Placental but not heart defects are associated with elevated hypoxia-inducible factor α levels in mice lacking prolyl hydroxylase domain protein 2

Molecular and Cellular Biology

Volumn 26, Issue 22, 2006, Pages 8336-8346

  Takeda, Kotaro ^a   Ho, Vivienne C ^a   Takeda, Hiromi ^a   Duan, Li Juan ^a   Nagy, Andras ^b   Fong, Guo Hua ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL HYDROXYLASE DOMAIN PROTEIN 1; PROLYL HYDROXYLASE DOMAIN PROTEIN 2; PROLYL HYDROXYLASE DOMAIN PROTEIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GCM1 GENE; GENE; GENE DISRUPTION; GIANT CELL; MASH2 GENE; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHD1 GENE; PHD2 GENE; PHD3 GENE; PLACENTA DISORDER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STABILITY; TFEB GENE; TROPHOBLAST;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARDIOVASCULAR SYSTEM; CELL HYPOXIA; GENE TARGETING; GIANT CELLS; HEART DEFECTS, CONGENITAL; HYPOXIA-INDUCIBLE FACTOR 1; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLACENTA; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN ISOFORMS;

EID: 33750976389     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00425-06     Document Type: Article

References (38)

1. Adelman, D. M., M. Gertsenstein, A. Nagy, M. C. Simon, and E. Maltepe. 2000. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev. 14:3191-3203.
2. Appelhoff, R. J., Y. M. Tian, R. R. Raval, H. Turley, A. L. Harris, C. W. Pugh, P. J. Ratcliffe, and J. M. Gleadle. 2004. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 279:38458-38465.
3. Berra, E., E. Benizri, A. Ginouves, V. Volmat, D. Roux, and J. Pouyssegur. 2003. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1α in normoxia. EMBO J. 22:4082-4090.
4. Bruick, R. K., and S. L. McKnight. 2001. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337-1340.
5. Cowden Dahl, K. D., B. H. Fryer, F. A. Mack, V. Compernolle, E. Maltepe, D. M. Adelman, P. Carmeliet, and M. C. Simon. 2005. Hypoxia-inducible factors 1α and 2α regulate trophoblast differentiation. Mol. Cell. Biol. 25:10479-10491.
6. D'Angelo, G., E. Duplan, N. Boyer, P. Vigne, and C. Frelin. 2003. Hypoxia up-regulates prolyl hydroxylase activity: a feedback mechanism that limits HIF-1 responses during reoxygenation. J. Biol. Chem. 278:38183-38187.
7. Epstein, A. C., J. M. Gleadle, L. A. McNeill, K, S. Hewitson, J. O'Rourke, D. R. Mole, M. Mukherji, E. Metzen, M. I. Wilson, A. Dhanda, Y. M. Tian, N. Masson, D. L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P. H. Maxwell, C. W. Pugh, C. J. Schofield, and P. J. Ratcliffe. 2001. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:43-54.
8. Forsythe, J. A., B. H. Jiang, N. V. Iyer, F. Agani, S. W. Leung, R. D. Koos, and G. L. Semenza. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
9. Gnarra, J. R., J. M. Ward, F. D. Porter, J. R. Wagner, D. E. Devor, A. Grinberg, M. R. Emmert-Buck, H. Westphal, R. D. Klausner, and W. M. Linehan. 1997. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc. Natl. Acad. Sci. USA 94:9102-9107.
10. Hirsila, M., P. Koivunen, V. Gunzler, K. I. Kivirikko, and J. Myllyharju. 2003. Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J. Biol. Chem. 278:30772-30780.
11. Ivan, M., K. Kondo, H. Yang, W. Kim, J. Valiando, M. Ohh, A. Salic, J. M. Asara, W. S. Lane, and W. G. Kaelin, Jr. 2001. HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468.
12. Iyer, N. V., L. E. Kotch, F. Agani, S. W. Leung, E. Laughner, R. H. Wenger, M. Gassmann, J. D. Gearhart, A. M. Lawler, A. Y. Yu, and G. L. Semenza. 1998. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12:149-162.
13. Jaakkola, P., D. R. Mole, Y. M. Tian, M. I. Wilson, J. Gielbert, S. J. Gaskell, A. Kriegsheim, H. F. Hebestreit, M. Mukherji, C. J. Schofield, P. H. Maxwell, C. W. Pugh, and P. J. Ratcliffe. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468-472.
14. Lakso, M., J. G. Pichel, J. R. Gorman, B. Sauer, Y. Okamoto, E. Lee, F. W. Alt, and H. Westphal. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93:5860-5865.
15. Lee, Y. M., C. H. Jeong, S. Y. Koo, M. J. Son, H. S. Song, S. K. Bae, J. A. Raleigh, H. Y. Chung, M. A. Yoo, and K. W. Kim. 2001. Determination of hypoxic region by hypoxia marker in developing mouse embryos in vivo: a possible signal for vessel development. Dev. Dyn. 220:175-186.
