The hypoxia-inducible factor 1/NOR-1 axis regulates the survival response of endothelial cells to hypoxia

Molecular and Cellular Biology

Volumn 29, Issue 21, 2009, Pages 5828-5842

  Martorell, Lluis ^a   Gentile, Maurizio ^a   Rius, Jordi ^a,b   Rodríguez, Cristina ^a   Crespo, Javier ^a   Badimon, Lina ^a   Martínez González, José ^a  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INHIBITOR OF APOPTOSIS PROTEIN 2; NEURON DERIVED ORPHAN RECEPTOR 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; RECEPTOR ANTIBODY; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; VASCULOTROPIN RECEPTOR 2;

APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CALCIUM CELL LEVEL; CELL HYPOXIA; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENDOTHELIUM CELL; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SECRETION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TIME; TRANSCRIPTION INITIATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; AUTOCRINE COMMUNICATION; CELL HYPOXIA; CELL SURVIVAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DERMIS; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INHIBITOR OF APOPTOSIS PROTEINS; MICROVESSELS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, STEROID; RECEPTORS, THYROID HORMONE; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; UMBILICAL VEINS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70350547779     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00945-09     Document Type: Article

References (62)

1. Alfranca, A., M. D. Gutiérrez, A. Vara, J. Aragonés, F. Vidal, and M. O. Landázuri. 2002. c-Jun and hypoxia-inducible factor 1 functionally cooperate in hypoxia-induced gene transcription. Mol. Cell. Biol. 22:12-22.
2. Ali, M. A., H. Choy, A. A. Habib, and D. Saha. 2007. SNS-032 prevents tumor cell-induced angiogenesis by inhibiting vascular endothelial growth factor. Neoplasia 9:370-381. (Pubitemid 46799980)
3. Alvarez-Tejado, M., S. Naranjo-Suarez, C. Jiménez, A. C. Carrera, M. O. Landázuri, and L. del Peso. 2001. Hypoxia induces the activation of the phosphatidylinositol 3-kinase/Akt cell survival pathway in PC12 cells: protective role in apoptosis. J. Biol. Chem. 276:22368-22374.
4. Arkenbout, E. K., M. van Bragt, E. Eldering, C. van Bree, J. M. Grimbergen, P. H. Quax, H. Pannekoek, and C. J. de Vries. 2003. TR3 orphan receptor is expressed in vascular endothelial cells and mediates cell cycle arrest. Arterioscler. Thromb. Vasc. Biol. 23:1535-1540.
5. Arkenbout, E. K., V. de Waard, M. van Bragt, T. A. van Achterberg, J. M. Grimbergen, B. Pichon, H. Pannekoek, and C. J. de Vries. 2002. Protective function of transcription factor TR3 orphan receptor in atherogenesis: decreased lesion formation in carotid artery ligation model in TR3 transgenic mice. Circulation 106:1530-1535.
6. Biliran, H., Jr., Y. Wang, S. Banerjee, H. Xu, H. Heng, A. Thakur, A. Bollig, F. H. Sarkar, and J. D. Liao. 2005. Overexpression of cyclin D1 promotes tumor cell growth and confers resistance to cisplatin-mediated apoptosis in an elastase-myc transgene-expressing pancreatic tumor cell line. Clin. Cancer Res. 11:6075-6086.
7. Björnheden, T., M. Levin, M. Evaldsson, and O. Wiklund. 1999. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler. Thromb. Vasc. Biol. 19:870-876.
8. Calvani, M., A. Rapisarda, B. Uranchimeg, R. H. Shoemaker, and G. Melillo. 2006. Hypoxic induction of an HIF-1alpha-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells. Blood 107:2705-2712.
9. Carmeliet, P. 2003. Angiogenesis in health and disease. Nat. Med. 9:653-660.
10. Cheng, L. E., F. K. Chan, D. Cado, and A. Winoto. 1997. Functional redundancy of the Nur77 and Nor-1 orphan steroid receptors in T-cell apoptosis. EMBO J. 16:1865-1875.
11. Choi, J. W., S. C. Park, G. H. Kang, J. O. Liu, and H. D. Youn. 2004. Nur77 activated by hypoxia-inducible factor-1alpha overproduces proopiomelanocortin in von Hippel-Lindau-mutated renal cell carcinoma. Cancer Res. 64:35-39.
