubitemid 32700276)
57. Berchem, G.J., Bosseler, M., Sugars, L.Y., Voeller, H.J., Zeitlin, S. and Gelmann, E.P. (1995) Androgens induce resistance to bcl-2-mediated apoptosis in LNCaP prostate cancer cells. Cancer Res., 55, 735-738.
58. Zhang, X.K. (2002) Vitamin A and apoptosis in prostate cancer. Endocr. Relat. Cancer, 9, 87-102.
59. Huss, W.J., Lai, L., Barrios, R.J., Hirschi, K.K. and Greenberg, N.M. (2004) Retinoic acid slows progression and promotes apoptosis of spontaneous prostate cancer. Prostate, 61, 142-152. (Pubitemid 39244701)
60. Pasquali, D., Thaller, C. and Eichele, G. (1996) Abnormal level of retinoic acid in prostate cancer tissues. J. Clin. Endocrinol. Metab., 81, 2186-2191. (Pubitemid 26175944)
61. Reichman, M.E., Hayes, R.B., Ziegler, R.G., Schatzkin, A., Taylor, P.R., Kahle, L.L. and Fraumeni, J.F. Jr (1990) Serum vitamin A and subsequent development of prostate cancer in the first National Health and Nutrition Examination Survey Epidemiologic Follow-up Study. Cancer Res., 50, 2311-2315. (Pubitemid 20134487)
62. Hayes, R.B., Bogdanovicz, J.F., Schroeder, F.H., De Bruijn, A., Raatgever, J.W., Van der Maas, P.J., Oishi, K. and Yoshida, O. (1988) Serum retinol and prostate cancer. Cancer, 62, 2021-2026. (Pubitemid 18261831)
63. Schenk, J.M., Riboli, E., Chatterjee, N., Leitzmann, M.F., Ahn, J., Albanes, D., Reding, D.J., Wang, Y., Friesen, M.D., Hayes, R.B. et al. (2009) Serum retinol and prostate cancer risk: a nested case-control study in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidemiol. Biomarkers Prev., 18, 1227-1231.
64. Dahiya, R., Park, H.D., Cusick, J., Vessella, R.L., Fournier, G. and Narayan, P. (1994) Inhibition of tumorigenic potential and prostate-specific antigen expression in LNCaP human prostate cancer cell line by 13-cis-retinoic acid. Int. J. Cancer, 59, 126-132. (Pubitemid 24310958)
65. Huang, J., Powell, W.C., Khodavirdi, A.C., Wu, J., Makita, T., Cardiff, R.D., Cohen, M.B., Sucov, H.M. and Roy-Burman, P. (2002) Prostatic intraepithelial neoplasia in mice with conditional disruption of the retinoid X receptor alpha allele in the prostate epithelium. Cancer Res., 62, 4812-4819.