HIF1α regulation of Sox9 in necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis

Development

Volumn 134, Issue 21, 2007, Pages 3917-3928

  Amarilio, Roy ^a   Viukov, Sergey V ^a   Sharir, Amnon ^a   Eshkar Oren, Idit ^a   Johnson, Randall S ^b   Zelzer, Elazar ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b SECTION OF MOLECULAR BIOLOGY   (United States)

Author keywords

BMP; Bone developement; Chondrocyte differentiation; Chondrogenesis; GDF5; HIF1; HIF1 ; Hypoxia; Joint formation; Mesenchymal condensation; SOX5; SOX6; SOX9; VEGF

Indexed keywords

AGGRECAN; COLLAGEN TYPE 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TRANSCRIPTION FACTOR SOX6; TRANSCRIPTION FACTOR SOX9; HIF1A PROTEIN, MOUSE; HIGH MOBILITY GROUP PROTEIN; HOMEODOMAIN PROTEIN; PRRX1 PROTEIN, MOUSE; SOX-9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL TYPE; CHONDROGENESIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; GENE INACTIVATION; JOINT; LIMB BUD; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REGULATORY MECHANISM; VASCULARIZATION; ANIMAL; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IN VITRO STUDY; LIMB; METABOLISM; PRENATAL DEVELOPMENT; SKELETON; STEM CELL; TIME;

ANIMALS; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; CHONDROGENESIS; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIGH MOBILITY GROUP PROTEINS; HOMEODOMAIN PROTEINS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; SKELETON; STEM CELLS; TIME FACTORS; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 36549088609     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.008441     Document Type: Article

References (56)

