Fetal growth plate: A developmental model of cellular adaptation to hypoxia

Annals of the New York Academy of Sciences

Volumn 1117, Issue , 2007, Pages 26-39

  Provot, Sylvain ^a   Schipani, Ernestina ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Chondrocytes; Hif 1 ; Hypoxia; Joint; Mensenchymal cells; VEGF; VHL

Indexed keywords

BETA GALACTOSIDASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEASOME; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

ADAPTATION; BIOLOGICAL MODEL; CARTILAGE CELL; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CHONDROGENESIS; CONFERENCE PAPER; DEGRADATION; ENCHONDRAL OSSIFICATION; ENZYME DEGRADATION; FETUS GROWTH; HUMAN; HYPOXIA; MESENCHYME CELL; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM;

EID: 36549065233     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1196/annals.1402.076     Document Type: Conference Paper

References (62)

1. CHEN, E., M. FUJINAGA & A. GIACCIA. 1999. Hypoxic microenvironment within an embryo induces apoptosis and is essential for proper morphological development. Teratology 60: 215-225.
2. GIACCIA, A., M. SIMON & R. JOHNSON. 2004. The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev. 18: 2183-2194.
3. BUNN, H. & R. POYTON. 1996. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76: 839-885.
4. KAELIN, W. 2002. Howoxygen makes its presence felt. Genes Dev. 16: 1441-1445.
5. GIACCIA, A., B. SIIM & R. JOHNSON. 2003. HIF-1 as a target for drug development. Nat. Rev. Drug Discov. 2: 803-811.
6. SEMENZA, G. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3: 721-732.
7. LIU, L. & M. SIMON. 2004. Regulation of transcription and translation by hypoxia. Cancer Biol. Ther. 3: 492-497.
8. GORDAN, J. & M. SIMON. 2007. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr. Opin. Genet. Dev. 17: 71-77.
9. POUYSSEGUR, J., F. DAYAN & N. MAZURE. 2006. Hypoxia signaling in cancer and approaches to enforce tumour regression. Nature 441: 437-443.
10. KALLIO, P.J. et al. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 17: 6573-6586.
11. BISHOP, T. et al. 2004. Genetic analysis of pathways regulated by the von Hippel-Lindau tumor suppressor in Caenorhabditis elegans. PLoS Biol. 2: e289.
12. GREIJER, A. et al. 2005. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J. Pathol. 206: 291-304.
13. WYKOFF, C. et al. 2000. Identification of novel hypoxia dependent and independent target genes of the von Hippel Lindau (VHL) tumor suppressor by mRNA differential expression profiling. Oncogene 19: 6297-6305.
14. LEO, C., A. GIACCIA & N. DENKO. 2004. The hypoxic tumor microenvironment and gene expression. Semin. Radiat. Oncol. 14: 207-214.
15. BRUICK, R. 2000. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. USA 97: 9082-9087.
16. WENGER, R. et al. 1998. Mouse hypoxia-inducible factor-1alpha is encoded by two different mRNA isoforms: expression from a tissue-specific ad a housekeeping-type promoter. Blood 91: 3471-3480.
17. OHH, M. & W. KAELIN. 1999. The von Hippel-Lindau tumor suppressor protein: new perspectives. Mol. Med. Today 5: 257-263.
18. IVAN, M. et al. 2001. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468.
19. JAAKKOLA, P. et al. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
20. CHAN, D. et al. 2002. Role of prolyl hydroxylation in oncogenically stabilized hyoxia-inducible factor-1alpha. J. Biol. Chem. 277: 40112-40117.
21. MIN, J. et al. 2002. Structure of an HIF-1alpha-pVHL complex: hydroxyproline recognition in signaling. Science 296: 1886-1889.
22. BERRA, B. et al. 2003. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of Hif-1alpha in normoxia. EMBO J. 22: 4082-4090.
23. LANDO, D. et al. 2002. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16: 1466-1471.
24. KRONENBERG, H. 2003. Developmental regulation of the growth plate. Nature 423: 332-336.
25. PROVOT, S. & E. SCHIPANI. 2005. Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 328: 658-665.
26. IYER, N. et al. 1998a. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1alpha. Genes Dev. 12: 149-162.
27. RYAN, H.E., J. LO & R.S. JOHNSON. 1998. HIF 1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 17: 3005-3015.
28. COMPERNOLLE, V. et al. 2003. Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor -1alpha. Cardiovasc. Res. 60: 569-579.
