Gene targeting by the vitamin D response element binding protein reveals a role for vitamin D in osteoblast mTOR signaling

FASEB Journal

Volumn 25, Issue 3, 2011, Pages 937-947

  Lisse, Thomas S ^a   Liu, Ting ^a   Irmler, Martin ^b   Beckers, Johannes ^b,c   Chen, Hong ^d   Adams, John S ^a   Hewison, Martin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone; Resistance; Vitamin D receptor

Indexed keywords

CALCITRIOL; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; RAPAMYCIN; SMALL INTERFERING RNA; VITAMIN D; VITAMIN D BINDING PROTEIN; VITAMIN D RECEPTOR;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA DAMAGE INDUCIBLE TRANSCRIPT 4 GENE; FAMILIAL HYPOPHOSPHATEMIC RICKETS; FLOW CYTOMETRY; GENE; GENE CONTROL; GENE OVEREXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; OSTEOBLAST; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VITAMIN D RESPONSIVE ELEMENT; WESTERN BLOTTING;

BONE NEOPLASMS; CALCITRIOL; CELL DIVISION; CELL LINE, TUMOR; HUMANS; HYPOPHOSPHATEMIC RICKETS, X-LINKED DOMINANT; OSTEOBLASTS; OSTEOSARCOMA; PROMOTER REGIONS, GENETIC; RECEPTORS, CALCITRIOL; RESPONSE ELEMENTS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 79954614306     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-172577     Document Type: Article

References (58)

