Bmp2 transcription in osteoblast progenitors is regulated by a distant 3′ enhancer located 156.3 kilobases from the promoter

Molecular and Cellular Biology

Volumn 27, Issue 8, 2007, Pages 2934-2951

  Chandler, Ronald L ^a   Chandler, Kelly J ^a   McFarland, Karen A ^b   Mortlock, Douglas P ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BMP2 GENE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA FLANKING REGION; EMBRYO; ENHANCER REGION; GENE; GENE CASSETTE; GENE CONTROL; GENE DELETION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCATION; GENETIC ENGINEERING; GENETIC REGULATION; GENETIC RISK; GENOME ANALYSIS; LACZ GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY DNA SEQUENCE; REPORTER GENE; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE;

3' FLANKING REGION; ANIMALS; BASE PAIRING; BETA-GALACTOSIDASE; BIOLOGICAL MARKERS; BONE AND BONES; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; EMBRYO; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; OSTEOBLASTS; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; SEQUENCE DELETION; STEM CELLS; TOOTH; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; TRANSGENES;

BACTERIA (MICROORGANISMS); MUS MUSCULUS;

EID: 34147205885     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01609-06     Document Type: Article

References (76)

1. brams, K. L., J. Xu, C. Nativelle-Serpentini, S. Dabirshahsahebi, and M. B. Rogers. 2004. An evolutionary and molecular analysis of Bmp2 expression. J. Biol. Chem. 279:15916-15928.
2. Aubin, J. E. 1998. Advances in the osteoblast lineage. Biochem. Cell Biol. 76:899-910.
3. Berman, B. P., Y. Nibu, B. D. Pfeiffer, P. Tomancak, S. E. Celniker, M. Levine, G. M. Rubin, and M. B. Eisen. 2002. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. USA 99:757-762.
4. Bitgood, M. J., and A. P. McMahon. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:126-138.
5. Blackman, R. K., M. Sanicola, L. A. Raftery, T. Gillevet, and W. M. Gelbart. 1991. An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development 111:657-666.
6. Blanchette, M., W. J. Kent, C. Riemer, L. Elnitski, A. F. Smit, K. M. Roskin, R. Baertsch, K. Rosenbloom, H. Clawson, E. D. Green, D. Haussler, and W. Miller. 2004. Aligning multiple genomic sequences with the threaded block-set aligner. Genome Res. 14:708-715.
7. Bouma, G. J., G. T. Hart, L. L. Washburn, A. K. Recknagel, and E. M. Eicher. 2004. Using real time RT-PCR analysis to determine multiple gene expression patterns during XX and XY mouse fetal gonad development. Gene Expr. Patterns 5:141-149.
8. Brinster, R. L., H. Y. Chen, M. Trumbauer, A. W. Senear, R. Warren, and R. D. Palmiter. 1981. Somatic expression of herpes thymidine kinase in mice following injection of a fusion gene into eggs. Cell 27:223-231.
9. Chen, D., M. Zhao, and G. R. Mundy. 2004. Bone morphogenetic proteins. Growth Factors 22:233-241.
10. Choi, K. Y., H. J. Kim, M. H. Lee, T. G. Kwon, H. D. Nah, T. Furuichi, T. Komori, S. H. Nam, Y. J. Kim, and H. M. Ryoo. 2005. Runx2 regulates FGF2-induced Bmp2 expression during cranial bone development. Dev. Dyn. 233:115-121.
11. Colnot, C., C. Lu, D. Hu, and J. A. Helms. 2004. Distinguishing the contributions of the perichondrium, cartilage, and vascular endothelium to skeletal development. Dev. Biol. 269:55-69.
12. DiLeone, R. J., G. A. Marcus, M. D. Johnson, and D. M. Kingsley. 2000. Efficient studies of long-distance Bmp5 gene regulation using bacterial artificial chromosomes. Proc. Natl. Acad. Sci. USA 97:1612-1617.