12. Crespo, J., J. Martínez-González, J. Rius, and L. Badimon. 2005. Simvastatin inhibits NOR-1 expression induced by hyperlipemia by interfering with CREB activation. Cardiovasc. Res. 67:333-341.
13. Das, M., O. Djahanbakhch, B. Hacihanefioglu, E. Saridogan, M. Ikram, L. Ghali, M. Raveendran, and A. Storey. 2008. Granulosa cell survival and proliferation are altered in polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 93:881-887.
14. DeYoung, R. A., J. C. Baker, D. Cado, and A. Winoto. 2003. The orphan steroid receptor Nur77 family member Nor-1 is essential for early mouse embryogenesis. J. Biol. Chem. 278:47104-47109.
15. Ferrara, N., H. P. Gerber, and J. LeCouter. 2003. The biology of VEGF and its receptors. Nat. Med. 9:669-676.
16. Greijer, A. E., and E. van der Wall. 2004. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J. Clin. Pathol. 57:1009-1014.
17. Hänze, J., N. Weissmann, F. Grimminger, W. Seeger, and F. Rose. 2007. Cellular and molecular mechanisms of hypoxia-inducible factor driven vascular remodeling. Thromb. Haemost. 97:774-787.
18. Honkaniemi, J., and F. R. Sharp. 1996. Global ischemia induces immediate-early genes encoding zinc finger transcription factors. J. Cereb. Blood Flow Metab. 16:557-565.
19. Hudson, C. C., M. Liu, G. G. Chiang, D. M. Otterness, D. C. Loomis, F. Kaper, A. J. Giaccia, and R. T. Abraham. 2002. Regulation of hypoxia-inducible factor 1α expression and function by the mammalian target of rapamycin. Mol. Cell. Biol. 22:7004-7014.
20. Hui, A. S., A. L. Bauer, J. B. Striet, P. O. Schnell, and M. F. Czyzyk-Krzeska. 2006. Calcium signaling stimulates translation of HIF-alpha during hypoxia. FASEB J. 20:466-475.
21. Inuzuka, H., H. Tokumitsu, N. Ohkura, and R. Kobayashi. 2002. Transcriptional regulation of nuclear orphan receptor, NOR-1, by Ca(2+)/calmodulin-dependent protein kinase cascade. FEBS Lett. 522:88-92.
22. Kim, Y., S. Hong, M. R. Noh, S. Y. Kim, P. W. Huh, S. H. Park, W. Sun, and H. Kim. 2006. Induction of neuron-derived orphan receptor-1 in the dentate gyrus of the hippocampal formation following transient global ischemia in the rat. Mol. Cells 22:8-12. (Pubitemid 44323039)
23. Kuwahara, F., H. Kai, K. Tokuda, R. Shibata, K. Kusaba, N. Tahara, H. Niiyama, T. Nagata, and T. Imaizumi. 2002. Hypoxia-inducible factor-1alpha/vascular endothelial growth factor pathway for adventitial vasa vasorum formation in hypertensive rat aorta. Hypertension 39:46-50. (Pubitemid 34098087)
24. Lee, S. H., M. Y. Lee, J. H. Lee, and H. J. Han. 2008. A potential mechanism for short time exposure to hypoxia-induced DNA synthesis in primary cultured chicken hepatocytes: correlation between Ca(2+)/PKC/MAPKs and PI3K/Akt/mTOR. J. Cell. Biochem. 104:1598-1611.
25. Liao, H., M. C. Hyman, D. A. Lawrence, and D. J. Pinsky. 2007. Molecular regulation of the PAI-1 gene by hypoxia: contributions of Egr-1, HIF-1α, and C/EBPα. FASEB J. 21:935-949. (Pubitemid 46348266)
26. Liu, D., H. Jia, D. I. Holmes, A. Stannard, and I. Zachary. 2003. Vascular endothelial growth factor-regulated gene expression in endothelial cells: KDR-mediated induction of Egr3 and the related nuclear receptors Nur77, Nurr1, and Nor1. Arterioscler. Thromb. Vasc. Biol. 23:2002-2007.
27. Liu, Z. G., S. W. Smith, K. A. McLaughlin, L. M. Schwartz, and B. A. Osborne. 1994. Apoptotic signals delivered through the T-cell receptor of a T-cell hybrid require the immediate-early gene Nur77. Nature 367:281-284.
