Constitutive activation of the mitogen-activated protein kinase pathway impairs vitamin D signaling in human prostate epithelial cells

Journal of Cellular Physiology

Volumn 224, Issue 2, 2010, Pages 433-442

  Zhang, Zhentao ^a   Kovalenko, Pavlo ^a   Cui, Min ^a   Desmet, Marsha ^a   Clinton, Steven K ^b   Fleet, James C ^a,c  

^a PURDUE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Purdue University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; HETERODIMER; MITOGEN ACTIVATED PROTEIN KINASE; RETINOID X RECEPTOR; RETINOID X RECEPTOR ALPHA; STEROID RECEPTOR COACTIVATOR 1; VITAMIN D; CALCITRIOL RECEPTOR; PROTEIN P21;

ARTICLE; CELL CLONE; CELL IMMORTALIZATION; CELL LINE; CELL TRANSFORMATION; DRUG MECHANISM; ENZYME ACTIVATION; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MAMMAL CELL; MUTATION; PHOSPHORYLATION; PRIORITY JOURNAL; PROSTATE EPITHELIUM; PROTEIN DOMAIN; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; PROMOTER REGION; PROSTATE; PROTEIN BINDING;

MAMMALIA;

AMINO ACID SEQUENCE; CALCITRIOL; CELL LINE; CELL LINE, TRANSFORMED; CELL PROLIFERATION; ENZYME ACTIVATION; EPITHELIAL CELLS; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NUCLEAR RECEPTOR COACTIVATOR 1; ONCOGENE PROTEIN P21(RAS); PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROSTATE; PROTEIN BINDING; RECEPTORS, CALCITRIOL; RETINOID X RECEPTOR ALPHA; TRANSCRIPTIONAL ACTIVATION;

EID: 77953642640     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22139     Document Type: Article

References (46)

