BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Hypoxia-induced Angiogenesis during Carcinogenesis

  • Published : 2003.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

The formation of new blood vessels, angiogenesis, is an essential process during development and disease. Angiogenesis is well known as a crucial step in tumor growth and progression. Angiogenesis is induced by hypoxic conditions and regulated by the hypoxia-inducible factor 1 (HIF-1). The expression of HIF-1 correlates with hypoxia-induced angiogenesis as a result of the induction of the major HIF-1 target gene, vascular endothelial cell growth factor (VEGF). In this review, a brief overview of the mechanism of angiogenesis is discussed, focusing on the regulatory processes of the HIF-1 transcription factor. HIF-1 consists of a constitutively expressed HIF-1 beta(HIF-1β) subunit and an oxygen-regulated HIF-1 alpha(HIF-1α) subunit. The stability and activity of HIF-1α are regulated by the interaction with various proteins, such as pVHL, p53, and p300/CBP as well as by post-translational modifications, hydroxylation, acetylation, and phosphorylation. It was recently reported that HIF-1α binds a co-activator of the AP-1 transciption factor, Jab-1, which inhibits the p53-dependent degradation of HIF-1 and enhances the transcriptional activity of HIF-1 and the subsequent VEGF expression under hypoxic conditions. ARD1 acetylates HIF-1α and stimulates pVHL-mediated ubiquitination of HIF-1α. With a growing knowledge of the molecular mechanisms in this field, novel strategies to prevent tumor angiogenesis can be developed, and form these, new anticancer therapies may arise.

Keywords

References

  1. Ahmed, A., Dunk, C., Ahmad, S. and Khaliq, A. (2000) Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble FIt-1 by oxygen-a review. Placenta 21 Suppl. A, S16-S24. https://doi.org/10.1053/plac.1999.0524
  2. An, F. Q., Matsuda, M., Fujii, H. and Matsumoto, Y. (2000) Expression of vascular endothelial growth factor in surgical specimens of hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 126, 153-160. https://doi.org/10.1007/s004320050025
  3. An, W. G., Kanekal, M., Simon, M. C., Maltepe, E., Blagosklonny, M. V. and Neckers, L. M. (1998) Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 392, 405-408. https://doi.org/10.1038/32925
  4. Arany, Z., Huang, L. E., Eckner, R., Bhattacharya, S., Jiang, C., Goldberg, M. A, Bunn, H. F. and Livingston, D. M. (l996) An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. USA 93, 12969-12973. https://doi.org/10.1073/pnas.93.23.12969
  5. Bae, M. K, Ahn, M. Y., Jeong, J. W., Bae, M. H., Lee, Y. M., Bae, S. K., Park, J. W., Kim, K. R. and Kim, K. W. (2002) Jab1 interacts directly with HIF-lalpha and regulates its stability. J. Biol. Chem. 277, 9-12.
  6. Bae, S. K., Bae, M. H., Abn, M. Y., Son, M. J., Lee, Y. M., Bae, M. K., Lee, O. H., Park, B. C. and Kim, K. W. (1999) Egr-1 mediates transcriptional activation of IGF-II gene in response to hypoxia. Cancer Res. 59, 5989-5994.
  7. Bech-Otschir, D., Kraft, R, Huang, X., Henklein, P., Kapelari, B., PoHmann, C. and Dubiel, W. (2001) COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. EMBO J. 20, 1630-1639. https://doi.org/10.1093/emboj/20.7.1630
  8. Berra, E., Pages, G. and Pouyssegur, J. (2000) MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Rev. 19, 139-145. https://doi.org/10.1023/A:1026506011458
  9. Berra, E., Roux, D., Richard, D. E. and Pouyssegur, J. (2001) Hypoxia-inducible factor-1 alpha (HIF-1 alpha) escapes O(2)-driven proteasomal degradation irrespective of its subcellular localization: nucleus or cytoplasm. EMBO Rep. 2,615-620. https://doi.org/10.1093/embo-reports/kve130
  10. Bhattacharya, S., Michels, C. L., Leung, M. K, Arany, Z. P., Kung, A L. and Livingston, D. M. (1999) Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev. 13, 64-75. https://doi.org/10.1101/gad.13.1.64
  11. Boyes, J., Byfield, P., Nakatani, Y. and Ogryzko, V. (1998) Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 396, 594-598. https://doi.org/10.1038/25166
  12. Bruick, R. K. and McKnight, S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340. https://doi.org/10.1126/science.1066373
  13. Bunn, H. F. and Poyton, R. O. (1996) Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev. 76, 839-885. https://doi.org/10.1152/physrev.1996.76.3.839
  14. Buschmann, I. and Schaper, W. (2000) The pathophysiology of the collateral circulation (arteriogenesis). J. Pathol. 190, 338-342. https://doi.org/10.1002/(SICI)1096-9896(200002)190:3<338::AID-PATH594>3.0.CO;2-7