13. DiLeone, R. J., L. B. Russell, and D. M. Kingsley. 1998. An extensive 3′ regulatory region controls expression of Bmp5 in specific anatomical structures of the mouse embryo. Genetics 148:401-408.
14. Ducy, P., and G. Karsenty. 2000. The family of bone morphogenetic proteins. Kidney Int. 57:2207-2214.
15. Ducy, P., R. Zhang, V. Geoffroy, A. L. Ridall, and G. Karsenty. 1997. Osf2/ Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747-754.
16. Dudley, A. T., and E. J. Robertson. 1997. Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev. Dyn. 208:349-362.
17. Erives, A., and M. Levine. 2004. Coordinate enhancers share common organizational features in the Drosophila genome. Proc. Natl. Acad. Sci. USA 101:3851-3856.
18. Feng, J. Q., L. Xing, J. H. Zhang, M. Zhao, D. Horn, J. Chan, B. F. Boyce, S. E. Harris, G. R. Mundy, and D. Chen. 2003. NF-kappaB specifically activates BMP-2 gene expression in growth plate chondrocytes in vivo and in a chondrocyte cell line in vitro. J. Biol. Chem. 278:29130-29135.
19. Folger, K. R., E. A. Wong, G. Wahl, and M. R. Capecchi. 1982. Patterns of integration of DNA microinjected into cultured mammalian cells: evidence for homologous recombination between injected plasmid DNA molecules. Mol. Cell. Biol. 2:1372-1387.
20. Franzen, A., A. Oldberg, and M. Solursh. 1989. Possible recruitment of osteoblastic precursor cells from hypertrophic chondrocytes during initial osteogenesis in cartilaginous limbs of young rats. Matrix 9:261-265.
21. Friedrich, G., and P. Soriano. 1991. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5:1513-1523.
22. Furuta, Y., D. W. Piston, and B. L. Hogan. 1997. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
23. Ghosh-Choudhury, N., G. G. Choudhury, M. A. Harris, J. Wozney, G. R. Mundy, S. L. Abboud, and S. E. Harris. 2001. Autoregulation of mouse BMP-2 gene transcription is directed by the proximal promoter element. Biochem. Biophys. Res. Commun. 286:101-108.
24. Gong, S., C. Zheng, M. L. Doughty, K. Losos, N. Didkovsky, U. B. Schambra, N. J. Nowak, A. Joyner, G. Leblanc, M. E. Hatten, and N. Heintz. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
25. Hager-Theodorides, A. L., S. V. Outram, D. K. Shah, R. Sacedon, R. E. Shrimpton, A. Vicente, A. Varas, and T. Crompton. 2002. Bone morphogenetic protein 2/4 signaling regulates early thymocyte differentiation. J. Immunol. 169:5496-5504.
26. Hardwick, J. C., G. R. Van Den Brink, S. A. Bleuming, I. Ballester, J. M. Van Den Brande, J. J. Keller, G. J. Offerhaus, S. J. Van Deventer, and M. P. Peppelenbosch. 2004. Bone morphogenetic protein 2 is expressed by, and acts upon, mature epithelial cells in the colon. Gastroenterology 126:111- 121.
27. Helvering, L. M., R. L. Sharp, X. Ou, and A. G. Geiser. 2000. Regulation of the promoters for the human bone morphogenetic protein 2 and 4 genes. Gene 256:123-138.
28. Hogan, B. L. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10:1580-1594.
29. Holtke, H. J., and C. Kessler. 1990. Non-radioactive labeling of RNA transcripts in vitro with the hapten digoxigenin (DIG); hybridization and ELISA-based detection. Nucleic Acids Res. 18:5843-5851.
30. Horner, A., L. Shum, J. A. Ayres, K. Nonaka, and G. H. Nuckolls. 2002. Fibroblast growth factor signaling regulates Dach1 expression during skeletal development. Dev. Dyn. 225:35-4-5.