1. Malloy, P. J., Pike, J. W., and Feldman, D. (1999) The vitamin D receptor and the syndrome of hereditary 1, 25-dihydroxyvitamin D-resistant rickets. Endocr. Rev. 20, 156-188 (Pubitemid 29341671)
2. Li, Y. C., Pirro, A. L., Amling, M., Delling, G., Baron, R., Bronson, R., and Demay, M. B. (1997) Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc. Natl. Acad. Sci. U. S. A. 94, 9831-9835
3. Miller, C. W., Morosetti, R., Campbell, M. J., Mendoza, S., and Koeffler, H. P. (1997) Integrity of the 1, 25-dihydroxyvitamin D3 receptor in bone, lung, and other cancers. Mol. Carcinog. 19, 254-257 (Pubitemid 27392004)
4. Banwell, C. M., MacCartney, D. P., Guy, M., Miles, A. E., Uskokovic, M. R., Mansi, J., Stewart, P. M., O'Neill, L. P., Turner, B. M., Colston, K. W., and Campbell, M. J. (2006) Altered nuclear receptor corepressor expression attenuates vitamin D receptor signaling in breast cancer cells. Clin Cancer Res. 12, 2004-2013
5. Arbelle, J. E., Chen, H., Gaead, M. A., Allegretto, E. A., Pike, J. W., and Adams, J. S. (1996) Inhibition of vitamin D receptorretinoid X receptor-vitamin D response element complex formation by nuclear extracts of vitamin D-resistant New World primate cells. Endocrinology 137, 786-789
6. Chen, H., Hu, B., Allegretto, E. A., and Adams, J. S. (2000) The vitamin D response element-binding protein. A novel dominantnegative regulator of vitamin D-directed transactivation. J. Biol. Chem. 275, 35557-35564
7. Chen, H., Hewison, M., and Adams, J. S. (2006) Functional characterization of heterogeneous nuclear ribonuclear protein C1/C2 in vitamin D resistance: a novel response elementbinding protein. J. Biol. Chem. 281, 39114-39120 (Pubitemid 46041870)
8. Hewison, M., Rut, A. R., Kristjansson, K., Walker, R. E., Dillon, M. J., Hughes, M. R., and O'Riordan, J. L. (1993) Tissue resistance to 1, 25-dihydroxyvitamin D without a mutation of the vitamin D receptor gene. Clin. Endocrinol. (Oxf.) 39, 663-670 (Pubitemid 24010955)
9. Adams, J. S., Ren, S., Liu, P. T., Chun, R. F., Lagishetty, V., Gombart, A. F., Borregaard, N., Modlin, R. L., Hewison, M. Vitamin D-directed rheostatic regulation of monocyte antibacterial responses. J. Immunol. 182, 4289-4295
10. Meyer, M. B., Goetsch, P. D., and Pike, J. W. (2010) A downstream intergenic cluster of regulatory enhancers contributes to the induction of CYP24A1 expression by 1α, 25-dihydroxyvitamin D3. J. Biol. Chem. 285, 15599-15610
11. Ohyama, Y., Ozono, K., Uchida, M., Yoshimura, M., Shinki, T., Suda, T., and Yamamoto, O. (1996) Functional assessment of two vitamin D-responsive elements in the rat 25-hydroxyvitamin D3 24-hydroxylase gene. J. Biol. Chem. 271, 30381-30385 (Pubitemid 26404040)
12. Zierold, C., Darwish, H. M., and DeLuca, H. F. (1994) Identification of a vitamin D-response element in the rat calcidiol (25-hydroxyvitamin D3) 24-hydroxylase gene. Proc. Natl. Acad. Sci. U. S. A. 91, 900-902
13. Sofer, A., Lei, K., Johannessen, C. M., and Ellisen, L. W. (2005) Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol. Cell. Biol. 25, 5834-5845 (Pubitemid 40946541)
14. Proud, C. G. (2009) mTORC1 signalling and mRNA translation. Biochem. Soc. Trans. 37, 227-231
15. Alarid, E. T. (2006) Lives and times of nuclear receptors. Mol. Endocrinol. 20, 1972-1981 (Pubitemid 44286698)
16. Thakur, M. K., and Paramanik, V. (2009) Role of steroid hormone coregulators in health and disease. Horm. Res. 71, 194-200
17. Penning, T. M., Jin, Y., Rizner, T. L., and Bauman, D. R. (2008) Pre-receptor regulation of the androgen receptor. Mol. Cell. Endocrinol. 281, 1-8 (Pubitemid 350296604)
18. Jurutka, P. W., Bartik, L., Whitfield, G. K., Mathern, D. R., Barthel, T. K., Gurevich, M., Hsieh, J. C., Kaczmarska, M., Haussler, C. A., and Haussler, M. R. (2007) Vitamin D receptor: key roles in bone mineral pathophysiology, molecular mechanism of action, and novel nutritional ligands. J. Bone Miner. Res. 22 (Suppl. 2), V2-V10 (Pubitemid 351304640)
19. Carlberg, C., and Seuter, S. (2009) A genomic perspective on vitamin D signaling. Anticancer Res. 29, 3485-3493
20. Adams, J. S., Chen, H., Chun, R., Gacad, M. A., Encinas, C., Ren, S., Nguyen, L., Wu, S., Hewison, M., and Barsony, J. (2004) Response element binding proteins and intracellular vitamin D binding proteins: novel regulators of vitamin D trafficking, action and metabolism. J. Steroid Biochem. Mol. Biol. 89-90, 461-465 (Pubitemid 38844331)
21. Swanson, M. S., and Dreyfuss, G. (1988) Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol. Cell. Biol. 8, 2237-2241