  15. Caniggia, I., Mostachfi, H., Winter, J., Gassmann, M., Lye, S. J., Kuliszewski, M. and Post, M. (2000) Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta (3). J. Clin. Invest. 105, 577-587. https://doi.org/10.1172/JCI8316
  16. Cao, Y., Linden, P., Shima, D., Browne, F. and Folkman, J. (1996) In vivo angiogenic activity and hypoxia induction of heterodimers of placenta growth factor/vascular endothelial growth factor. J. Clin. Invest. 98, 2507-2511. https://doi.org/10.1172/JCI119069
  17. Carmeliet, P., Dor, Y., Herbert, J. M., Fukumura, D., Brusselmans, K., Dewerchin, M., Neeman, M., Bono, F., Abramovitch, R., Maxwell, P., Koch, C. J., Ratcliffe, P., Moons, L., Jain, R. K, Collen, D., Keshert, E. and Keshet, E. (1998) Role of HlF- 1alpha in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 394, 485-490. https://doi.org/10.1038/28867
  18. Carmeliet, P. and Jain, R. K (2000) Angiogenesis in cancer and other diseases. Nature 407, 249-257. https://doi.org/10.1038/35025220
  19. Carrero, P., Okamoto, K., Coumailleau, P., O'Brien, S., Tanaka, H. and Poellinger, L. (2000) Redox-regulated recruitment of the transcriptional co-activators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1alpha. Mol. Cell Biol. 20, 402-415. https://doi.org/10.1128/MCB.20.1.402-415.2000
  20. Chauchereau, A, Georgiakaki, M., Perrin-Wolff, M., Milgrom, E. and Loosfelt, H. (2000) JAB1 interacts with both the progesterone receptor and SRC-1. J. Biol. Chem. 275, 8540- 8548. https://doi.org/10.1074/jbc.275.12.8540
  21. Cho, H., Kim, W. J., Lee, S. W., Kim, Y. M., Choi, E. Y., Park, S., Kwon, Y. G. and Kim, K. W. (2001) Anti-angiogenic activity of mouse N-/C-terminal deleted endostation. J. Biochem. Mol. Biol. 34, 206-21l.
  22. Cockman, M. E., Masson, N., Mole, D. R., Jaakkola, P., Chang, G. W., Clifford, S. C., Maher, E. R., Pugh, C. W., Ratcliffe, P. J. and Maxwell, P. H. (2000) Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J. Biol. Chem. 275, 25733-25741. https://doi.org/10.1074/jbc.M002740200
  23. Conway, E. M., Collen, D. and Carmeliet, P. (2001) Molecular mechanisms of blood vessel growth. Cardiovasc. Res. 49, 507- 521. https://doi.org/10.1016/S0008-6363(00)00281-9
  24. Cormier-Regard, S., Nguyen, S. V. and Claycomb, W. C. (1998) Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem 273, 17787-17792. https://doi.org/10.1074/jbc.273.28.17787
  25. Eckhart, A. D., Yang, N., Xin, X. and Faber, J. E. (1997) Characterization of the alpha1B-adrenergic receptor gene promoter region and hypoxia regulatory elements in vascular smooth muscle. Proc. Natl. Acad. Sci. USA 94, 9487-9492. https://doi.org/10.1073/pnas.94.17.9487
  26. Ema, M., Hirota, K., Mimura, J., Abe, H., Yodoi, J., Sogawa, K, Poellinger, L. and Fujii-Kuriyama, Y. (1999) Molecular mechanisms of transcription activation by HLF and HlF1alpha in response to hypoxia: their stabilization and redox signal- induced interaction with CBP/p300. EMBO J. 18, 1905-1914. https://doi.org/10.1093/emboj/18.7.1905
  27. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., MukheIji, M., Metzen, E., Wilson, M. I., Dhanda, A., Tian, Y. M., Masson, N., Hamilton, D. L., Jaakkola, P., Barstead, R., Hodgkin, J., Maxwell, P. H., Pugh, C. W., Schofield, C. J. and Ratcliffe, P. J. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by proly1 hydroxylation. Cell 107, 43-54. https://doi.org/10.1016/S0092-8674(01)00507-4
  28. Feldser, D., Agani, F., Iyer, N. V., Pak, B., Ferreira, G. and Semenza, G. L. (1999) Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res. 59, 3915-3918.
  29. Folkman, J., Merier, E., Abernathy, C. and Williams, G. (1971) Isolation of a tumor factor responsible or angiogenesis. J. Exp. Med. 133, 275-288. https://doi.org/10.1084/jem.133.2.275
  30. Gerber, H. P., Condorelli, F., Park, J. and Ferrara, N. (1997) Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. FIt-1, but not FIk-1/ KDR, is up-regulated by hypoxia. J. BioI. Chem. 272, 23659- 23667. https://doi.org/10.1074/jbc.272.38.23659
  31. Giordano, E. J. and Johnson, R. S. (2001) Angiogenesis: the role of the microenvironment in flipping the switch. Curr. Opin. Genet. Dev. 11, 35-40. https://doi.org/10.1016/S0959-437X(00)00153-2
  32. Gleadle, J. M., Ebert, B. L., Firth, J. D. and Ratcliffe, P. J. (1995) Regulation of angiogenic growth factor expression by hypoxia, transition metals, and chelating agents. Am. J. Physiol 268, C1362-C1368. https://doi.org/10.1152/ajpcell.1995.268.6.C1362
  33. Hanahan, D., Christofori, G., Naik, P. and Arbeit, J. (1996) Transgenic mouse models of tumor angiogenesis: the angiogenic switch, its molecular controls, and prospects for preclinical therapeutic models. Eur. J. Cancer 32A, 2386-2393.