31. Howard, M. L., and E. H. Davidson. 2004. cis-Regulatory control circuits in development. Dev. Biol. 271:109-118.
32. Ikeda, T., S. Nomura, A. Yamaguchi, T. Suda, and S. Yoshiki. 1992. In situ hybridization of bone matrix proteins in undecalcified adult rat bone sections. J. Histochem. Cytochem. 40:1079-1088.
33. Jung, H. S., V. Oropeza, and I. Thesleff. 1999. Shh, Bmp-2, Bmp-4 and Fgf-8 are associated with initiation and patterning of mouse tongue papillae. Mech. Dev. 81:179-182.
34. Karsenty, G., and E. F. Wagner. 2002. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2:389-406.
35. Kent, W. J., C. W. Sugnet, T. S. Furey, K. M. Roskin, T. H. Pringle, A. M. Zahler, and D. Haussler. 2002. The human genome browser at UCSC. Genome Res. 12:996-1006.
36. Khandekar, M., N. Suzuki, J. Lewton, M. Yamamoto, and J. D. Engel. 2004. Multiple, distant Gata2 enhancers specify temporally and tissue-specific patterning in the developing urogenital system. Mol. Cell. Biol. 24:10263-10276.
37. Kim, D. G., H. M. Kang, S. K. Jang, and H. S. Shin. 1992. Construction of a bifunctional mRNA in the mouse by using the internal ribosomal entry site of the encephalomyocarditis virus. Mol. Cell. Biol. 12:3636-3643.
38. Kim, I. S., F. Otto, B. Zabel, and S. Mundlos. 1999. Regulation of chondrocyte differentiation by Cbfa1. Mech. Dev. 80:159-170.
39. Kingsley, D. M. 1994. What do BMPs do in mammals? Clues from the mouse short-ear mutation. Trends Genet. 10:16-21.
40. Kingsley, D. M., A. E. Bland, J. M. Grubber, P. C. Marker, L. B. Russell, N. G. Copeland, and N. A. Jenkins. 1992. The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF beta superfamily. Cell 71:399-410.
41. Kleinjan, D. A., and V. van Heyningen. 2005. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76:8-32.
42. Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R. T. Branson, Y. H. Gao, M. Inada, M. Sato, R. Okamoto, Y. Kitamura, S. Yoshiki, and T. Kishimoto. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
43. Kulessa, H., G. Turk, and B. L. Hogan. 2000. Inhibition of Bmp signaling affects growth and differentiation in the anagen hair follicle. EMBO J. 19:6664-6674.
44. Kurokawa, D., H. Kiyonari, R. Nakayama, C. Kimura-Yoshida, I. Matsuo, and S. Aizawa. 2004. Regulation of Otx2 expression and its functions in mouse forebrain and midbrain. Development 131:3319-3331.
45. Kurokawa, D., N. Takasaki, H. Kiyonari, R. Nakayama, C. Kimura-Yoshida, I. Matsuo, and S. Aizawa. 2004. Regulation of Otx2 expression and its functions in mouse epiblast and anterior neuroectoderm. Development 131: 3307-3317.
46. Lecanda, F., L. V. Avioli, and S. L. Cheng. 1997. Regulation of bone matrix protein expression and induction of differentiation of human osteoblasts and human bone marrow stromal cells by bone morphogenetic protein-2. J. Cell Biochem. 67:386-396.
47. Lee, E. C., D. Yu, J. Martinez de Velasco, L. Tessarollo, D. A. Swing, D. L. Court, N. A. Jenkins, and N. G. Copeland. 2001. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
48. Long, F., U. I. Chung, S. Ohba, J. McMahon, H. M. Kronenberg, and A. P. McMahon. 2004. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 131:1309-1318.
49. Loots, G. G., R. M. Locksley, C. M. Blankespoor, Z. E. Wang, W. Miller, E. M. Rubin, and K. A. Frazer. 2000. Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science 288:136-140.