1. Ainbinder, E., Amir-Zilberstein, L., Yamaguchi, Y., Handa, H. and Dikstein, R. (2004). Elongation inhibition by DRB sensitivity-inducing factor is regulated by the A20 promoter via a novel negative element and NF-kappaB. Mol. Cell. Biol. 24, 2444-2454.
2. Akiyama, H., Chaboissier, M. C., Martin, J. F., Schedl, A. and de Crombrugghe, B. (2002). The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 16, 2813-2828.
3. Ambati, B. K., Nozaki, M., Singh, N., Takeda, A., Jani, P. D., Suthar, T., Albuquerque, R. J., Richter, E., Sakurai, E., Newcomb, M. T. et al. (2006). Corneal avascularity is due to soluble VEGF receptor-1. Nature 443, 993-997.
4. Archer, C. W., Dowthwaite, G. P. and Francis-West, P. (2003). Development of synovial joints. Birth Defects Res. C Embryo Today 69, 144-155.
5. Arteel, G. E., Thurman, R. G. and Raleigh, J. A. (1998). Reductive metabolism of the hypoxia marker pimonidazole is regulated by oxygen tension independent of the pyridine nucleotide redox state. Eur. J. Biochem. 253, 743-750.
6. Bi, W., Deng, J. M., Zhang, Z., Behringer, R. R. and de Crombrugghe, B. (1999). Sox9 is required for cartilage formation. Nat. Genet. 22, 85-89.
7. Brunet, L. J., McMahon, J. A., McMahon, A. P. and Harland, R. M. (1998). Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280, 1455-1457.
8. Cowden Dahl, K. D., Fryer, B. H., Mack, F. A., Compernolle, V., Maltepe, E., Adelman, D. M., Carmeliet, P. and Simon, M. C. (2005). Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblas: differentiation. Mol. Cell. Biol. 25, 10479-10491.
9. D'Ippolito, G., Diabira, S., Howard, G. A., Roos, B. A. and Schiller, P. C. (2006). Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39, 513-522.
10. DeLise, A. M., Stringa, E., Woodward, W. A., Mello, M. A. and Tuan, R. S. (2000). Embryonic limb mesenchyme micromass culture as an in vitro model for chondrogenesis and cartilage maturation. Methods Mol. Biol. 137, 359-375.
11. 2 tensions and the prevention of differentiation of hES cells. Proc. Natl. Acad. Sci. USA 102, 4783-4788.
12. Feinberg, R. N., Latker, C. H. and Beebe, D. C. (1986). Localized vascular regression during limb morphogenesis in the chicken embryo. I. Spatial and temporal changes in the vascular pattern. Anat. Rec. 214, 405-409.
13. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. and Semenza, G. L. (1996). Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4604-4613.
14. Gong, Y., Krakow, D., Marcelino, J., Wilkin, D., Chitayat, D., Babul-Hirji, R., Hudgins, L., Cremers, C. W., Cremers, F. P., Brunner, H. G. et al. (1999). Heterozygous mutations in the gene encoding noggin affect human joint morphogenesis. Nat. Genet. 21, 302-304.
15. Gustafsson, M. V., Zheng, X., Pereira, T., Gradin, K., Jin, S., Lundkvist, J., Ruas, J. L., Poellinger, L., Lendahl, U. and Bondesson, M. (2005). Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9, 617-628.
16. Hallmann, R., Feinberg, R. N., Latker, C. H., Sasse, J. and Risau, W. (1987). Regression of blood vessels precedes cartilage differentiation during chick limb development. Differentiation 34, 98-105.
17. Hartmann, C. and Tabin, C. J. (2001). Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104, 341-351.
18. Hogan, K. A., Ambler, C. A., Chapman, D. L. and Bautch, V. L. (2004). The neural tube patterns vessels developmentally using the VEGF signaling pathway. Development 131, 1503-1513.
19. 2-regulated prolyl hydroxylation. Science 292, 468-472.
20. Karsenty, G. and Wagner, E. F. (2002). Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2, 389-406.
21. Kjaer, K. W., Eiberg, H., Hansen, L., van der Hagen, C. B., Rosendahl, K., Tommerup, N. and Mundlos, S. (2006). A mutation in the receptor binding site of GDF5 causes Mohr-Wriedt brachydactyly type A2. J. Med. Genet. 43, 225-231.
22. Kronenberg, H. M. (2003). Developmental regulation of the growth plate. Nature 423, 332-336.
23. Lehmann, K., Seemann, P., Stricker, S., Sammar, M., Meyer, B., Suring, K., Majewski, F., Tinschert, S., Grzeschik, K. H., Muller, D. et al. (2003). Mutations in bone morphogenetic protein receptor 1B cause brachydactyly type A2. Proc. Natl. Acad. Sci. USA 100, 12277-12282.
24. Liu, Y., Cox, S. R., Morita, T. and Kourembanas, S. (1995). Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ. Res. 77, 638-643.
25. Logan, M., Martin, J. F., Nagy, A., Lobe, C., Olson, E. N. and Tabin, C. J. (2002). Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80.
26. Maltepe, E. and Simon, M. C. (1998). Oxygen, genes, and development: an analysis of the role of hypoxic gene regulation during murine vascular development. J. Mol. Med. 76, 391-401.