  34. Harris, A. L. (2000) von Hippel-Lindau syndrome: target for anti-vascular endothelial growth factor (VEGF) receptor therapy. Oncologist 5 Suppl.1, 32-36. https://doi.org/10.1634/theoncologist.5-suppl_1-32
  35. Hewitson, K. S., McNeill, L. A, Riordan, M. V., Tian, Y. M., Bullock, A. N., Welford, R. W., Elkins, J. M., Oldham, N. J., Bhattacharya, S., Gleadle, J. M., Ratcliffe, P. J., Pugh, C. W. and Schofield, C. J. (2002) Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FlH) and is related to the cupin structural family. J. BioI. Chem. 277, 26351-26355. https://doi.org/10.1074/jbc.C200273200
  36. Hu, J., Discher, D. J., Bishopric, N. H. and Webster, K. A. (1998) Hypoxia regulates expression of the endothelin-1 gene through a proximal hypoxia-inducible factor-1 binding site on the antisense strand. Biochem. Biophys. Res. Commun. 245, 894- 899. https://doi.org/10.1006/bbrc.1998.8543
  37. Huang, L. E., Gu, J., Schau, M. and Bunn, H. F. (1998) Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin- proteasome pathway. Proc. Natl. Acad. Sci. USA 95, 7987-7992. https://doi.org/10.1073/pnas.95.14.7987
  38. Ingram, A. K, Cross, G. A. and Horn, D. (2000) Genetic manipulation indicates that ARD1 is an essential N(infinity)-acetyltransferase in Trypanosoma brucei. Mol. Biochem. Parasitol. 111, 309-317. https://doi.org/10.1016/S0166-6851(00)00322-4
  39. Ivan, M., Kondo, K, Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S. and Kaelin, W. G., Jr. (2001) HlFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for $O_{2}$ sensing. Science 292, 464-468. https://doi.org/10.1126/science.1059817
  40. Iyer, N. V., Kotch, L. E., Agani, F.E, Leung, S. W., Laughner, E., Wenger, R. H., Gassmann, M., Gearhart, J. D., Lawler, A. M., Yu, A. Y. and Semenza, G. L. (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 12, 149-162. https://doi.org/10.1101/gad.12.2.149
  41. Jaakkola, P., Mole, D. R., Tian, Y. M., Wilson, M. I., Gielbert, J., Gaskell, S. J., Kriegsheim, A., Hebestreit, H. F., MukheIji, M., Schofield, C. J., Maxwell, P. H., Pugh, C. W. and Ratcliffe, P. J. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by $O_{2}$-regulated prolyl hydroxylation. Science 292, 468-472. https://doi.org/10.1126/science.1059796
  42. Jeong, J. -W., Bae, M. -K, Ahn, M. -Y., Kim, S. -H., Shon, T. - K, Bae, M. -H., Yoo, H. -A, Song, E. J., Lee, K -J. and Kim, K. -W. (2002) Regulation and destabilization of HIF-1 alpha by ARD1-mediated acetylation. Cell 111, 709-720 .. https://doi.org/10.1016/S0092-8674(02)01085-1
  43. Jiang, B. H., Rue, E., Wang, G. L., Roe, R and Semenza, G. L. (1996) Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. BioI. Chem. 271, 17771-17778. https://doi.org/10.1074/jbc.271.30.17771
  44. Josko, J., Gwozdz, B., Jedrzejowska-Szypulka, H. and Hendryk, S. (2000) Vascular endothelial growth factor (VEGF) and its effect on angiogenesis. Med. Sci. Monit. 6, 1047-1052.
  45. Kallio, P. J., Wilson, W. J., O'Brien, S., Makino, Y. and Poellinger, L. (l999) Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J. BioI. Chem. 274,6519-6525. https://doi.org/10.1074/jbc.274.10.6519
  46. Kamura, T., Sato, S., Iwai, K, Czyzyk-Krzeska, M., Conaway, R.C. and Conaway, J.W. (2000) Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl. Acad. Sci. USA 97, 10430-10435. https://doi.org/10.1073/pnas.190332597
  47. Kietzmann, T., Roth, U. and Jungermann. K (1999) Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia- inducible factor-1 in rat hepatocytes. Blood 94.4177-4185.
  48. Kim, K. W.. Bae. S. K. Lee, O. H., Bae, M. H., Lee, M. J. and Park, B. C. (1998) Insulin-like growth factor II induced by hypoxia may contribute to angiogenesis of human hepatocellular carcinoma. Cancer Res. 58. 348-351.