50. Lyons, K. M., B. L. Hogan, and E. J. Robertson. 1995. Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50:71-83.
51. Lyons, K. M., R. W. Pelton, and B. L. Hogan. 1990. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development 109:833-844.
52. Lyons, K. M., R. W. Pelton, and B. L. Hogan. 1989. Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-beta-like genes coordinately regulate aspects of embryonic development. Genes Dev. 3:1657-1668.
53. Mortlock, D. P., C. Guenther, and D. M. Kingsley. 2003. A general approach for identifying distant regulatory elements applied to the Gdf6 gene. Genome Res. 13:2069-2081.
54. Mountford, P., B. Zevnik, A. Duwel, J. Nichols, M. Li, C. Dani, M. Robertson, I. Chambers, and A. Smith. 1994. Dicistronic targeting constructs: reporters and modifiers of mammalian gene expression. Proc. Natl. Acad. Sci. USA 91:4303-4307.
55. Mundy, G., R. Garrett, S. Harris, J. Chan, D. Chen, G. Rossini, B. Boyce, M. Zhao, and G. Gutierrez. 1999. Stimulation of bone formation in vitro and in rodents by statins. Science 286:1946-1949.
56. Nobrega, M. A., I. Ovcharenko, V. Afzal, and E. M. Rubin. 2003. Scanning human gene deserts for long-range enhancers. Science 302:413.
57. Otto, F., A. P. Thornell, T. Crompton, A. Denzel, K. C. Gilmour, I. R. Rosewell, G. W. Stamp, R. S. Beddington, S. Mundlos, B. R. Olsen, P. B. Selby, and M. J. Owen. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771.
58. Ovcharenko, I., G. G. Loots, M. A. Nobrega, R. C. Hardison, W. Miller, and L. Stubbs. 2005. Evolution and functional classification of vertebrate gene deserts. Genome Res. 15:137-145.
59. Ovcharenko, I., M. A. Nobrega, G. G. Loots, and L. Stubbs. 2004. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res. 32:W280-W286.
60. Pathi, S., J. B. Rutenberg, R. L. Johnson, and A. Vortkamp. 1999. Interaction of Ihh and BMP/Noggin signaling during cartilage differentiation. Dev. Biol. 209:239-253.
61. Patton, J. T., and M. H. Kaufman. 1995. The timing of ossification of the limb bones, and growth rates of various long bones of the fore and hind limbs of the prenatal and early postnatal laboratory mouse. J. Anat. 186:175-185.
62. Peacock, M., C. H. Turner, M. J. Econs, and T. Foroud. 2002. Genetics of osteoporosis. Endocrinol. Rev. 23:303-326.
63. Portnoy, M. E., K. J. McDermott, A. Antonellis, E. H. Margulies, A. B. Prasad, D. M. Kingsley, E. D. Green, and D. P. Mortlock. 2005. Detection of potential GDF6 regulatory elements by multispecies sequence comparisons and identification of a skeletal joint enhancer. Genomics 86:295-305.
64. Siepel, A., G. Bejerano, J. S. Pedersen, A. S. Hinrichs, M. Hou, K. Rosenbloom, H. Clawson, J. Spieth, L. W. Hillier, S. Richards, G. M. Weinstock, R. K. Wilson, R. A. Gibbs, W. J. Kent, W. Miller, and D. Haussler. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15:1034-1050.
65. Solloway, M. J., A. T. Dudley, E. K. Bikoff, K. M. Lyons, B. L. Hogan, and E. J. Robertson. 1998. Mice lacking Bmp6 function. Dev. Genet. 22:321-339.
66. St-Jacques, B., M. Hammerschmidt, and A. P. McMahon. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13:2072-2086.
