Activation of receptor activator of NF-κB ligand gene expression by 1,25-dihydroxyvitamin D3 is mediated through multiple long-range enhancers

Molecular and Cellular Biology

Volumn 26, Issue 17, 2006, Pages 6469-6486

  Kim, Sungtae ^a   Yamazaki, Miwa ^a   Zella, Lee A ^a   Shevde, Nirupama K ^a   Pike, J Wesley ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; CYTOKINE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; RECEPTOR ANTIBODY; RETINOID X RECEPTOR; RNA POLYMERASE II; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL SECRETION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA FLANKING REGION; DNA MICROARRAY; DNA RESPONSIVE ELEMENT; ENHANCER REGION; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; HORMONAL REGULATION; HUMAN; HUMAN CELL; MESENCHYME CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; RANKL GENE; T LYMPHOCYTE; TRANSCRIPTION INITIATION;

EID: 33747787316     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00353-06     Document Type: Article

References (71)

1. Bettoun, D. J., T. P. Burris, K. A. Houck, D. W. Buck II, K. R. Stayrook, B. Khalifa, J. Lu, W. W. Chin, and S. Nagpal. 2003. Retinoid X receptor is a nonsilent major contributor to vitamin D receptor-mediated transcriptional activation. Mol. Endocrinol. 17:2320-2328. [Epub ahead of print.]
2. Carroll, J. S., X. S. Liu, A. S. Brodsky, W. Li, C. A. Meyer, A. J. Szary, J. Eeckhoute, W. Shao, E. V. Hestermann, T. R. Geistlinger, E. A. Fox, P. A. Silver, and M. Brown. 2005. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33-43.
3. Cawley, S., S. Bekiranov, H. H. Ng, P. Kapranov, E. A. Sekinger, D. Kampa, A. Piccolboni, V. Sementchenko, J. Cheng, A. J. Williams, R. Wheeler, B. Wong, J. Drenkow, M. Yamanaka, S. Patel, S. Brubaker, H. Tammana, G. Helt, K. Struhl, and T. R. Gingeras. 2004. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116:499-509.
4. Cheng, J., P. Kapranov, J. Drenkow, S. Dike, S. Brubaker, S. Patel, J. Long, D. Stern, H. Tammana, G. Helt, V. Sementchenko, A. Piccolboni, S. Bekiranov, D. K. Bailey, M. Ganesh, S. Ghosh, I. Bell, D. S. Gerhard, and T. R. Gingeras. 2005. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308:1149-1154. [Epub ahead of print.]
5. Cosgrove, M. S., J. D. Boeke, and C. Wolberger. 2004. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11:1037-1043.
6. de Bruin, D., Z. Zaman, R. A. Liberatore, and M. Ptashne. 2001. Telomere looping permits gene activation by a downstream UAS in yeast. Nature 409:109-113.
7. Dekker, J., K. Rippe, M. Dekker, and N. Kleckner. 2002. Capturing chromosome conformation. Science 295:1306-1311.
8. 3 24-hydroxylase. Mol. Cell. Biol. 25:472-487.
9. Drissen, R., R. J. Palstra, N. Gillemans, E. Splinter, F. Grosveld, S. Philipsen, and W. de Laat. 2004. The active spatial organization of the beta-globin locus requires the transcription factor EKLF. Genes Dev. 18:2485-2490.
10. ENCODE Project Consortium. 2004. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306:636-640.
11. Fan, X., E. M. Roy, T. C. Murphy, M. S. Nanes, S. Kim, J. W. Pike, and J. Rubin. 2004. Regulation of RANKL promoter activity is associated with histone remodeling in murine bone stromal cells. J. Cell Biochem. 93:807-818.
12. Fu, Q., R. L. Jilka, S. C. Manolagas, and C. A. O'Brien. 2002. Parathyroid hormone stimulates receptor activator of NFkappa B ligand and inhibits osteoprotegerin expression via protein kinase A activation of cAMP-response element-binding protein. J. Biol. Chem. 277:48868-48875. [Epub ahead of print.]
13. Fu, Q., S. C. Manolagas, and C. A. O'Brien. Parathyroid hormone controls receptor activator of NF-κB ligand gene expression via a distant transcriptional enhancer. Mol. Cell. Biol. 26:6453-6468.
14. Glynn, E. F., P. C. Megee, H. G. Yu, C. Mistrot, E. Unal, D. E. Koshland, J. L. Derisi, and J. L. Gerton. 2004. Genome-wide mapping of the cohesion complex in the yeast Saccharomyces cerevisiae. PLoS Biol. 2:E259. [Online.]