  49. Kouzarides, T. (1999) Histone acetylases and deacetylases in cell proliferation. Curr. Opin. Genet. Dev. 9, 40-48. https://doi.org/10.1016/S0959-437X(99)80006-9
  50. Kouzarides, T. (2000) Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 19. 1176-1179. https://doi.org/10.1093/emboj/19.6.1176
  51. Lando, D., Peet. D. J.. Gorman. J. J., Whelan. D. A, Whitelaw, M. L. and Bmick, R. K. (2002a) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16. 1466-1471. https://doi.org/10.1101/gad.991402
  52. Lando. D., Peet, D. J., Whelan. D. A. Gorman. J. J. and Whitelaw, M. L. (2002b) Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295. 858-861. https://doi.org/10.1126/science.1068592
  53. Laughner, E., Taghavi, P., Chiles, K, Mahon, P. C. and Semenza, G. L. (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell BioI. 21, 3995-4004. https://doi.org/10.1128/MCB.21.12.3995-4004.2001
  54. LeCouter, J., Kowalski. J., Foster, J., Hass, P., Zhang, Z., Dillard-Telm, L.. Frantz, G., Rangell, L., DeGuzman, L., Keller, G. A., Peale, F., Gurney, A, Hillan, K. J. and Ferrara, N. (2001) Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 877-884. https://doi.org/10.1038/35091000
  55. Lee, P. J., Jiang, B. H., Chin, B. Y., lyer, N. V., Alam, J., Semenza. G. L. and Choi, A. M. (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272, 5375-5381. https://doi.org/10.1074/jbc.272.9.5375
  56. Lelievre, E., Lionneton, F., Soncin, F. and Vandenbunder, B. (2001) The Ets family contains transcriptional activators and repressors involved in angiogenesis. Int. J. Biochem. Cell Biol. 33. 391-407. https://doi.org/10.1016/S1357-2725(01)00025-5
  57. Lok, C. N. and Ponka, P. (1999) Identification of a hypoxia response element in the transferrin receptor gene. J. BioI. Chem. 274, 24147-24152. https://doi.org/10.1074/jbc.274.34.24147
  58. Mahon, P. C., Hirota, K. and Semenza. G. L. (2001) FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 5, 2675-2686. https://doi.org/10.1101/gad.924501
  59. Makino, Y., Cao, R., Svensson, K., Bertilsson, G., Asman, M., Tanaka, H., Cao. Y.. Berkenstam, A. and Poellinger, L. (2001) Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 414, 550-554. https://doi.org/10.1038/35107085
  60. Masson, N., Willam, C., Maxwell, P. H., Pugh, C. W. and Ratcliffe, P. J. (2001) Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 20, 5197-5206. https://doi.org/10.1093/emboj/20.18.5197
  61. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R. and Ratcliffe, P. J. (1999) The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen- dependent proteolysis. Nature 399. 271-275. https://doi.org/10.1038/20459
  62. Melillo, G., Musso, T., Sica, A., Taylor. L. S., Cox. G. W. and Varesio, L. (1995) A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182, 1683-1693. https://doi.org/10.1084/jem.182.6.1683
  63. Minet, E., Michel, G., Mottet, D., Raes, M. and Michiels, C. (2001) Transduction pathways involved in Hypoxia-Inducible Factor-1 phosphorylation and activation. Free Radic. Biol. Med. 31, 847-855. https://doi.org/10.1016/S0891-5849(01)00657-8
  64. Minet, E., Mottet, D., Michel, G., Roland, I., Raes, M., Remacle, J. and Michiels, C. (1999) Hypoxia-induced activation of HIF- I: role of HIF-1alpha-Hsp90 interaction. FEBS Lett. 460, 251-256. https://doi.org/10.1016/S0014-5793(99)01359-9
  65. Mukhopadhyay. C. K., Mazumder. B. and Fox, P. L. (2000) Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency. J. Biol. Chem 275, 21048- 21054. https://doi.org/10.1074/jbc.M000636200
  66. Neufeld, G., Cohen, T., Gengrinovitch, S. and Poltorak, Z. (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13,9-22. https://doi.org/10.1096/fasebj.13.1.9
  67. Ogryzko, V. V.. Kotani, T., Zhang. X., Schiltz. R. L., Howard, T., Yang, X. J., Howard, B. H., Qin, J. and Nakatani, Y. (1998) Histone-like TAFs within the PCAP histone acetylase complex. Cell 94, 35-44. https://doi.org/10.1016/S0092-8674(00)81219-2
  68. Ohh, M., Park, C. W., Ivan, M., Hoffman, M. A, Kim, T. Y., Huang. L. E., Pavletich, N., Chau, V. and Kaelin, W. G. (2000) Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nature Cell Biol. 2, 423-427. https://doi.org/10.1038/35017054
  69. Oikawa, M., Abe, M., Kurosawa, H., Hida, W., Shirato, K. and Sato, Y. (2001) Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem. Biophys. Res. Commun. 289, 39-43. https://doi.org/10.1006/bbrc.2001.5927
  70. Palmer, L. A. Semenza. G. L., Stoler, M. H. and Johns, R. A. (1998) Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIP-1. Am. J. Physiol 274. L212-L219.
  71. Park. J. H., Park, T., Kim, H. Y. and Yang. Y. M. (2001) The IGFBP-1 mRNA experession in HepG2 cells is affected by inhibition of heme biosynthesis. J. Biochem. Mol. Biol. 34, 385-389.
  72. Park, E. C. and Szostak, J. W. (1992) ARD1 and NAT1 proteins form a complex that has N-terminal acetyltransferase activity. EMBO J. 11, 2087-2093.