22. Mahajan, M. C., Narlikar, G. J., Boyapaty, G., Kingston, R. E., and Weissman, S. M. (2005) Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at the beta-globin locus control region. Proc. Natl. Acad. Sci. U. S. A. 102, 15012-15017 (Pubitemid 41513326)
23. Tolnay, M., Vereshchagina, L. A., and Tsokos, G. C. (1999) Heterogeneous nuclear ribonucleoprotein D0B is a sequencespecific DNA-binding protein. Biochem. J. 338, 417-425
24. Krecic, A. M., and Swanson, M. S. (1999) hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11, 363-371 (Pubitemid 29273808)
25. Tiscornia, G., and Mahadevan, M. S. (2000) Myotonic dystrophy: the role of the CUG triplet repeats in splicing of a novel DMPK exon and altered cytoplasmic DMPK mRNA isoform ratios. Mol. Cell 5, 959-967
26. Tay, N., Chan, S. H., and Ren, E. C. (1992) Identification and cloning of a novel heterogeneous nuclear ribonucleoprotein C-like protein that functions as a transcriptional activator of the hepatitis B virus enhancer II. J. Virol. 66, 6841-6848
27. Tomonaga, T., and Levens, D. (1995) Heterogeneous nuclear ribonucleoprotein K is a DNA-binding transactivator. J. Biol. Chem. 270, 4875-4881
28. Chen, H., Hewison, M., Hu, B., and Adams, J. S. (2003) Heterogeneous nuclear ribonucleoprotein (hnRNP) binding to hormone response elements: a cause of vitamin D resistance. Proc. Natl. Acad. Sci. U. S. A. 100, 6109-6114 (Pubitemid 36576939)
29. Omdahl, J. M. B. (2005) The 25-hydroxyvitamin D-24-hydroxylase. In VitaminD, Vol. 1 (Feldman, D., Pike, J. W., and Glorieux, F. H., eds) pp. 85-104, Elsevier, New York
30. Demay, M. B., Kiernan, M. S., DeLuca, H. F., and Kronenberg, H. M. (1992) Sequences in the human parathyroid hormone gene that bind the 1, 25-dihydroxyvitamin D3 receptor and mediate transcriptional repression in response to 1, 25-dihydroxyvitamin D3. Proc. Natl. Acad. Sci. U. S. A. 89, 8097-8101
31. Eiring, A. M., Harb, J. G., Neviani, P., Garton, C., Oaks, J. J., Spizzo, R., Liu, S., Schwind, S., Santhanam, R., Hickey, C. J., Becker, H., Chandler, J. C., Andino, R., Cortes, J., Hokland, P., Huettner, C. S., Bhatia, R., Roy, D. C., Liebhaber, S. A., Caligiuri, M. A., Marcucci, G., Garzon, R., Croce, C. M., Calin, G. A., Perrotti, D. (2010) miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140, 652-665
32. Iacobazzi, V., Invernizzi, F., Baratta, S., Pons, R., Chung, W., Garavaglia, B., Dionisi-Vici, C., Ribes, A., Parini, R., Huertas, M. D., Roldan, S., Lauria, G., Palmieri, F., and Taroni, F. (2004) Molecular and functional analysis of SLC25A20 mutations causing carnitine-acylcarnitine translocase deficiency. Hum. Mutat. 24, 312-320 (Pubitemid 39336637)
33. Shibuya, T., Watanabe, K., Yamashita, H., Shimizu, K., Miyashita, H., Abe, M., Moriya, T., Ohta, H., Sonoda, H., Shimosegawa, T., Tabayashi, K., and Sato, Y. (2006) Isolation and characterization of vasohibin-2 as a homologue of VEGF-inducible endothelium-derived angiogenesis inhibitor vasohibin. Arterioscler. Thromb. Vasc. Biol. 26, 1051-1057 (Pubitemid 43732111)
34. Chung, I., Han, G., Seshadri, M., Gillard, B. M., Yu, W. D., Foster, B. A., Trump, D. L., and Johnson, C. S. (2009) Role of vitamin D receptor in the antiproliferative effects of calcitriol in tumor-derived endothelial cells and tumor angiogenesis in vivo. Cancer Res. 69, 967-975
35. Fernandez-Garcia, N. I., Palmer, H. G., Garcia, M., Gonzalez-Martin, A., Del Rio, M., Barettino, D., Volpert, O., Muñoz, A., and Jimenez, B. (2005) 1alpha, 25-Dihydroxyvitamin D3 regulates the expression of Id1 and Id2 genes and the angiogenic phenotype of human colon carcinoma cells. Oncogene 24, 6533-6544 (Pubitemid 41486636)
36. Kovalenko, P. L., Zhang, Z., Cui, M., Clinton, S. K., and Fleet, J. C. (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
37. Rhodes, D. R., Yu, J., Shanker, K., Deshpande, N., Varambally, R., Ghosh, D., Barrette, T., Pandey, A., and Chinnaiyan, A. M. (2004) ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6, 1-6 (Pubitemid 38391943)
38. Foster, K. G., and Fingar, D. C. (2010) Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J. Biol. Chem. 285, 14071-14077
39. Yu, L., McPhee, C. K., Zheng, L., Mardones, G. A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F., Hailey, D. W., Oorschot, V., Klumperman, J., Baehrecke, E. H., and Lenardo, M. J. (2010) Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465, 942-946
40. Nojima, H., Tokunaga, C., Eguchi, S., Oshiro, N., Hidayat, S., Yoshino, K., Hara, K., Tanaka, N., Avruch, J., and Yonezawa, K. (2003) The mammalian target of rapamycin (mTOR) partner, raptor, binds the mTOR substrates p70 S6 kinase and 4E-BP1 through their TOR signaling (TOS) motif. J. Biol. Chem. 278, 15461-15464 (Pubitemid 36799651)