1. Adam-Stitah S, Penna L, Chambon P, Rochette-Egly C. 1999. Hyperphosphorylation of the retinoid X receptor alpha by activated c-Jun NH2-terminal kinases. J Biol Chem 274:18932-18941. (Pubitemid 129519310)
2. Ahonen MH, Tenkanen L, Teppo L, Hakama M, Tuohimaa P. 2000. Prostate cancer risk and prediagnostic serum 25-hydroxyvitamin D levels (Finland). Cancer Causes Control 11:847-852.
3. Alagbala AA, Moser MT, Johnson CS, Trump DL, Foster BA. 2007. Characterization of vitamin D insensitive prostate cancer cells. J Steroid Biochem Mol Biol 103:712-716. (Pubitemid 46401313)
4. Anwar K, Nakakuki K, Shiraishi T, Naiki H, Yatani R, Inuzuka M. 1992. Presence of ras oncogene mutations and human papillomavirus DNA in human prostate carcinomas. Cancer Res 52:5991-5996.
5. Bastien J, Adam-Stitah S, Plassat JL, Chambon P, Rochette-Egly C. 2002. The phosphorylation site located in the A region of retinoic X receptor alpha is required for the antiproliferative effect of retinoic acid (RA) and the activation of RA target genes in F9 cells. J Biol Chem 277:28683-28689.
6. Bello D, Webber MM, Kleinman HK, Wartinger DD, Rhim JS. 1997. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis 18:1215-1223. (Pubitemid 28132513)
7. Benecke A, Chambon P, Gronemeyer H. 2000. Synergy between estrogen receptor alpha activation functions AF1 and AF2 mediated by transcription intermediary factor TIF2. EMBO Rep 1:151-157.
8. Bettoun DJ, Burris TP, Houck KA, Buck DW, Stayrook KR, Khalifa B, Lu J, Chin WW, Nagpal S. 2003. Retinoid X receptor is a non-silent major contributor to vitamin D receptor-mediated transcriptional activation. Mol Endocrinol 17:2320-2328. (Pubitemid 37352541)
9. Brelivet Y, Kammerer S, Rochel N, Poch O, Moras D. 2004. Signature of the oligomeric behaviour of nuclear receptors at the sequence and structural level. EMBO Rep 5:423-429. (Pubitemid 38618287)
10. Bruck N, Bastien J, Bour G, Tarrade A, Plassat JL, Bauer A, Adam-Stitah S, Rochette-Egly C. 2005. Phosphorylation of the retinoid X receptor at the omega loop, modulates the expression of retinoic-acid-target genes with a promoter context specificity. Cell Signal 17:1229-1239. (Pubitemid 40982613)
11. Chen TC, Wang L, Whitlatch LW, Flanagan JN, Holick MF. 2003. Prostatic 25-hydroxyvitamin D-1alpha-hydroxylase and its implication in prostate cancer. J Cell Biochem 88:315-322. (Pubitemid 36119904)
12. Cui M, Zhao Y, Hance KW, Shao A, Wood RJ, Fleet JC. 2009. Effects of MAPK signaling on 1,25-dihydroxyvitamin D-mediated CYP24 gene expression in the enterocyte-like cell line, Caco-2. J Cell Physiol 219:132-142.
13. Dwivedi PP, Hii CS, Ferrante A, Tan J, Der CJ, Omdahl JL, Morris HA, May BK. 2002. Role of MAP kinases in the 1,25-dihydroxyvitamin D3-induced transactivation of the rat cytochrome P450C24 (CYP24) promoter. Specific functions for ERK1/ERK2 and ERK5. J Biol Chem 277:29643-29653. (Pubitemid 41079254)
14. Fleet JC. 2008. Molecular actions of vitamin D contributing to cancer prevention. Mol Aspects Med 29:388-396.
15. 3-mediated regulation of transcellular calcium transport in Caco-2 cells. Am J Physiol 276:G958-G964.
16. Forman BM, Umesono K, Chen J, Evans RM. 1995. Unique response pathways are established by allosteric interactions among nuclear hormone receptors. Cell 81:541-550.
17. Gioeli D, Mandell JW, Petroni GR, Frierson HF, Jr., Weber MJ. 1999. Activation of mitogen-activated protein kinase associated with prostate cancer progression. Cancer Res 59:279-284. (Pubitemid 29048852)
18. Giovannucci E, Liu Y, Rimm EB, Hollis BW, Fuchs CS, Stampfer MJ, Willett WC. 2006. Prospective study of predictors of vitamin D status and cancer incidence and mortality in men. J Natl Cancer Inst 98:451-459.
19. Hedlund TE, Moffatt KA, Miller GJ. 1996. Vitamin D receptor expression is required for growth modulation by 1 alpha, 25-dihydroxyvitamin D3 in the human prostatic carcinoma cell line ALAV-31. J Steroid Biochem Mol Biol 58:277-288.
20. Hittelman AB, Burakov D, Iniguez-Lluhi JA, Freedman LP, Garabedian MJ. 1999. Differential regulation of glucocorticoid receptor transcriptional activation via AF-1-associated proteins. EMBO J 18:5380-5388. (Pubitemid 29465587)
21. Kerry DM, Dwivedi PP, Hahn CN, Morris HA, Omdahl JL, May BK. 1996. Transcriptional synergism between vitamin D-responsive elements in the rat 25-hydroxyvitamin D3 24-hydroxylase (CYP24) promoter. J Biol Chem 271:29715-29721. (Pubitemid 26389597)
22. Kovalenko PL, Zhang Z, Cui M, Clinton SK, Fleet JC. 2010. 1,25 Dihydroxyvitamin D-mediated orchestration of anticancer, transcript-level effects in the immortalized, non-transformed prostate epithelial cell line, RWPE1. BMC Genomics 11:26.
23. Kumar R, Thompson EB. 2003. Transactivation functions of the N-terminal domains of nuclear hormone receptors: Protein folding and coactivator interactions. Mol Endocrinol 17:1-10. (Pubitemid 36132655)
