Hypoxia-inducible factor in cancer angiogenesis: Structure, regulation and clinical perspectives

Critical Reviews in Oncology/Hematology - Tập 70 - Trang 93-102 - 2009
Zaher K. Otrock1, Hassan A. Hatoum2, Ahmad H. Awada3, Rim S. Ishak2, Ali I. Shamseddine4
1Department of Pathology and Laboratory Medicine, American University of Beirut Medical Center, Beirut, Lebanon
2Department of Internal Medicine, American University of Beirut Medical Center, Beirut, Lebanon
3Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium
4Department of Internal Medicine, American University of Beirut-Medical Center, Beirut, Lebanon

Tài liệu tham khảo

Folkman, 1990, What is the evidence that tumors are angiogenesis dependent?, J Natl Cancer Inst, 82, 4, 10.1093/jnci/82.1.4 Wang, 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, 10.1073/pnas.92.12.5510 Semenza, 1998, Hypoxia-inducible factor 1: master regulator of O2 homeostasis, Curr Opin Genet Dev, 8, 588, 10.1016/S0959-437X(98)80016-6 Bruick, 2001, A conserved family of prolyl-4-hydroxylases that modify HIF, Science, 294, 1337, 10.1126/science.1066373 Höpfl, 2004, HIFs and tumors—causes and consequences, Am J Physiol Regul Integr Comp Physiol, 286, R608, 10.1152/ajpregu.00538.2003 Goldberg, 1988, Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein, Science, 242, 1412, 10.1126/science.2849206 Semenza, 1991, Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene, Proc Natl Acad Sci USA, 88, 5680, 10.1073/pnas.88.13.5680 Wang, 1993, General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia, Proc Natl Acad Sci USA, 90, 4304, 10.1073/pnas.90.9.4304 Jiang, 1996, Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1, J Biol Chem, 271, 17771, 10.1074/jbc.271.30.17771 Michel, 2000, A model for the complex between the hypoxia-inducible factor-1 (HIF-1) and its consensus DNA sequence, J Biomol Struct Dyn, 18, 169, 10.1080/07391102.2000.10506656 Carrero, 2000, Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1alpha, Mol Cell Biol, 20, 402, 10.1128/MCB.20.1.402-415.2000 Richard, 1999, p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1, J Biol Chem, 274, 32631, 10.1074/jbc.274.46.32631 Hofer, 2001, Dissecting hypoxia-dependent and hypoxia-independent steps in the HIF-1alpha activation cascade: implications for HIF-1alpha gene therapy, FASEB J, 15, 2715, 10.1096/fj.01-0546fje Aragonés, 2001, Evidence for the involvement of diacylglycerol kinase in the activation of hypoxia-inducible transcription factor 1 by low oxygen tension, J Biol Chem, 276, 10548, 10.1074/jbc.M006180200 Huang, 1996, Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit, J Biol Chem, 271, 32253, 10.1074/jbc.271.50.32253 Jeong, 2002, Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation, Cell, 111, 709, 10.1016/S0092-8674(02)01085-1 Huang, 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, 10.1073/pnas.95.14.7987 Pugh, 1997, Activation of hypoxia-inducible factor-1; definition of regulatory domains within the alpha subunit, J Biol Chem, 272, 11205, 10.1074/jbc.272.17.11205 Semenza, 1999, Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1, Annu Rev Cell Dev Biol, 15, 551, 10.1146/annurev.cellbio.15.1.551 Ema, 1997, A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development, Proc Natl Acad Sci USA, 94, 4273, 10.1073/pnas.94.9.4273 Tian, 1997, Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells, Genes Dev, 11, 72, 10.1101/gad.11.1.72 Tian, 1998, The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development, Genes Dev, 12, 3320, 10.1101/gad.12.21.3320 Makino, 2002, Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus, J Biol Chem, 277, 32405, 10.1074/jbc.C200328200 Gu, 1998, Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3alpha, Gene Expr, 7, 205 Salceda, 1997, Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin–proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes, J Biol Chem, 272, 22642, 10.1074/jbc.272.36.22642 Kallio, 1997, Activation of hypoxia-inducible factor 1alpha: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor, Proc Natl Acad Sci USA, 94, 5667, 10.1073/pnas.94.11.5667 Lando, 2002, Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch, Science, 295, 858, 10.1126/science.1068592 Perkins, 1996, The role of MAP kinase in interleukin-3 stimulation of proliferation, Blood, 87, 3669, 10.1182/blood.V87.9.3669.bloodjournal8793669 Dameron, 1994, Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1, Science, 265, 1582, 10.1126/science.7521539 Bouvet, 1998, Adenovirus-mediated wild-type p53 gene transfer down-regulates vascular endothelial growth factor expression and inhibits angiogenesis in human colon cancer, Cancer Res, 58, 2288 Blancher, 2001, Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1alpha, HIF-2alpha, and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3′-kinase/Akt signaling pathway, Cancer Res, 61, 7349 Zundel, 2000, Loss of PTEN facilitates HIF-1-mediated gene expression, Genes Dev, 14, 391, 10.1101/gad.14.4.391 Jiang, 2001, Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1, Cell Growth Differ, 12, 363 Zhong, 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 Krishnamachary, 2003, Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1, Cancer