  73. Ravi, R., Mooketjee, B., Bhujwalla, Z. M., Sutter, C. H., Artemov, D., Zeng, Q., Dillehay, L. E., Madan, A, Semenza, G. L. and Bedi, A. (2000) Regulation of tumor angiogenesis by p53- induced degradation of hypoxia-inducible factor 1alpha. Genes Dev. 14, 34-44.
  74. Rolfs, A, Kvietikova, I., Gassmann, M. and Wenger, R. H. (1997) Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J. Biol. Chem. 272, 20055-20062. https://doi.org/10.1074/jbc.272.32.20055
  75. Rossetti, G., Collinge, M., Bender, J. R., Molteni, R. and Pardi, R. (2002) Iotegrin-dependent regulation of gene expression in leukocytes. Immunol. Rev. 186, 189-207. https://doi.org/10.1034/j.1600-065X.2002.18616.x
  76. Ruas, J. L., Poellinger, L. and Pereira, T. (2002) Functional Analysis of Hypoxia-inducible Factor-1alpha-mediated Transactivation. J. BioI. Chem. 277, 38723-38730. https://doi.org/10.1074/jbc.M205051200
  77. Ryan, H. E., Lo, J. and Johnson, R. S. (1998) HlF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 17, 3005-3015. https://doi.org/10.1093/emboj/17.11.3005
  78. Salceda, S., Beck, I., Srinivas, V. and Caro, J. (1997) Complex role of protein phosphorylation in gene activation by hypoxia. Kidney Int. 51, 556-559. https://doi.org/10.1038/ki.1997.78
  79. Salceda, S. and Caro, J. (1997) Hypoxia-inducible factor lalpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin- proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. BioI. Chem. 272, 22642-22647. https://doi.org/10.1074/jbc.272.36.22642
  80. Schaper, W. and Buschmann, I. (1999) VEGF and therapeutic opportunities in cardiovascular diseases. Curr. Opin. Biotechnol. 10, 541-543. https://doi.org/10.1016/S0958-1669(99)00032-4
  81. Scholz, D., Cai, W.J. and Schaper, W. (2001) Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Angiogenesis. 4, 247-257. https://doi.org/10.1023/A:1016094004084
  82. Seeger, M., Kraft, R., Ferrell, K., Bech-Otschir, D., Dumdey, R., Schade, R, Gordon, C., Naumann, M. and Dubiel, W. (1998) A novel protein complex involved in signal transduction possessing similarities to 26S proteasome subunits. FASEB J. 12, 469-478. https://doi.org/10.1096/fasebj.12.6.469
  83. Semenza, G. L. (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15, 551-578. https://doi.org/10.1146/annurev.cellbio.15.1.551
  84. Semenza, G. L. (2000) Oxygen-regulated transcription factors and their role in pulmonary disease. Respir. Res. 1, 159-162. https://doi.org/10.1186/rr27
  85. Semenza, G. L. (2002) HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol. Med. 8, S62-S67. https://doi.org/10.1016/S1471-4914(02)02317-1
  86. Sutter, C. H., Laughner, E. and Semenza, G. L. (2000) Hypoxia-inducible factor lalpha protein expression is controlled by oxygen-regulated ubiquitination that is disrupted by deletions and missense mutations. Proc. Natl. Acad. Sci. USA 97, 4748- 4753. https://doi.org/10.1073/pnas.080072497
  87. Tacchini, L., Bianchi, L., Bemelli-Zazzera, A. and Cairo, G. (1999) Transferrin receptor induction by hypoxia. HIF-1- mediated transcriptional activation and cell-specific post- transcriptional regulation. J. Bioi. Chem. 274, 24142-24146. https://doi.org/10.1074/jbc.274.34.24142
  88. Tacchini, L., Dansi, P., Matteucci, E. and Desiderio, M. A. (2001) Hepatocyte growth factor signaling stimulates hypoxia inducible factor-1 (HIF-1) activity in HepG2 hepatoma cells. Carcinogenesis 22, 1363-1371. https://doi.org/10.1093/carcin/22.9.1363
  89. Takahashi, Y., Takahashi, S., Shiga, Y., Yoshimi, T. and Miura, T. (2000) Hypoxic induction of prolyl 4-hydroxylase alpha (I) in cultured cells. J. BioI. Chem. 275, 14139-14146. https://doi.org/10.1074/jbc.275.19.14139
  90. Tanimoto, K, Makino, Y., Pereira, T. and Poellinger, L. (2000) Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19, 4298-4309. https://doi.org/10.1093/emboj/19.16.4298
  91. Tazuke, S. I., Mazure, N. M., Sugawara, J., Carland, G., Faessen, G. H., Suen, L. E, Irwin, J.C., Powell, D. R, Giaccia, A. J. and Giudice, L. C. (1998) Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc. Natl. Acad. Sci. USA 95, 10188-10193. https://doi.org/10.1073/pnas.95.17.10188
  92. Tomoda, K, Kubota, Y. and Kato, J. (1999) Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jabl. Nature 398, 160-165. https://doi.org/10.1038/18230