41. Ellisen, L. W., Ramsayer, K. D., Johannessen, C. M., Yang, A., Beppu, H., Minda, K., Oliner, J. D., McKeon, F., and Haber, D. A. (2002) REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol. Cell 10, 995-1005 (Pubitemid 35453821)
42. Ellisen, L. W. (2005) Growth control under stress: mTOR regulation through the REDD1-TSC pathway. Cell Cycle 4, 1500-1502
43. Shoshani, T., Faerman, A., Mett, I., Zelin, E., Tenne, T., Gorodin, S., Moshel, Y., Elbaz, S., Budanov, A., Chajut, A., Kalinski, H., Kamer, I., Rozen, A., Mor, O., Keshet, E., Leshkowitz, D., Einat, P., Skaliter, R., and Feinstein, E. (2002) Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell. Biol. 22, 2283-2293 (Pubitemid 34224633)
44. Brafman, A., Mett, I., Shafir, M., Gottlieb, H., Damari, G., Gozlan-Kelner, S., Vishnevskia-Dai, V., Skaliter, R., Einat, P., Faerman, A., Feinstein, E., and Shoshani, T. (2004) Inhibition of oxygen-induced retinopathy in RTP801-deficient mice. Invest. Ophthalmol. Vis. Sci. 45, 3796-3805 (Pubitemid 39298599)
45. Reiling, J. H., and Hafen, E. (2004) The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev. 18, 2879-2892 (Pubitemid 39602307)
46. Pineau, P., Volinia, S., McJunkin, K., Marchio, A., Battiston, C., Terris, B., Mazzaferro, V., Lowe, S. W., Croce, C. M., and Dejean, A. (2010) miR-221 overexpression contributes to liver tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 107, 264-269
47. Yang, J., Ikezoe, T., Nishioka, C., Ni, L., Koeffler, H. P., and Yokoyama, A. (2010) Inhibition of mTORC1 by RAD001 (everolimus) potentiates the effects of 1, 25-dihydroxyvitamin D (3) to induce growth arrest and differentiation of AML cells in vitro and in vivo. Exp. Hematol. 38, 666-676
48. O'Kelly, J., Uskokovic, M., Lemp, N., Vadgama, J., and Koeffler, H. P. (2006) Novel Gemini-vitamin D3 analog inhibits tumor cell growth and modulates the Akt/mTOR signaling pathway. J. Steroid Biochem. Mol. Biol. 100, 107-116 (Pubitemid 44175834)
49. Wang, Q. M., Jones, J. B., and Studzinski, G. P. (1996) Cyclindependent kinase inhibitor p27 as a mediator of the G1-S phase block induced by 1, 25-dihydroxyvitamin D3 in HL60 cells. Cancer Res. 56, 264-267 (Pubitemid 26026352)
50. Liu, M., Lee, M. H., Cohen, M., Bommakanti, M., and Freedman, L. P. (1996) Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced differentiation of the myelomonocytic cell line U937. Genes Dev. 10, 142-153 (Pubitemid 26049905)
51. Muto, A., Kizaki, M., Yamato, K., Kawai, Y., Kamata-Matsushita, M., Ueno, H., Ohguchi, M., Nishihara, T., Koeffler, H. P., and Ikeda, Y. (1999) 1, 25-Dihydroxyvitamin D3 induces differentiation of a retinoic acid-resistant acute promyelocytic leukemia cell line (UF-1) associated with expression of p21 (WAF1/CIP1) and p27 (KIP1). Blood 93, 2225-2233 (Pubitemid 29153624)
52. Yen, A., and Varvayanis, S. (1994) Late dephosphorylation of the RB protein in G2 during the process of induced cell differentiation. Exp. Cell Res. 214, 250-257 (Pubitemid 24302399)
53. Abraham, R. T., and Gibbons, J. J. (2007) The mammalian target of rapamycin signaling pathway: twists and turns in the road to cancer therapy. Clin Cancer Res. 13, 3109-3114 (Pubitemid 46944891)
54. Canaud, G., Knebelmann, B., Harris, P. C., Vrtovsnik, F., Correas, J. M., Pallet, N., Heyer, C. M., Letavernier, E., Bienaimé, F., Thervet, E., Martinez, F., Terzi, F., and Legendre, C. (2010) Therapeutic mTOR inhibition in autosomal dominant polycystic kidney disease: What is the appropriate serum level? Am. J. Transplant. 10, 1701-1706
55. Alvarez-Garcia, O., García-López, E., Loredo, V., Gil-Peña, H., Rodríguez-Suárez, J., Ordóñez, F. A., Carbajo-Pérez, E., and Santos, F. (2010) Rapamycin induces growth retardation by disrupting angiogenesis in the growth plate. Kidney Int. 78, 561-568
56. Vellai, T., Takacs-Vellai, K., Zhang, Y., Kovacs, A. L., Orosz, L., and Müller, F. (2003) Genetics: influence of TOR kinase on lifespan in C. elegans. Nature 426, 620 (Pubitemid 38009359)
57. Kaeberlein, M., Powers, R. W. 3rd, Steffen, K. K., Westman, E. A., Hu, D., Dang, N., Kerr, E. O., Kirkland, K. T., Fields, S., and Kennedy, B. K. (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310, 1193-1196 (Pubitemid 41681747)
58. Harrison, D. E., Strong, R., Sharp, Z. D., Nelson, J. F., Astle, C. M., Flurkey, K., Nadon, N. L., Wilkinson, J. E., Frenkel, K., Carter, C. S., Pahor, M., Javors, M. A., Fernandez, E., and Miller, R. A. (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392-395