29. SCHIPANI, E. et al. 2001. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 15: 2865-2876.
30. LEEK, R., I. STRATFORD & A. HARRIS. 2005. The role of hypoxia-inducible factor-1 in three-dimensional tumor growth, apoptosis, and regulation by the insulin-signaling pathway. Cancer Res. 65: 4147-4152.
31. PFANDER, D. et al. 2004. Deletion of Vhlh in chondrocytes reduces cell proliferation and increases matrix deposition during growth plate development. Development 131: 2497-2508.
32. CRAMER, T. et al. 2004. Expression of VEGF isoforms by epithelial chondrocytes during low-oxygen tension is Hif-1alpha dependent. Osteoarthr. Cart. 12: 433-439.
33. PFANDER, D. et al. 2003. HIF-1alpha controls extracellular matrix synthesis by epiphyseal chondrocytes. J. Cell Sci. 116: 1819-1826.
34. FERRARA, N., H. GERBER & J. LECOUTER. 2003. The biology of VEGF and its receptors. Nat. Med. 9: 669-676.
35. ZELZER, E. et al. 2004. VEGFA is necessary for chondrocyte survival during bone development. Development 131: 2161-2171.
36. GNARRA, J. et al. 1997. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc. Natl. Acad. Sci. 94: 9102-9107.
37. CRAMER, T. et al. 2003. Hif-1alpha is essential for myeloid cell-mediated inflammation. Cell 112: 645-657.
38. BIJU, M. et al. 2004. Vhlh gene deletion induces Hif-1-mediated cell death in thymocytes. Mol. Cell Biol. 24: 9038-9047.
39. RANKIN, E. et al. 2005. Inactivation of the arylhydrocarbon receptor nuclear translocator (ARNT) suppresses von Hippel-Lindau disease-associated vascular tumors in mice. Mol. Cell Biol. 25: 3163-3172.
40. RANKIN, E. et al. 2007. Hypoxia-inducible factor 2 (Hif-2) regulates hepatic erythropoietin in vivo. J. Clin. Invest. 117: 1068-1077.
41. WG KAELIN, J. 2005. The von Hippel-Lindau tumor suppressor protein: roles in cancer and oxygen sensing. Cold Spring Harb. Symp. Quant. Biol. 70: 159-166.
42. MACK, F. et al. 2005. Decreased growth of Vhl-/- fibrosarcomas is associated with elevated levels of cyclin kinase inhibitors p21 and p27. Mol. Cell Biol. 25: 4565-4578.
43. GODA, N. et al. 2003. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol. Cell Biol. 23: 359-369.
44. KOSHIJI, M. et al. 2004. Hif-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J. 23: 1949-1956.
45. PROVOT, S. et al. 2007. Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J. Cell Biol. 177: 451-464.
46. LOGAN, M. et al. 2002. Expression of Cre recombinase in the developing mouse limb bud driven by a Prx1 enhancer. Genesis 33: 77-80.
47. LESLIE, M. 2007. The up side of a gas shortage. J. Cell Biol. 177: 371.
48. BRUNET, L. et al. 1998. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280: 1455-1457.
49. STORM, E. & D. KINGSLEY. 1999. GDF5 coordinates bone and joint formation during digit development. Dev. Biol. 209: 11-27.
50. HARTMANN, C. & C. TABIN. 2001. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104: 341-351.
51. KINGSLEY, D. 2001. Genetic control of bone and joint formation. Novartis Found Symp. 232: 213-222.
52. GUO, X. et al. 2004. Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev. 18: 2404-2417.
53. AKIYAMA, H. et al. 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.
54. HUANG, W. et al. 2000. Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocytespecific enhancer. Mol. Cell Biol. 20: 4149-4158.
55. SMITS, P. et al. 2001. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell. 1: 277-290.
56. LEFEBVRE, V. & P. SMITS. 2005. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res. Part C Embryo Today 75: 200-212.
57. MYLLYHARJU, J. & K. KIVIRIKKO. 2004. Collagen, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20: 33-43.
58. SVODOBA, K. 1998. Chondrocyte-matrix attachment complexes mediate survival and differentiation. Microsc. Res. Tech. 43: 111-122.
59. EGERBACHER, M. & G. HAEUSLER. 2003. Integrins in growth plate cartilage. Pediatr. Endocrinol. Rev. 1: 2-8.
60. PACIFICI, M. & R. JOZZO. 1998. Remodeling of the rough endoplasmic reticulum during stimulation of procollagen secretion by ascorbic acid in cultured chondrocytes. A biochemical and morphological study. J. Biol. Chem. 263: 2483-2492.
61. ZHANG, K. & R. KAUFMAN. 2006. Protein folding in the endoplasmic reticulum and the unfolded protein response. Handbook Exp. Pharmacol. 172: 69-91.
62. TSANG, K. et al. 2007. Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol. 5: e44.