15. Gribnau, J., K. Diderich, S. Pruzina, R. Calzolari, and P. Fraser. 2000. Intergenic transcription and developmental remodeling of chromatin subdomains in the human beta-globin locus. Mol. Cell 5:377-386.
16. Groyer, A., G. Schweizer-Groyer, F. Cadepond, M. Mariller, and E. E. Baulieu. 1987. Antiglucocorticosteroid effects suggest why steroid hormone is required for receptors to bind DNA in vivo but not in vitro. Nature 328:624-626.
17. Harris, W. H., and R. P. Heaney. 1969. Skeletal renewal and metabolic bone disease. N. Engl. J. Med. 280:193-202.
18. Hofbauer, L. C., F. Gori, L. Riggs, D. L. Lacey, C. R. Dunstan, T. C. Spelsberg, and S. Khosla. 1999. Stimulation of osteoprotegerin ligand and inhibition of osteoprotegerin production by glucocorticoids in human osteoblastic lineage cells: potential paracrine mechanisms of glucocorticoid-induced osteoporosis. Endocrinology 140:4382-4389.
19. Hofbauer, L. C., S. Khosla, C. R. Dunstan, D. L. Lacey, W. J. Boyle, and B. L. Riggs. 2000. The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J. Bone Miner. Res. 15:2-12.
20. Hsu, H., D. L. Lacey, C. R. Dunstan, I. Solovyev, A. Colombero, E. Timms, H. L. Tan, G. Elliott, M. J. Kelley, I. Sarosi, L. Wang, X. Z. Xia, R. Elliott, L. Chiu, T. Black, S. Scully, C. Capparelli, S. Morony, G. Shimamoto, M. B. Bass, and W. J. Boyle. 1999. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. USA 96:3540-3545.
21. Impey, S., S. R. McCorkle, H. Cha-Molstad, J. M. Dwyer, G. S. Yochum, J. M. Boss, S. McWeeney, J. J. Dunn, G. Mandel, and R. H. Goodman. 2004. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119:1041-1054.
22. Jimi, E., S. Akiyama, T. Tsurukai, N. Okahashi, K. Kobayashi, N. Udagawa, T. Nishihara, N. Takahashi, and T. Suda. 1999. Osteoclast differentiation factor acts as a multifunctional regulator in murine osteoclast differentiation and function. J. Immunol. 163:434-442.
23. Jimi, E., I. Nakamura, L. T. Duong, T. Ikebe, N. Takahashi, G. A. Rodan, and T. Suda. 1999. Interleukin 1 induces multinucleation and bone-resorbing activity of osteoclasts in the absence of osteoblasts/stromal cells. Exp. Cell Res. 247:84-93.
24. Kabe, Y., J. Yamada, H. Uga, Y. Yamaguchi, T. Wada, and H. Handa. 2005. NF-Y is essential for the recruitment of RNA polymerase II and inducible transcription of several CCAAT box-containing genes. Mol. Cell. Biol. 25:512-522.
25. 2 stimulates osteoclast-like cell formation and bone resorbing activity via osteoblasts: role of cAMP-dependent protein kinase. J. Bone Miner. Res. 11:62-71.
26. Kamp, D., J. Cheng, P. Kapranov, M. Yamanaka, S. Brubaker, S. Cawley, J. Drenkow, A. Piccolboni, S. Bekiranov, G. Helt, H. Tammana, and T. R. Gingeras. 2004. Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res. 14:331-342.
27. Kapranov, P., S. E. Cawley, J. Drenkow, S. Bekiranov, R. L. Strausberg, S. P. Fodor, and T. R. Gingeras. 2002. Large-scale transcriptional activity in chromosomes 21 and 22. Science 296:916-919.
28. Karst, M., G. Gorny, R. J. Galvin, and M. J. Oursler. 2004. Roles of stromal cell RANKL, OPG, and M-CSF expression in biphasic TGF-beta regulation of osteoclast differentiation. J. Cell Physiol. 200:99-106.
29. Kato, S., K. Sekine, T. Matsumoto, and T. Yoshizawa. 1998. Molecular genetics of vitamin D receptor acting in bone. J. Bone Miner. Metab. 16:65-71.
30. 3 stimulates cyclic vitamin D receptor/retinoid X receptor DNA-binding, coactivator recruitment, and histone acetylation in intact osteoblasts. J. Bone Miner. Res. 20:305-317. [Epub ahead of print.]
31. Kim, T. H., L. O. Barrera, M. Zheng, C. Qu, M. A. Singer, T. A. Richmond, Y. Wu, R. D. Green, and B. Ren. 2005. A high resolution map of active promoters in the human genome. Nature 436:876-880.