24. Lee HY, Suh YA, Robinson MJ, Clifford JL, Hong WK, Woodgett JR, Cobb MH, Mangelsdorf DJ, Kurie JM. 2000. Stress pathway activation induces phosphorylation of retinoid X receptor. J Biol Chem 275:32193-32199.
25. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
26. Macoritto M, Nguyen-Yamamoto L, Huang DC, Samuel S, Yang XF, Wang TT, White JH, Kremer R. 2008. Phosphorylation of the human retinoid X receptor alpha at serine 260 impairs coactivator(s) recruitment and induces hormone resistance to multiple ligands. J Biol Chem 283:4943-4956.
27. Mann KK, Padovani AM, Guo Q, Colosimo AL, Lee HY, Kurie JM, Miller WH, Jr. 2005. Arsenic trioxide inhibits nuclear receptor function via SEK1/JNK-mediated RXRalpha phosphorylation. J Clin Invest 115:2924-2933. (Pubitemid 41434420)
28. Matsushima-Nishiwaki R, Okuno M, Adachi S, Sano T, Akita K, Moriwaki H, Friedman SL, Kojima S. 2001. Phosphorylation of retinoid X receptor alpha at serine 260 impairs its metabolism and function in human hepatocellular carcinoma. Cancer Res 61:7675-7682. (Pubitemid 32995065)
29. McInerney EM, Rose DW, Flynn SE, Westin S, Mullen TM, Krones A, Inostroza J, Torchia J, Nolte RT, Assa-Munt N, Milburn MV, Glass CK, Rosenfeld MG. 1998. Determinants of coactivator LXXLL motif specificity in nuclear receptor transcriptional activation. Genes Dev 12:3357-3368.
30. Miller GJ, Stapleton GE, Hedlund TE, Moffat KA. 1995. Vitamin D receptor expression, 24-hydroxylase activity, and inhibition of growth by 1 alpha, 25-dihydroxyvitamin D3in seven human prostatic carcinoma cell lines. Clin Cancer Res 1:997-1003.
31. Narayanan R, Tovar SV, Falzon M, Weigel NL. 2004. The functional consequences of cross talk between the vitamin D receptor and ERK signaling pathways are cell specific. J Biol Chem 278:47298-47310. (Pubitemid 39518387)
32. Pike JW, Zella LA, Meyer MB, Fretz JA, Kim S. 2007. Molecular actions of 1,25-dihydroxyvitamin D3 on genes involved in calcium homeostasis. J Bone Miner Res 22:V16-V19. (Pubitemid 351304642)
33. Prufer K, Schroder C, Hegyi K, Barsony J. 2002. Degradation of RXRs influences sensitivity of rat osteosarcoma cells to the antiproliferative effects of calcitriol.Mol Endocrinol 16:961-976.
34. Rhim JS, Webber MM, Bello D, Lee MS, Arnstein P, Chen LS, Jay G. 1994. Stepwise immortalization and transformation of adult human prostate epithelial cells by a combination of HPV-18 and v-Ki-ras. Proc Natl Acad Sci USA 91:11874-11878.
35. Robbins DJ, Zhen EH, Cheng MG, Xu SC, Vanderbilt CA, Ebert D, Garcia C, Dang A, Cobb MH. 1993. Regulation and properties of extracellular signal-regulated protein kinase-1, kinase-2, and kinase-3. J Am Soc Nephrol 4:1104-1110.
36. Roovers K, Assoian RK. 2000. Integrating the MAP kinase signal into the G1 phase cell cycle machinery. BioEssays 22:818-826.
37. Schubbert S, Shannon K, Bollag G. 2007. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 7:295-308. (Pubitemid 46480970)
38. Sebag M, Henderson J, Rhim J, Kremer R. 1992. Relative resistance to 1,25-dihydroxyvitamin D3 in a keratinocyte model of tumor progression. J Biol Chem 267:12162-12167.
39. Shields JM, Pruitt K, McFall A, Shaub A, Der CJ. 2000. Understanding Ras: 'It ain't over til it's over'. Trends Cell Biol 10:147-154.
40. Simboli-Campbell M, Narvaez CJ, Tenniswood M, Welsh J. 1996. 1,25-Dihydroxyvitamin D3 induces morphological and biochemical markers of apoptosis in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol 58:367-376. (Pubitemid 26348970)
41. Solomon C, White JH, Kremer R. 1999. Mitogen-activated protein kinase inhibits 1,25-dihydroxyvitamin D3-dependent signal transduction by phosphorylating human retinoid X receptor alpha. J Clin Invest 103:1729-1735.
42. Song Y, Fleet JC. 2007. Intestinal resistance to 1,25 dihydroxyvitaminDinmice heterozygous for the vitamin D receptor knockout allele. Endocrinology 148:1396-1402. (Pubitemid 46272812)
43. Viola MV, Fromowitz F, Oravez S, Deb S, Finkel G, Lundy J, Hand P, Thor A, Schlom J. 1986. Expression of ras oncogene p21 in prostate cancer. N Engl J Med 314:133-137. (Pubitemid 16183168)
44. Wajchmann HJ, Rathod B, Song S, Xu H, Wang X, Uskokovic MR, Studzinski GP. 1996. Loss of deoxcytidine kinase expression and tetraploidization of HL60 cells following long-term culture in 1,25-dihydroxyvitamin D3. Exp Cell Res 224:312-322. (Pubitemid 26140565)
45. Zhuang SH, Schwartz GG, Cameron D, Burnstein KL. 1997. Vitamin Dreceptor content and transcriptional activity do not fully predict antiproliferative effects of vitamin D in human prostate cancer cell lines. Mol Cell Endocrinol 126:83-90. (Pubitemid 27055550)
46. Zimmerman TL, Thevananther S, Ghose R, Burns AR, Karpen SJ. 2006. Nuclear export of retinoid X receptor alpha in response to interleukin-1beta-mediated cell signaling: Roles for JNK and SER260. J Biol Chem 281:15434-15440. (Pubitemid 43855135)