  93. Tribioli, C., Mancini, M., Plassart, E., Bione, S., Rivella, S., Sala, C., Torri, G. and Toniolo, D. (1994) Isolation of new genes in distal Xq28: transcriptional map and identification of a human homologue of the ARDI N-acetyl transferase of Saccharomyces cerevisiae. Human Mol. Genet. 3, 1061-1067. https://doi.org/10.1093/hmg/3.7.1061
  94. Tsukamoto, A., Kaneko, Y., Yoshida, T., Ichinose, M. and Kimura, S. (1999) Regulation of angiogenesis in human hepatomas: possible involvement of p53-inducible inhibitor of vascular endothelial cell proliferation. Cancer Lett. 141, 79-84. https://doi.org/10.1016/S0304-3835(99)00074-9
  95. Wang, G. L. and Semenza, G. L. (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. USA 90, 4304-4308. https://doi.org/10.1073/pnas.90.9.4304
  96. Wood, S. M., Wiesener, M. S., Yeates, K. M., Okada, N., Pugh, C. W, Maxwell, P. H. and Ratcliffe, P. J. (1998) Selection and analysis of a mutant cell line defective in the hypoxia-inducible factor-1 alpha-subunit (HlF-1alpha). Characterization of hif- 1alpha-dependent and -independent hypoxia-inducible gene expression. J. BioI. Chem. 273, 8360-8368. https://doi.org/10.1074/jbc.273.14.8360
  97. Wykoff, C. C., Pugh, C. W., Maxwell, P. H., Harris, A. L. and Ratcliffe, P. J. (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. https://doi.org/10.1038/sj.onc.1204012
  98. Xie, K. (2001) Interleukin-8 and human cancer biology. Cytokine Growth Factor Rev. 12, 375-391. https://doi.org/10.1016/S1359-6101(01)00016-8
  99. Zhong, H., Chiles, K., Feldser, D., Laughner, E., Hanrahan, C., Georgescu, M. M., Simons, J. W. and Semenza, G. L. (2000) Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/ PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 60, 1541-1545.

Cited by

  1. c-Jun kinase mediates expression of VEGF induced at transcriptional level by Rac1 and Cdc42Hs but not by RhoA vol.98, pp.3, 2006, https://doi.org/10.1002/jcb.20801
  2. HIF at the crossroads between ischemia and carcinogenesis vol.200, pp.1, 2004, https://doi.org/10.1002/jcp.10479
  3. Hypoxia inducible factor-1α contributes to UV radiation-induced inflammation, epidermal hyperplasia and immunosuppression in mice vol.11, pp.2, 2012, https://doi.org/10.1039/C1PP05265A
  4. Effect of alpha tocopherol acetate in Walker 256/B cells-induced oxidative damage in a rat model of breast cancer skeletal metastases vol.182, pp.2-3, 2009, https://doi.org/10.1016/j.cbi.2009.09.010
  5. Manganese superoxide dismutase suppresses hypoxic induction of hypoxia-inducible factor-1α and vascular endothelial growth factor 2005, https://doi.org/10.1038/sj.onc.1208986
  6. Inhibition of p53 during physiological angiogenesis in the hamster ovary does not affect extent of new vessel formation but delays vessel maturation vol.320, pp.3, 2005, https://doi.org/10.1007/s00441-005-1078-8
  7. Prospective validation of the prognostic value of elevated serum vascular endothelial growth factor in patients with nasopharyngeal carcinoma: More distant metastases and shorter overall survival after treatment vol.33, pp.6, 2011, https://doi.org/10.1002/hed.21541
  8. Progress and Prospects of Reactive Oxygen Species in Metal Carcinogenesis vol.2, pp.4, 2016, https://doi.org/10.1007/s40495-016-0061-2
  9. HIF-1 and p53: communication of transcription factors under hypoxia vol.8, pp.4, 2004, https://doi.org/10.1111/j.1582-4934.2004.tb00467.x
  10. Activation of the PI3K/AKT pathway mediates FSH-stimulated VEGF expression in ovarian serous cystadenocarcinoma vol.18, pp.7, 2008, https://doi.org/10.1038/cr.2008.70
  11. Ischemic Preconditioning: From Molecular Mechanisms to Therapeutic Opportunities vol.10, pp.2, 2008, https://doi.org/10.1089/ars.2007.1679
  12. Hypoxia enhances the stemness markers of cochlear stem/progenitor cells and expands sphere formation through activation of hypoxia-inducible factor-1alpha vol.275, pp.1-2, 2011, https://doi.org/10.1016/j.heares.2010.12.004
  13. Non-invasive measurement of the morphology and physiology of oral mucosa by use of optical spectroscopy vol.44, pp.1, 2008, https://doi.org/10.1016/j.oraloncology.2006.12.011
  14. Alterations of the Thioredoxin System by Hyperoxia vol.41, pp.5, 2009, https://doi.org/10.1165/rcmb.2008-0224OC
  15. Stimulation of HIF-1α, HIF-2α, and VEGF by prolyl 4-hydroxylase inhibition in human lung endothelial and epithelial cells vol.38, pp.8, 2005, https://doi.org/10.1016/j.freeradbiomed.2004.12.004