28. Maltais, A., C. Filion, and Y. Labelle. 2002. The AF2 domain of the orphan nuclear receptor TEC is essential for the transcriptional activity of the oncogenic fusion protein EWS/TEC. Cancer Lett. 183:87-94. (Pubitemid 34607355)
29. Manalo, D. J., A. Rowan, T. Lavoie, L. Natarajan, B. D. Kelly, S. Q. Ye, J. G. García, and G. L. Semenza. 2005. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659-669. (Pubitemid 40070750)
30. Mangelsdorf, D. J., C. Thummel, M. Beato, P. Herrlich, G. Schütz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R. M. Evans. 1995. The nuclear receptor superfamily: the second decade. Cell 83:835-839. (Pubitemid 126663112)
31. Martínez-González, J., and L. Badimon. 2005. The NR4A subfamily of nuclear receptors: new early genes regulated by growth factors in vascular cells. Cardiovasc. Res. 65:609-618.
32. Martínez-González, J., J. Rius, A. Castelló, C. Cases-Langhoff, and L. Badimon. 2003. Neuron-derived orphan receptor-1 (NOR-1) modulates vascular smooth muscle cell proliferation. Circ. Res. 92:96-103.
33. Martorell, L., J. Martínez-González, J. Crespo, O. Calvayrac, and L. Badimon. 2007. Neuron-derived orphan receptor-1 (NOR-1) is induced by thrombin and mediates vascular endothelial cell growth. J. Thromb. Haemost. 5:1766-1773.
34. Mayerhofer, M., P. Valent, W. R. Sperr, J. D. Griffin, and C. Sillaber. 2002. BCR/ABL induces expression of vascular endothelial growth factor and its transcriptional activator, hypoxia inducible factor-1alpha, through a pathway involving phosphoinositide 3-kinase and the mammalian target of rapamycin. Blood 100:3767-3775. (Pubitemid 35303950)
35. Mayo, L. D., K. M. Kessler, R. Pincheira, R. S. Warren, and D. B. Donner. 2001. Vascular endothelial cell growth factor activates CRE-binding protein by signaling through the KDR receptor tyrosine kinase. J. Biol. Chem. 276:25184-25189.
36. Mayr, B., and M. Montminy. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2:599-609.
37. Min, J., Y. M. Jin, J. S. Moon, M. S. Sung, S. A. Jo, and I. Jo. 2006. Hypoxia-induced endothelial NO synthase gene transcriptional activation is mediated through the tax-responsive element in endothelial cells. Hypertension 47:1189-1196.
38. Nagamatsu, T., T. Fujii, M. Kusumi, L. Zou, T. Yamashita, Y. Osuga, M. Momoeda, S. Kozuma, and Y. Taketani. 2004. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 145:4838-4845. (Pubitemid 39551100)
39. Nomiyama, T., T. Nakamachi, F. Gizard, E. B. Heywood, K. L. Jones, N. Ohkura, R. Kawamori, O. M. Conneely, and D. Bruemmer. 2006. The NR4A orphan nuclear receptor NOR1 is induced by platelet-derived growth factor and mediates vascular smooth muscle cell proliferation. J. Biol. Chem. 281:33467-33476.
40. Nomiyama, T., Y. Zhao, F. Gizard, H. M. Findeisen, E. B. Heywood, K. L. Jones, O. M. Conneely, and D. Bruemmer. 2009. Deficiency of the NR4A neuron-derived orphan receptor-1 attenuates neointima formation after vascular injury. Circulation 119:577-586.
41. Ohkubo, T., N. Ohkura, K. Maruyama, K. Sasaki, K. Nagasaki, H. Hanzawa, T. Tsukada, and K. Yamaguchi. 2000. Early induction of the orphan nuclear receptor NOR-1 during cell death of the human breast cancer cell line MCF-7. Mol. Cell. Endocrinol. 162:151-156.
42. Ohkura, N., M. Hijikuro, A. Yamamoto, and K. Miki. 1994. Molecular cloning of a novel thyroid/steroid receptor superfamily gene from cultured rat neuronal cells. Biochem. Biophys. Res. Commun. 205:1959-1965.
43. Pei, L., A. Castrillo, M. Chen, A. Hoffmann, and P. Tontonoz. 2005. Induction of NR4A orphan nuclear receptor expression in macrophages in response to inflammatory stimuli. J. Biol. Chem. 280:29256-29262.