27. Maltepe, E., Schmidt, J. V., Baunoch, D., Bradfield, C. A. and Simon, M. C. (1997). Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386, 403-407.
28. Marcelino, J., Sciortino, C. M., Romero, M. F., Ulatowski, L. M., Ballock, R. T., Economides, A. N., Eimon, P. M., Harland, R. M. and Warman, M. L. (2001). Human disease-causing NOG missense mutations: effects on noggin secretion, dimer formation, and bone morphogenetic protein binding. Proc. Natl. Acad. Sci. USA 98, 11353-11358.
29. McLeod, M. J. (1980). Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22, 299-301.
30. Mitchell, J. A. and Yochim, J. M. (1968). Measurement of intrauterine oxygen tension in the rat and its regulation by ovarian steroid hormones. Endocrinology 83, 691-700.
31. Mitrovic, D. R. (1977). Development of the metatarsophalangeal joint of the chick embryo: morphological, ultrastructural and histochemical studies. Am. J. Anat. 150, 333-347.
32. Mori-Akiyama, Y., Akiyama, H., Rowitch, D. H. and de Crombrugghe, B. (2003). Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc. Natl. Acad. Sci. USA 100, 9360-9365.
33. Murtaugh, L. C., Chyung, J. H. and Lassar, A. B. (1999). Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev. 13, 225-237.
34. Olsen, B. R., Reginato, A. M. and Wang, W. (2000). Bone development. Annu. Rev. Cell Dev. Biol. 16, 191-220.
35. Oster, G. F., Shubin, N., Murray, J. D. and Alberch, P. (1988). Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogeny. Evolution 42, 862-884.
36. Pacifici, M., Koyama, E. and Iwamoto, M. (2005). Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries. Birth Defects Res. C Embryo Today 75, 237-248.
37. Ramirez-Bergeron, D. L., Runge, A., Dahl, K. D., Fehling, H. J., Keller, G. and Simon, M. C. (2004). Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development 131, 4623-4634.
38. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
39. Robins, J. C., Akeno, N., Mukherjee, A., Dalal, R. R., Aronow, B. J., Koopman, P. and Clemens, T. L. (2005). Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone 37, 313-322.
40. Rodesch, F., Simon, P., Donner, C. and Jauniaux, E. (1992). Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet. Gynecol. 80, 283-285.
41. Ryan, H. E., Poloni, M., McNulty, W., Elson, D., Gassmann, M., Arbeit, J. M. and Johnson, R. S. (2000). Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 60, 4010-4015.
42. Salim, A., Nacamuli, R. P., Morgan, E. F., Giaccia, A. J. and Longaker, M. T. (2004). Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J. Biol. Chem. 279, 40007-40016.
43. Schipani, E., Ryan, H. E., Didrickson, S., Kobayashi, T., Knight, M. and Johnson, R. S. (2001). Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 15, 2865-2876.
44. Schofield, C. J. and Ratcliffe, P. J. (2004). Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354.
45. Seemann, P., Schwappacher, R., Kjaer, K. W., Krakow, D., Lehmann, K., Dawson, K., Stricker, S., Pohl, J., Ploger, F., Staub, E. et al. (2005). Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J.. Clin. Invest. 115, 2373-2381.
46. 2 homeostasis. Curr. Opin. Genet. Dev. 8, 588-594.
47. Semenza, G. L. (2003). Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
48. Semenza, G. L. (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology Bethesda 19, 176-182.
49. Semenza, G. L., Agani, F., Iyer, N., Kotch, L., Laughner, E., Leung, S. and Yu, A. (1999). Regulation of cardiovascular development and physiology by hypoxia-inducible factor 1. Ann. N. Y. Acad. Sci. 874, 262-268.
50. Smits, P., Li, P., Mandel, J., Zhang, Z., Deng, J. M., Behringer, R. R., de Crombrugghe, B. and Lefebvre, V. (2001). The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell 1, 277-290.
51. Storm, E. E. and Kingsley, D. M. (1999) GDF5 coordinates bone and joint formation during digit development. Dev. Biol. 209, 11-27.
52. Studer, L., Csete, M., Lee, S. H., Kabbani, N., Walikonis, J., Wold, B. and McKay, R. (2000). Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J. Neurosci. 20, 7377-7383.
53. Tiscornia, G., Singer, O. and Verma, I. M. (2006). Production and purification of lentiviral vectors. Nat. Protoc. 1, 241-245.
54. Tylzanowski, P., Mebis, L. and Luyten, F. P. (2006). The Noggin null mouse phenotype is strain dependent and haploinsufficiency leads to skeletal defects. Dev. Dyn. 235, 1599-1607.
55. Wenger, R. H., Stiehl, D. P. and Camenisch, G. (2005). Integration of oxygen signaling at the consensus HRE. Sci. STKE 306, re12.
56. Yun, Z., Maecker, H. L., Johnson, R. S. and Giaccia, A. J. (2002). Inhibition of PPAR garnma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev. Cell 2, 331-341.