© 1995 American Heart Association, Inc.
Articles |
Hypoxia Regulates Vascular Endothelial Growth Factor Gene Expression in Endothelial Cells
Identification of a 5' Enhancer
From the Joint Program in Neonatology, Harvard Medical School and Children's Hospital, Boston, Mass.
Correspondence to Dr Stella Kourembanas, Joint Program in Neonatology, Children's Hospital, 300 Longwood Ave, Enders 9, Boston, MA 02115. E-mail kourembanas@a1.tch.harvard.edu.
Abstract Vascular endothelial growth factor (VEGF) is a potent mitogen specific for endothelial cells. Its expression is dramatically induced by low oxygen tension in a variety of cell types, and it has been suggested to be a key mediator of hypoxia-induced angiogenesis. Although VEGF action is targeted to endothelial cells, it is generally believed that these cells do not express VEGF. In addition, the mechanisms by which hypoxia regulates VEGF production remain unclear. We report in the present study that pulmonary artery endothelial cells do not express VEGF under basal conditions; however, significant VEGF mRNA levels accumulate when these cells are exposed to hypoxia. Using a DNA fragment containing human VEGF promoter sequence, we identified a 28-bp element that is necessary and sufficient to upregulate transcription in response to hypoxia. This element can act as a hypoxia-specific enhancer when placed upstream or downstream from a heterologous promoter. The enhancer includes, in addition to an octamer homologous to the hypoxia-inducible factor-1 (HIF-1) consensus, a sequence that resides 3' to the consensus. Although this sequence may not be involved in the binding of HIF-1, it is absolutely required for the enhancer activity and may be the binding site for certain constitutive binding proteins. The expression of VEGF by endothelial cells in response to hypoxia may provide an important mechanism by which endothelial cell permeability and proliferation is regulated in an autocrine manner.
Key Words: hypoxia • vascular endothelial growth factor • endothelial cells • gene regulation • enhancer
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C. K. Sen, S. Khanna, B. M. Babior, T. K. Hunt, E. C. Ellison, and S. Roy Oxidant-induced Vascular Endothelial Growth Factor Expression in Human Keratinocytes and Cutaneous Wound Healing J. Biol. Chem., August 30, 2002; 277(36): 33284 - 33290. [Abstract] [Full Text] [PDF]
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N. Gao, M. Ding, J. Z. Zheng, Z. Zhang, S. S. Leonard, K. J. Liu, X. Shi, and B.-H. Jiang Vanadate-induced Expression of Hypoxia-inducible Factor 1alpha and Vascular Endothelial Growth Factor through Phosphatidylinositol 3-Kinase/Akt Pathway and Reactive Oxygen Species J. Biol. Chem., August 23, 2002; 277(35): 31963 - 31971. [Abstract] [Full Text] [PDF]
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S. F. Abcouwer, P. L. Marjon, R. K. Loper, and D. L. Vander Jagt Response of VEGF Expression to Amino Acid Deprivation and Inducers of Endoplasmic Reticulum Stress Invest. Ophthalmol. Vis. Sci., August 1, 2002; 43(8): 2791 - 2798. [Abstract] [Full Text] [PDF]
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R. H. WENGER Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression FASEB J, August 1, 2002; 16(10): 1151 - 1162. [Abstract] [Full Text] [PDF]
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S. J. Leibovich, J.-F. Chen, G. Pinhal-Enfield, P. C. Belem, G. Elson, A. Rosania, M. Ramanathan, C. Montesinos, M. Jacobson, M. A. Schwarzschild, et al. Synergistic Up-Regulation of Vascular Endothelial Growth Factor Expression in Murine Macrophages by Adenosine A2A Receptor Agonists and Endotoxin Am. J. Pathol., June 1, 2002; 160(6): 2231 - 2244. [Abstract] [Full Text] [PDF]
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 S. Hashimoto, N. Minami, R. Takakura, and H. Imai Bovine Immature Oocytes Acquire Developmental Competence During Meiotic Arrest In Vitro Biol Reprod, June 1, 2002; 66(6): 1696 - 1701. [Abstract] [Full Text] [PDF]