16. Lieb, M. E., K. Menzies, M. C. Moschella, R. Ni, and M. B. Taubman. 2002. Mammalian EGLN genes have distinct patterns of mRNA expression and regulation. Biochem. Cell Biol. 80:421-426.
17. Liu, P., N. A. Jenkins, and N. G. Copeland. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 13:476-484.
18. Maltepe, E., J. V. Schmidt, D. Baunoch, C. A. Bradfield, and M. C. Simon. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403-407.
19. Masson, N., and P. J. Ratcliffe. 2003. HIF prolyl and asparaginyl hydroxylases in the biological response to intracellular O(2) levels. J. Cell Sci. 116:3041-3049.
20. Maxwell, P. H., M. S. Wiesener, G. W. Chang, S. C. Clifford, E. C. Vaux, M. E. Cockman, C. C. Wykoff, C. W. Pugh, E. R. Maher, and P. J. Ratcliffe. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275.
21. Metzen, E., U. Berchner-Pfannschmidt, P. Stengel, J. H. Marxsen, I. Stolze, M. Klinger, W. Q. Huang, C. Wotzlaw, T. Hellwig-Burgel, W. Jelkmann, H. Acker, and J. Fandrey. 2003. Intracellular localisation of human HIF-1 α hydroxylases: implications for oxygen sensing. J. Cell Sci. 116:1319-1326.
22. Nagy, A., J. Rossant, R. Nagy, W. Abramow-Newerly, and J. C. Roder. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90:8424-8428.
23. Nakamura, Y., Y. Hamada, T. Fujiwara, H. Enomoto, T. Hiroe, S. Tanaka. M. Nose, M. Nakahara, N. Yoshida, T. Takenawa, and K. Fukami. 2005. Phospholipase C-δ1 and δ3 are essential in the trophoblast for placental development. Mol. Cell. Biol. 25:10979-10988.
24. Ozer, A., L. C. Wu, and R. K. Bruick. 2005. The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF). Proc. Natl. Acad. Sci. USA 102:7481-7486.
25. Peng, J., L. Zhang, L. Drysdale, and G. H. Fong. 2000. The transcription factor EPAS-1/hypoxia-inducible factor 2α plays an important role in vascular remodeling. Proc. Natl. Acad. Sci. USA 97:8386-8391.
26. Percy, M. J., Q. Zhao, A. Flores, C. Harrison, T. R. Lappin, P. H. Maxwell, M. F. McMullin, and F. S. Lee. 2006. From the cover: a family with erythrocytosis establishes a role for prolyl hydroxylase domain protein 2 in oxygen homeostasis. Proc. Natl. Acad. Sci. USA 103:654-659.
27. Roberts, A. W., L. Robb, S. Rakar, L. Hartley, L. Cluse, N. A. Nicola, D. Metcalf, D. J. Hilton, and W. S. Alexander. 2001. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. USA 98:9324-9329.
28. Rossant, J., and J. C. Cross. 2001. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2:538-548.
29. Ryan, H. E., J. Lo, and R. S. Johnson. 1998. HIF-1 α is required for solid tumor formation and embryonic vascularization. EMBO J. 17:3005-3015.
30. Semenza, G. L. 1998. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr. Opin. Genet. Dev. 8:588-594.
31. Semenza, G. L., M. K. Nejfelt, S. M. Chi, and S. E. Antonarakis. 1991. Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene. Proc. Natl. Acad. Sci. USA 88:5680-5684.
32. Semenza, G. L., P. H. Roth, H. M. Fang, and G. L. Wang. 1994. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269:23757-23763.
33. Tian, H., R. E. Hammer, A. M. Matsumoto, D. W. Russell, and S. L. McKnight. 1998. The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev. 12:3320-3324.
34. To, K. K., and L. E. Huang. 2005. Suppression of HIF-1α transcriptional activity by the HIF prolyl hydroxylase EGLN1. J. Biol. Chem.
35. Wang, G. L., B. H. Jiang, E. A. Rue, and G. L. Semenza. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92:5510-5514.
36. Wiesener, M. S., H. Turley, W. E. Allen, C. Willam, K. U. Eckardt, K. L. Talks, S. M. Wood, K. C. Gatter, A. L. Harris, C. W. Pugh, P. J. Ratcliffe, and P. H. Maxwell. 1998. Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1α. Blood 92:2260-2268.
37. Wilkinson, D. G., and M. A. Nieto. 1993. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225:361-373.
38. Withington, S. L., A. N. Scott, D. N. Saunders, K. Lopes Floro, J. I. Preis, J. Michalicek, K. Maclean, D. B. Sparrow, J. P. Barbera, and S. L. Dunwoodie. 2006. Loss of Cited2 affects trophoblast formation and vascularization of the mouse placenta. Dev. Biol. 294:67-82.