32. Kim, T. H., L. O. Barrera, C. Qu, S. Van Calcar, N. D. Trinklein, S. J. Cooper, R. M. Luna, C. K. Glass, M. G. Rosenfeld, R. M. Myers, and B. Ren. 2005. Direct isolation and identification of promoters in the human genome. Genome Res. 15:830-839.
33. Kirmizis, A., S. M. Bartley, A. Kuzmichev, R. Margueron, D. Reinberg, R. Green, and P. J. Farnham. 2004. Silencing of human polycomb target genes is associated with methylation of histone H3 lys 27. Genes Dev. 18:1592-1605.
34. Kitazawa, S., R. Kitazawa, and S. Maeda. 1999. Promoter structure of mouse RANKL/TRANCE/ODF gene. Biochim. Biophys. Acta 1445:134-141.
35. Koga, T., M. Inui, K. Inoue, S. Kim, A. Suematsu, E. Kobayashi, T. Iwata, H. Ohnishi, T. Matozaki, T. Kodama, T. Taniguchi, H. Takayanagi, and T. Takai. 2004. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428:758-763.
36. Kondo, H., J. Guo, and F. R. Bringhurst. 2002. Cyclic adenosine monophosphate/protein kinase A mediates parathyroid hormone/parathyroid hormone-related protein receptor regulation of osteoclastogenesis and expression of RANKL and osteoprotegerin mRNAs by marrow stromal cells. J. Bone Miner. Res. 17:1667-1679.
37. Kong, Y. Y., H. Yoshida, I. Sarosi, H. L. Tan, E. Timms, C. Capparelli, S. Morony, A. J. Oliveira-dos-Santos, G. Van, A. Itie, W. Khoo, A. Wakeham, C. R. Dunstan, D. L. Lacey, T. W. Mak, W. J. Boyle, and J. M. Penninger. 1999. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397:315-323.
38. Lacey, D. L., E. Timm, H. L. Tan, M. J. Kelley, C. R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, H. Hsu, J. Sullivan, N. Hawkins, E. Davy, C. Capparelli, A. Eli, Y. X. Qian, S. Kaufman, I. Sarosi, V. Shalhoub, G. Senaldi, J. Guo, J. Delaney, and W. J. Boyle. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176.
39. Laganiere, J., G. Deblois, C. Lefebvre, A. R. Bataille, F. Robert, and V. Giguere. 2005. Location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc. Natl. Acad. Sci. USA 102:11651-11656. [Epub ahead of print.]
40. Lee, S. K., and J. A. Lorenzo. 1999. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology 140:3552-3561.
41. Liu, B. Y., J. Guo, B. Lanske, P. Divieti, H. M. Kronenberg, and F. R. Bringhurst. 1998. Conditionally immortalized murine bone marrow stromal cells mediate parathyroid hormone-dependent osteoclastogenesis in vitro. Endocrinology 139:1952-1964.
42. Manolagas, S. C. 2000. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev. 21:115-137.
43. Manolagas, S. C., R. S. Weinstein, R. L. Jilka, and A. M. Parfitt. 1998. Parathyroid hormone and corticosteroid-induced osteoporosis. Lancet 352:1940.
44. Matsuo, K., D. L. Galson, C. Zhao, L. Peng, C. Laplace, K. Z. Wang, M. A. Bachler, H. Amano, H. Aburatani, H. Ishikawa, and E. F. Wagner. 2004. Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J. Biol. Chem. 279:26475-26480. [Epub ahead of print.]
45. Mundy, G. R. 2000. Pathogenesis of osteoporosis and challenges for drug delivery. Adv. Drug Delivery Rev. 42:165-173.
46. Nagpal, S., S. Na, and R. Rathnachalam. 2005. Noncalcemic actions of vitamin D receptor ligands. Endocr. Rev. 26:662-687. (First published 29 March 2005; doi:10.1210/er.2004-0002.)
47. Oberley, M. J., J. Tsao, P. Yau, and P. J. Farnham. 2004. High throughput screening of chromatin immunoprecipitates using CpG-island microarrays. Methods Enzymol. 376:315-334.
48. O'Brien, C. A., B. Kern, I. Gubrij, G. Karsenty, and S. C. Manolagas. 2002. Cbfa1 does not regulate RANKL gene activity in stromal/osteoblastic cells. Bone 30:453-462.
49. O'Sullivan, J. M., S. M. Tan-Wong, A. Morillon, B. Lee, J. Coles, J. Mellor, and N. J. Proudfoot. 2004. Gene loops juxtapose promoters and terminators in yeast. Nat. Genet. 36:1014-1018. [Epub ahead of print.]