  16. Hypoxia enhances angiogenesis in an adipose-derived stromal cell/endothelial cell co-culture 3D gel model vol.49, pp.2, 2016, https://doi.org/10.1111/cpr.12244
  17. Ganglioside GM3 inhibits VEGF/VEGFR-2-mediated angiogenesis: Direct interaction of GM3 with VEGFR-2 vol.19, pp.3, 2009, https://doi.org/10.1093/glycob/cwn114
  18. Aberrant regulation of pVHL levels by microRNA promotes the HIF/VEGF axis in CLL B cells vol.113, pp.22, 2009, https://doi.org/10.1182/blood-2008-10-185686
  19. Identification of novel genes expressed in hypoxic brain condition by fluorescence differential display vol.169, pp.2-3, 2007, https://doi.org/10.1016/j.forsciint.2006.08.015
  20. Lower Osteopontin Plasma Levels Are Associated With Superior Outcomes in Advanced Non–Small-Cell Lung Cancer Patients Receiving Platinum-Based Chemotherapy: SWOG Study S0003 vol.26, pp.29, 2008, https://doi.org/10.1200/JCO.2008.17.0662
  21. An update on molecular biology of thyroid cancers vol.90, pp.3, 2014, https://doi.org/10.1016/j.critrevonc.2013.12.007
  22. Molecular pathogenesis and mechanisms of thyroid cancer vol.13, pp.3, 2013, https://doi.org/10.1038/nrc3431
  23. Restoring Transcription Factor HoxA5 Expression Inhibits the Growth of Experimental Hemangiomas in the Brain vol.68, pp.6, 2009, https://doi.org/10.1097/NEN.0b013e3181a491ce
  24. Autophagy and hypoxia in colonic adenomas related to aggressive features vol.15, pp.5, 2013, https://doi.org/10.1111/codi.12147
  25. Angiogenesis and hematological malignancies vol.10, pp.1, 2005, https://doi.org/10.1080/10245330400018409
  26. Modulation of vascular endothelial growth factor (VEGF) expression in motor neurons and its electrophysiological effects vol.76, pp.1-2, 2008, https://doi.org/10.1016/j.brainresbull.2007.11.018
  27. Epstein-Barr virus-encoded EBNA1 modulates the AP-1 transcription factor pathway in nasopharyngeal carcinoma cells and enhances angiogenesis in vitro vol.89, pp.11, 2008, https://doi.org/10.1099/vir.0.2008/003392-0
  28. An Oxygen Molecular Sensor, the HIF Prolyl 4-Hydroxylase, in the Marine Protist Perkinsus olseni vol.159, pp.3, 2008, https://doi.org/10.1016/j.protis.2008.03.002
  29. Therapeutic effect of a TM4SF5-specific peptide vaccine against colon cancer in a mouse model vol.47, pp.4, 2014, https://doi.org/10.5483/BMBRep.2014.47.4.157
  30. Constitutively active CCK2 receptor splice variant increases Src-dependent HIF-1α expression and tumor growth vol.26, pp.7, 2007, https://doi.org/10.1038/sj.onc.1209862
  31. Circulating CD105 shows significant impact in patients of oral cancer and promotes malignancy of cancer cells via CCL20 vol.37, pp.2, 2016, https://doi.org/10.1007/s13277-015-3991-0
  32. Unique expression and regulatory mechanisms of EG-VEGF/prokineticin-1 and its receptors in the corpus luteum vol.187, pp.5-6, 2005, https://doi.org/10.1016/j.aanat.2005.07.005
  33. Gene polymorphisms and prostate cancer: the evidence vol.104, pp.11, 2009, https://doi.org/10.1111/j.1464-410X.2009.08973.x
  34. Non-invasive measurement of the microvascular properties of non-dysplastic and dysplastic oral leukoplakias by use of optical spectroscopy vol.47, pp.12, 2011, https://doi.org/10.1016/j.oraloncology.2011.08.014
  35. Full range physiological mass transport control in 3D tissue cultures vol.13, pp.1, 2013, https://doi.org/10.1039/C2LC40787F
  36. Placenta: The Forgotten Organ vol.31, pp.1, 2015, https://doi.org/10.1146/annurev-cellbio-100814-125620
  37. Histological expression of angiogenic factors: VEGF, PDGFRα, and HIF-1α in Hodgkin lymphoma vol.205, pp.1, 2009, https://doi.org/10.1016/j.prp.2008.07.007
  38. Significance of MTA1 in the molecular characterization of osteosarcoma vol.33, pp.4, 2014, https://doi.org/10.1007/s10555-014-9523-3
  39. Molecular mechanisms of mTOR regulation by stress vol.2, pp.2, 2015, https://doi.org/10.4161/23723548.2014.970489
  40. DT-13, a saponin of dwarf lilyturf tuber, exhibits anti-cancer activity by down-regulating C-C chemokine receptor type 5 and vascular endothelial growth factor in MDA-MB-435 cells vol.12, pp.1, 2014, https://doi.org/10.1016/S1875-5364(14)60005-4
  41. The Thioredoxin System in Neonatal Lung Disease vol.21, pp.13, 2014, https://doi.org/10.1089/ars.2013.5782