67. Styrkarsdottir, U., J. B. Cazier, A. Kong, O. Rolfsson, H. Larsen, E. Bjarnadottir, V. D. Johannsdottir, M. S. Sigurdardottir, Y. Bagger, C. Christiansen, I. Reynisdottir, S. F. Grant, K. Jonasson, M. L. Frigge, J. R. Gulcher, G. Sigurdsson, and K. Stefansson. 2003. Linkage of osteoporosis to chromosome 20p12 and association to BMP2. PloS Biol. 1:E69.
68. Sugiura, T. 1999. Cloning and functional characterization of the 5′-flanking region of the human bone morphogenetic protein-2 gene. Biochem. J. 338: 433-440.
69. Sykaras, N., and L. A. Opperman. 2003. Bone morphogenetic proteins (BMPs): how do they function and what can they offer the clinician? J. Oral Sci. 45:57-73.
70. Takae, R., S. Matsunaga, N. Origuchi, T. Yamamoto, N. Morimoto, S. Suzuki, and T. Sakou. 1999. Immunolocalization of bone morphogenetic protein and its receptors in degeneration of intervertebral disc. Spine 24: 1397-1401.
71. Treier, M., A. S. Gleiberman, S. M. O'Connell, D. P. Szeto, J. A. McMahon, A. P. McMahon, and M. G. Rosenfeld. 1998. Multistep signaling requirements for pituitary organogenesis in vivo. Genes Dev. 12:1691-1704.
72. Warming, S., N. Costantino, D. L. Court, N. A. Jenkins, and N. G. Copeland. 2005. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 33:e36.
73. Waterston, R. H., K. Lindblad-Toh, E. Birney, J. Rogers, J. F. Abril, P. Agarwal, R. Agarwala, R. Ainscough, M. Alexandersson, P. An, S. E. Antonarakis, J. Attwood, R. Baertsch, J. Bailey, K. Barlow, S. Beck, E. Berry, B. Birren, T. Bloom, P. Bork, M. Botcherby, N. Bray, M. R. Brent, D. G. Brown, S. D. Brown, C. Bult, J. Burton, J. Butler, R. D. Campbell, P. Carninci, S. Cawley, F. Chiaromonte, A. T. Chinwalla, D. M. Church, M. Clamp, C. Clee, F. S. Collins, L. L. Cook, R. R. Copley, A. Coulson, O. Couronne, J. Cuff, V. Curwen, T. Cutts, M. Daly, R. David, J. Davies, K. D. Delehaunty, J. Deri, E. T. Dermitzakis, C. Dewey, N. J. Dickens, M. Diekhans, S. Dodge, I. Dubchak, D. M. Dunn, S. R. Eddy, L. Elnitski, R. D. Ernes, P. Eswara, E. Eyras, A. Felsenfeld, G. A. Fewell, P. Flicek, K. Foley, W. N. Frankel, L. A. Fulton, R. S. Fulton, T. S. Furey, D. Gage, R. A. Gibbs, G. Glusman, S. Gnerre, N. Goldman, L. Goodstadt, D. Grafham, T. A. Graves, E. D. Green, S. Gregory, R. Guigo, M. Guyer, R. C. Hardison, D. Haussler, Y. Hayashizaki, L. W. Hillier, A. Hinrichs, W. Hlavina, T. Holzer, F. Hsu, A. Hua, T. Hubbard, A. Hunt, I. Jackson, D. B. Jane, L. S. Johnson, M. Jones, T. A. Jones, A. Joy, M. Kamal, E. K. Karlsson, et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420:520-562.
74. Wozney, J. M., V. Rosen, A. J. Celeste, L. M. Mitsock, M. J. Whitters, R. W. Kriz, R. M. Hewick, and E. A. Wang. 1988. Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534.
75. Zhang, H., and A. Bradley. 1996. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977-2986.
76. Zhao, M., M. Qiao, S. E. Harris, D. Chen, B. O. Oyajobi, and G. R. Mundy. 2006. The zinc finger transcription factor gli2 mediates bone morphogenetic protein 2 expression in osteoblasts in response to hedgehog signaling. Mol. Cell. Biol. 26:6197-6208.