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T. Shoshani, A. Faerman, I. Mett, E. Zelin, T. Tenne, S. Gorodin, Y. Moshel, S. Elbaz, A. Budanov, A. Chajut, et al. Identification of a Novel Hypoxia-Inducible Factor 1-Responsive Gene, RTP801, Involved in Apoptosis Mol. Cell. Biol., April 1, 2002; 22(7): 2283 - 2293. [Abstract] [Full Text] [PDF]
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L. D. Ke, Y.-X. Shi, and W. K. A. Yung VEGF121, VEGF165 Overexpression Enhances Tumorigenicity in U251 MG but not in NG-1 Glioma Cells Cancer Res., March 1, 2002; 62(6): 1854 - 1861. [Abstract] [Full Text] [PDF]
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N. M. Mazure, C. Chauvet, B. Bois-Joyeux, M.-A. Bernard, H. Nacer-Cherif, and J.-L. Danan Repression of {alpha}-Fetoprotein Gene Expression under Hypoxic Conditions in Human Hepatoma Cells: Characterization of a Negative Hypoxia Response Element That Mediates Opposite Effects of Hypoxia Inducible Factor-1 and c-Myc Cancer Res., February 1, 2002; 62(4): 1158 - 1165. [Abstract] [Full Text] [PDF]
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 H. O. Akman, H. Zhang, M. A. Q. Siddiqui, W. Solomon, E. L. P. Smith, and O. A. Batuman Response to hypoxia involves transforming growth factor-beta 2 and Smad proteins in human endothelial cells Blood, December 1, 2001; 98(12): 3324 - 3331. [Abstract] [Full Text] [PDF]
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T. Sanchez-Elsner, L. M. Botella, B. Velasco, A. Corbi, L. Attisano, and C. Bernabeu Synergistic Cooperation between Hypoxia and Transforming Growth Factor-beta Pathways on Human Vascular Endothelial Growth Factor Gene Expression J. Biol. Chem., October 12, 2001; 276(42): 38527 - 38535. [Abstract] [Full Text] [PDF]
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A. Orimo, Y. Tomioka, Y. Shimizu, M. Sato, S. Oigawa, K. Kamata, Y. Nogi, S. Inoue, M. Takahashi, T. Hata, et al. Cancer-associated Myofibroblasts Possess Various Factors to Promote Endometrial Tumor Progression Clin. Cancer Res., October 1, 2001; 7(10): 3097 - 3105. [Abstract] [Full Text] [PDF]
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K. Neben, T. Moehler, G. Egerer, A. Kraemer, J. Hillengass, A. Benner, A. D. Ho, and H. Goldschmidt High Plasma Basic Fibroblast Growth Factor Concentration Is Associated with Response to Thalidomide in Progressive Multiple Myeloma Clin. Cancer Res., September 1, 2001; 7(9): 2675 - 2681. [Abstract] [Full Text] [PDF]
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D. A. Davis, A. S. Rinderknecht, J. P. Zoeteweij, Y. Aoki, E. L. Read-Connole, G. Tosato, A. Blauvelt, and R. Yarchoan Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus Blood, May 15, 2001; 97(10): 3244 - 3250. [Abstract] [Full Text] [PDF]
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Q. Shi, X. Le, J. L. Abbruzzese, Z. Peng, C.-N. Qian, H. Tang, Q. Xiong, B. Wang, X.-C. Li, and K. Xie Constitutive Sp1 Activity Is Essential for Differential Constitutive Expression of Vascular Endothelial Growth Factor in Human Pancreatic Adenocarcinoma Cancer Res., May 1, 2001; 61(10): 4143 - 4154. [Abstract] [Full Text]
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M. Cho, T. K. Hunt, and M. Z. Hussain Hydrogen peroxide stimulates macrophage vascular endothelial growth factor release Am J Physiol Heart Circ Physiol, May 1, 2001; 280(5): H2357 - H2363. [Abstract] [Full Text] [PDF]
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 N.M. Siafakas, M. Jordan, H. Wagner, E.C. Breen, H. Benoit, and P.D. Wagner Diaphragmatic angiogenic growth factor mRNA responses to increased ventilation caused by hypoxia and hypercapnia Eur. Respir. J., April 1, 2001; 17(4): 681 - 687. [Abstract] [Full Text] [PDF]
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M. WARTENBERG, F. DONMEZ, F. C. LING, H. ACKER, J. HESCHELER, and H. SAUER Tumor-induced angiogenesis studied in confrontation cultures of multicellular tumor spheroids and embryoid bodies grown from pluripotent embryonic stem cells FASEB J, April 1, 2001; 15(6): 995 - 1005. [Abstract] [Full Text] [PDF]