  42. The invasive front in endometrial carcinoma: higher proliferation and associated derailment of cell cycle regulators vol.38, pp.8, 2007, https://doi.org/10.1016/j.humpath.2007.01.008
  43. Imaging vascular physiology to monitor cancer treatment vol.58, pp.2, 2006, https://doi.org/10.1016/j.critrevonc.2005.10.006
  44. Hypoxia-Inducible Factor-1 as a Therapeutic Target in Endometrial Cancer Management vol.2010, 2010, https://doi.org/10.1155/2010/580971
  45. Angiogenic factors are associated with multiple sclerosis vol.301, 2016, https://doi.org/10.1016/j.jneuroim.2016.11.005
  46. Expression of hypoxia inducible factor-1α and vascular endothelial growth factor-C in human chronic periodontitis vol.10, pp.3, 2015, https://doi.org/10.1016/j.jds.2014.09.004
  47. c-Src Regulates Constitutive and EGF-mediated VEGF Expression in Pancreatic Tumor Cells Through Activation of Phosphatidyl Inositol-3 Kinase and p38 MAPK vol.31, pp.3, 2005, https://doi.org/10.1097/01.mpa.0000178280.50534.0c
  48. Biliverdin’s regulation of reactive oxygen species signalling leads to potent inhibition of proliferative and angiogenic pathways in head and neck cancer vol.110, pp.8, 2014, https://doi.org/10.1038/bjc.2014.98
  49. Similar gene expression profiles of sporadic, PGL2-, and SDHD-linked paragangliomas suggest a common pathway to tumorigenesis vol.2, pp.1, 2009, https://doi.org/10.1186/1755-8794-2-25
  50. Angioprevention in Colon Cancer from Bench to Bedside vol.11, pp.6, 2015, https://doi.org/10.1007/s11888-015-0300-7
  51. Hypoxia downregulates Ku70/80 expression in cervical carcinoma tumors vol.89, pp.2, 2008, https://doi.org/10.1016/j.radonc.2008.07.018
  52. Immunohistochemical Study of the Angiogenetic Network of VEGF, HIF1α, VEGFR-2 and Endothelial Nitric Oxide Synthase (eNOS) in Human Breast Cancer vol.18, pp.1, 2012, https://doi.org/10.1007/s12253-011-9413-8
  53. AXIN2 polymorphism and its association with prostate cancer in a Turkish population vol.28, pp.4, 2011, https://doi.org/10.1007/s12032-010-9588-y
  54. Constitutive and inducible expression and regulation of vascular endothelial growth factor vol.15, pp.5, 2004, https://doi.org/10.1016/j.cytogfr.2004.04.003
  55. Hypoxia regulation of expression and angiogenic effects of vasoactive intestinal peptide (VIP) and VIP receptors in LNCaP prostate cancer cells vol.249, pp.1-2, 2006, https://doi.org/10.1016/j.mce.2006.02.004
  56. Mutant p53 facilitates pro-angiogenic, hyperproliferative phenotype in response to chronic relative hypoxia vol.249, pp.2, 2007, https://doi.org/10.1016/j.canlet.2006.08.017
  57. Inhibition of the VEGF expression and cell growth in hepatocellular carcinoma by blocking HIF-1α and Smad3 binding site in VEGF promoter vol.26, pp.1, 2006, https://doi.org/10.1007/BF02828043
  58. Gene-expression of metastasized versus non-metastasized primary head and neck squamous cell carcinomas: A pathway-based analysis vol.8, pp.1, 2008, https://doi.org/10.1186/1471-2407-8-168
  59. Enhanced expression of CD31/platelet endothelial cell adhesion molecule 1 (PECAM1) correlates with hypoxia inducible factor-1 alpha (HIF-1α) in human glioblastoma multiforme vol.339, pp.2, 2015, https://doi.org/10.1016/j.yexcr.2015.09.007
  60. Effect of age on vascularization during fracture repair vol.26, pp.10, 2008, https://doi.org/10.1002/jor.20667
  61. CAPE suppresses VEGFR-2 activation, and tumor neovascularization and growth vol.91, pp.2, 2013, https://doi.org/10.1007/s00109-012-0952-6
  62. Betulinic acid inhibits the expression of hypoxia-inducible factor 1α and vascular endothelial growth factor in human endometrial adenocarcinoma cells vol.340, pp.1-2, 2010, https://doi.org/10.1007/s11010-010-0395-8
  63. Phospholipase D activates HIF-1-VEGF pathway via phosphatidic acid vol.46, pp.12, 2014, https://doi.org/10.1038/emm.2014.86
  64. Pathogenic angiogenesis in IBD and experimental colitis: new ideas and therapeutic avenues vol.293, pp.1, 2007, https://doi.org/10.1152/ajpgi.00107.2007
  65. Minoxidil Induction of VEGF Is Mediated by Inhibition of HIF-Prolyl Hydroxylase vol.19, pp.1, 2017, https://doi.org/10.3390/ijms19010053
  66. A Meta-Analysis of Vascular Endothelial Growth Factor for Nasopharyngeal Cancer Prognosis vol.8, pp.2234-943X, 2018, https://doi.org/10.3389/fonc.2018.00486