44. Pei, L., A. Castrillo, and P. Tontonoz. 2006. Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77. Mol. Endocrinol. 20:786-794.
45. Pichiule, P., J. C. Chavez, and J. C. LaManna. 2004. Hypoxic regulation of angiopoietin-2 expression in endothelial cells. J. Biol. Chem. 279:12171-12180.
46. Ponnio, T., and O. M. Conneely. 2004. NOR-1 regulates hippocampal axon guidance, pyramidal cell survival, and seizure susceptibility. Mol. Cell. Biol. 24:9070-9078.
47. Pouysségur, J., F. Dayan, and N. M. Mazure. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437-443. (Pubitemid 44050138)
48. Pugh, C. W., and P. J. Ratcliffe. 2003. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 9:677-684.
49. Rius, J., J. Martinez-Gonzalez, J. Crespo, and L. Badimon. 2004. Involvement of neuron-derived orphan receptor-1 (NOR-1) in LDL-induced mitogenic stimulus in vascular smooth muscle cells: role of CREB. Arterioscler. Thromb. Vasc. Biol. 24:697-702.
50. Rius, J., J. Martinez-Gonzalez, J. Crespo, and L. Badimon. 2006. NOR-1 is involved in VEGF-induced endothelial cell growth. Atherosclerosis 184:276-282. (Pubitemid 43049710)
51. Safran, M., and W. G. Kaelin, Jr. 2003. HIF hydroxylation and the mammalian oxygen-sensing pathway. J. Clin. Investig. 111:779-783.
52. Salvesen, G. S., and C. S. Duckett. 2002. IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell Biol. 3:401-410.
53. Semenza, G. L. 2009. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda) 24:97-106.
54. Semenza, G. L. 2000. Surviving ischemia: adaptive responses mediated by hypoxia-inducible factor 1. J. Clin. Investig. 106:809-812.
55. Suzuki, S., N. Suzuki, C. Mirtsos, T. Horacek, E. Lye, S. K. Noh, A. Ho, D. Bouchard, T. W. Mak, and W. C. Yeh. 2003. Nur77 as a survival factor in tumor necrosis factor signaling. Proc. Natl. Acad. Sci. USA 100:8276-8280.
56. Wang, Z., G. Benoit, J. Liu, S. Prasad, P. Aarnisalo, X. Liu, H. Xu, N. P. Walker, and T. Perlmann. 2003. Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423:555-560. (Pubitemid 36648581)
57. Wilson, S. H., J. Herrmann, L. O. Lerman, D. R. Holmes, Jr., C. Napoli, E. L. Ritman, and A. Lerman. 2002. Simvastatin preserves the structure of coronary adventitial vasa vasorum in experimental hypercholesterolemia independent of lipid lowering. Circulation 105:415-418. (Pubitemid 34141695)
58. Yoo, Y. G., M. G. Yeo, D. K. Kim, H. Park, and M. O. Lee. 2004. Novel function of orphan nuclear receptor Nur77 in stabilizing hypoxia-inducible factor-1alpha. J. Biol. Chem. 279:53365-53373.
59. Yoo, Y. G., T. Y. Na, W. K. Yang, H. J. Kim, I. K. Lee, G. Kong, J. H. Chung, and M. O. Lee. 2007. 6-Mercaptopurine, an activator of Nur77, enhances transcriptional activity of HIF-1alpha resulting in new vessel formation. Oncogene 26:3823-3834.
60. Yuan, G., J. Nanduri, C. R. Bhasker, G. L. Semenza, and N. R. Prabhakar. 2005. Ca2+/calmodulin kinase-dependent activation of hypoxia inducible factor 1 transcriptional activity in cells subjected to intermittent hypoxia. J. Biol. Chem. 280:4321-4328.
61. Zeng, H., L. Qin, D. Zhao, X. Tan, E. J. Manseau, M. Van Hoang, D. R. Senger, L. F. Brown, J. A. Nagy, and H. F. Dvorak. 2006. Orphan nuclear receptor TR3/Nur77 regulates VEGF-A-induced angiogenesis through its transcriptional activity. J. Exp. Med. 203:719-729.
62. Zetterstrom, R. H., L. Solomin, T. Mitsiadis, L. Olson, and T. Perlmann. 1996. Retinoid X receptor heterodimerization and developmental expression distinguish the orphan nuclear receptors NGFI-B, Nurr1, and Nor1. Mol. Endocrinol. 10:1656-1666.