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 E. M. Conway, D. Collen, and P. Carmeliet Molecular mechanisms of blood vessel growth Cardiovasc Res, February 16, 2001; 49(3): 507 - 521. [Full Text] [PDF]
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K. B. Sandau, J. Fandrey, and B. Brune Accumulation of HIF-1{alpha} under the influence of nitric oxide Blood, February 15, 2001; 97(4): 1009 - 1015. [Abstract] [Full Text] [PDF]
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W. Zheng, E. A. Seftor, C. J. Meininger, M. J. C. Hendrix, and R. J. Tomanek Mechanisms of coronary angiogenesis in response to stretch: role of VEGF and TGF-{beta} Am J Physiol Heart Circ Physiol, February 1, 2001; 280(2): H909 - H917. [Abstract] [Full Text] [PDF]
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C. Robinson and S. Stringer The splice variants of vascular endothelial growth factor (VEGF) and their receptors J. Cell Sci., January 3, 2001; 114(5): 853 - 865. [Abstract] [PDF]
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J. Grunstein, J. J. Masbad, R. Hickey, F. Giordano, and R. S. Johnson Isoforms of Vascular Endothelial Growth Factor Act in a Coordinate Fashion To Recruit and Expand Tumor Vasculature Mol. Cell. Biol., October 1, 2000; 20(19): 7282 - 7291. [Abstract] [Full Text]
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J. Sugawara, S. I. Tazuke, L. F-Suen, D. R. Powell, F. Kaper, A. J. Giaccia, and L. C. Giudice Regulation of Insulin-Like Growth Factor-Binding Protein 1 by Hypoxia and 3',5'-Cyclic Adenosine Monophosphate Is Additive in HepG2 Cells J. Clin. Endocrinol. Metab., October 1, 2000; 85(10): 3821 - 3827. [Abstract] [Full Text]
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S. Boussat, S. Eddahibi, A. Coste, V. Fataccioli, M. Gouge, B. Housset, S. Adnot, and B. Maitre Expression and regulation of vascular endothelial growth factor in human pulmonary epithelial cells Am J Physiol Lung Cell Mol Physiol, August 1, 2000; 279(2): L371 - L378. [Abstract] [Full Text] [PDF]
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P. Koehne, C. Willam, E. Strauss, R. Schindler, K.-U. Eckardt, and C. Buhrer Lack of hypoxic stimulation of VEGF secretion from neutrophils and platelets Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H817 - H824. [Abstract] [Full Text] [PDF]
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T. P. Gavin, D. A. Spector, H. Wagner, E. C. Breen, and P. D. Wagner Nitric oxide synthase inhibition attenuates the skeletal muscle VEGF mRNA response to exercise J Appl Physiol, April 1, 2000; 88(4): 1192 - 1198. [Abstract] [Full Text] [PDF]
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 G. McMahon VEGF Receptor Signaling in Tumor Angiogenesis Oncologist, April 1, 2000; 5(90001): 3 - 10. [Abstract] [Full Text]
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 Y. Hojo, U. Ikeda, Y. Zhu, M. Okada, S. Ueno, H. Arakawa, H. Fujikawa, T.-a. Katsuki, and K. Shimada Expression of vascular endothelial growth factor in patients with acute myocardial infarction J. Am. Coll. Cardiol., March 15, 2000; 35(4): 968 - 973. [Abstract] [Full Text] [PDF]
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H. J. H. Marti, M. Bernaudin, A. Bellail, H. Schoch, M. Euler, E. Petit, and W. Risau Hypoxia-Induced Vascular Endothelial Growth Factor Expression Precedes Neovascularization after Cerebral Ischemia Am. J. Pathol., March 1, 2000; 156(3): 965 - 976. [Abstract] [Full Text] [PDF]
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 F. Jung, L. A. Palmer, N. Zhou, and R. A. Johns Hypoxic Regulation of Inducible Nitric Oxide Synthase via Hypoxia Inducible Factor-1 in Cardiac Myocytes Circ. Res., February 18, 2000; 86(3): 319 - 325. [Abstract] [Full Text] [PDF]
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