50. Pike, J. W., and N. K. Shevde. 2005. The vitamin D receptor, p. 167-191. In D. Feldman, J. W. Pike, and F. H. Glorieux (ed.), Vitamin D, 2nd ed. Elsevier, San Diego, Calif.
51. Romas, E., N. Udagawa, H. Zhou, T. Tamura, M. Saito, T. Taga, D. J. Hilton, T. Suda, K. W. Ng, and T. J. Martin. 1996. The role of gp130-mediated signals in osteoclast development: regulation of interleukin 11 production by osteoblasts and distribution of its receptor in bone marrow cultures. J. Exp. Med. 183:2581-2591.
52. Schubeler, D., D. M. MacAlpine, D. Scalzo, C. Wirbelauer, C. Kooperberg, F. van Leeuwen, D. E. Gottschling, L. P. O'Neill, B. M. Turner, J. Delrow, S. P. Bell, and M. Groudine. 2004. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18:1263-1271.
53. 3 selectively induces bone formation. Proc. Natl. Acad. Sci. USA 99:13487-13491. [Epub ahead of print.]
54. Sivagurunathan, S., M. M. Muir, T. C. Brennan, J. P. Seale, and R. S. Mason. 2005. Influence of glucocorticoids on human osteoclast generation and activity. J. Bone Miner. Res. 20:390-398. [Epub ahead of print.]
55. Smith, C. L., and B. W. O'Malley. 2004. Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr. Rev. 25:45-71.
56. Spotswood, H. T., and B. M. Turner. 2002. An increasingly complex code. J. Clin. Investig. 110:577-582.
57. Suda, T., N. Takahashi, N. Udagawa, E. Jimi, M. T. Gillespie, and T. J. Martin. 1999. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 20:345-357.
58. Sutton, A. L., and P. N. MacDonald. 2003. Vitamin D: more than a "bone-a-fide" hormone. Mol. Endocrinol. 17:777-791. [Epub ahead of print.]
59. Szutorisz, H., N. Dillon, and L. Tora. 2005. The role of enhancers as centres for general transcription factor recruitment. Trends Biochem. Sci. 30:593-599. [Epub ahead of print.]
60. Takahashi, N., T. Akatsu, T. Sasaki, G. C. Nicholson, J. M. Moseley, T. J. Martin, and T. Suda. 1993. Induction of calcitonin receptors by 1,25-dihydroxyvitamin D in osteoclast-like multinucleated cells formed from mouse bone marrow cells. Endocrinology 123:1504-1510.
61. Takayanagi, H., S. Kim, T. Koga, H. Nishina, M. Isshiki, H. Yoshida, A. Saiura, M. Isobe, T. Yokochi, J. Inoue, E. F. Wagner, T. W. Mak, T. Kodama, and T. Taniguchi. 2002. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 3:889-901.
62. Tamura, T., N. Udagawa, N. Takahashi, C. Miyaura, S. Tanaka, Y. Yamada, Y. Koishihara, Y. Ohsugi, K. Kumaki, and T. Taga. 1993. Soluble interleukin-6 receptor triggers osteoclast formation by interleukin 6. Proc. Natl. Acad. Sci. USA 90:11924-11928.
63. Teitelbaum, S. L. 2000. Bone resorption by osteoclasts. Science 289:1504-1508.
64. Teitelbaum, S. L., and F. P. Ross. 2003. Genetic regulation of osteoclast development and function. Nat. Rev. Genet. 4:638-649.
65. Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Laat. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 10:1453-1465.
66. Wani, M. R., K. Fuller, N. S. Kim, Y. Choi, and T. Chambers. 1999. Prostaglandin E2 cooperates with TRANCE in osteoclast induction from hemopoietic precursors: synergistic activation of differentiation, cell spreading, and fusion. Endocrinology 140:1927-1935.
67. Weinstein, R. S., R. L. Jilka, A. M. Parfitt, and S. C. Manolagas. 1998. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J. Clin. Investig. 102:274-282.
68. Whyte, M. P., and S. Mumm. 2004. Heritable disorders of the RANKL/OPG/RANKL signaling pathway. Musculoskelet. Neuronal Interact. 4:254-267.
69. Yamada, K., D. T. Duong, D. K. Scott, J. C. Wang, and D. K. Granner. 1999. CCAAT/enhancer-binding protein beta is an accessory factor for the glucocorticoid response from the cAMP response element in the rat phosphoenolpyruvate carboxykinase gene promoter. J. Biol. Chem. 274:5880-5888.
70. 3 potently stimulates gene-specific DNA binding of the vitamin D receptor in osteoblasts. J. Biol. Chem. 278:31756-31765. [Epub ahead of print.]
71. 3. Mol. Endocrinol. 20:1231-1247. (First published 23 February 2006; 10.1210/me.2000-0015.)