Res, 63, 1138 Treins, 2002, Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway, J Biol Chem, 277, 27975, 10.1074/jbc.M204152200 Laughner, 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 Biol, 21, 3995, 10.1128/MCB.21.12.3995-4004.2001 Stiehl, 2002, Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway, FEBS Lett, 512, 157, 10.1016/S0014-5793(02)02247-0 Brahimi-Horn, 2005, Signalling via the hypoxia-inducible factor-1alpha requires multiple posttranslational modifications, Cell Signal, 17, 1, 10.1016/j.cellsig.2004.04.010 Srinivas, 1999, Characterization of an oxygen/redox-dependent degradation domain of hypoxia-inducible factor alpha (HIF-alpha) proteins, Biochem Biophys Res Commun, 260, 557, 10.1006/bbrc.1999.0878 Masson, 2001, Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation, EMBO J, 20, 5197, 10.1093/emboj/20.18.5197 Masson, 2003, HIF prolyl and asparaginyl hydroxylases in the biological response to intracellular O(2) levels, J Cell Sci, 116, 3041, 10.1242/jcs.00655 Epstein, 2001, C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation, Cell, 107, 43, 10.1016/S0092-8674(01)00507-4 Huang, 2002, Sequence determinants in hypoxia-inducible factor-1alpha for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3, J Biol Chem, 277, 39792, 10.1074/jbc.M206955200 Berra, 2003, HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia, EMBO J, 22, 4082, 10.1093/emboj/cdg392 Ivan, 2001, HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing, Science, 292, 464, 10.1126/science.1059817 Jaakkola, 2001, Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation, Science, 292, 468, 10.1126/science.1059796 Krek, 2000, VHL takes HIF's breath away, Nat Cell Biol, 2, E121, 10.1038/35017129 Jung, 2003, Microtubule disruption utilizes an NFkappa B-dependent pathway to stabilize HIF-1alpha protein, J Biol Chem, 278, 7445, 10.1074/jbc.M209804200 Cockman, 2000, Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein, J Biol Chem, 275, 25733, 10.1074/jbc.M002740200 Kamura, 2000, Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex, Proc Natl Acad Sci USA, 97, 10430, 10.1073/pnas.190332597 Krieg, 2000, Up-regulation of hypoxia-inducible factors HIF-1alpha and HIF-2alpha under normoxic conditions in renal carcinoma cells by von Hippel-Lindau tumor suppressor gene loss of function, Oncogene, 19, 5435, 10.1038/sj.onc.1203938 Ohh, 2000, Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein, Nat Cell Biol, 2, 423, 10.1038/35017054 Tanimoto, 2000, Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein, EMBO J, 19, 4298, 10.1093/emboj/19.16.4298 Kim, 2001, Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes, Nat Med, 7, 437, 10.1038/86507 Sang, 2002, Carboxyl-terminal transactivation activity of hypoxia-inducible factor 1 alpha is governed by a von Hippel-Lindau protein-independent, hydroxylation-regulated association with p300/CBP, Mol Cell Biol, 22, 2984, 10.1128/MCB.22.9.2984-2992.2002 Dames, 2002, Structural basis for Hif-1 alpha/CBP recognition in the cellular hypoxic response, Proc Natl Acad Sci USA, 99, 5271, 10.1073/pnas.082121399 Freedman, 2002, Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1 alpha, Proc Natl Acad Sci USA, 99, 5367, 10.1073/pnas.082117899 Hewitson, 2002, Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family, J Biol Chem, 277, 26351, 10.1074/jbc.C200273200 Mahon, 2001, FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity, Genes Dev, 15, 2675, 10.1101/gad.924501 Metzen, 2003, Intracellular localisation of human HIF-1 alpha hydroxylases: implications for oxygen sensing, J Cell Sci, 116, 1319, 10.1242/jcs.00318 Chan, 2002, Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1alpha, J Biol Chem, 277, 40112, 10.1074/jbc.M206922200 Isaacs, 2002, Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway, J Biol Chem, 277, 29936, 10.1074/jbc.M204733200 Katschinski, 2002, Heat induction of the unphosphorylated form of hypoxia-inducible factor-1alpha is dependent on heat shock protein-90 activity, J Biol Chem, 277, 9262, 10.1074/jbc.M110377200 Sodhi, 2000, The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1alpha, Cancer Res, 60, 4873 Minet, 2001, Transduction pathways involved in Hypoxia-Inducible Factor-1 phosphorylation and activation, Free Radic Biol Med, 31, 847, 10.1016/S0891-5849(01)00657-8 Hur, 2001, Mitogen-activated protein kinase inhibitor PD98059 blocks the trans-activation but not the stabilization or DNA binding ability of hypoxia-inducible factor-1alpha, Mol Pharmacol, 59, 1216, 10.1124/mol.59.5.1216 Suzuki, 2001, Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia, Oncogene, 20, 5779, 10.1038/sj.onc.1204742 Forsythe, 1996, Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1, Mol Cell Biol, 16, 4604, 10.1128/MCB.16.9.4604 Olsson, 2006, VEGF receptor signalling—in control of vascular function, Nat Rev Mol Cell Biol, 7, 359, 10.1038/nrm1911 Jensen, 2006, Inhibition of hypoxia inducible factor-1alpha (HIF-1alpha) decreases vascular endothelial growth factor (VEGF) secretion and tumor growth in malignant gliomas, J Neurooncol, 78, 233, 10.1007/s11060-005-9103-z Bos, 2001, Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis, J Natl Cancer Inst, 93, 309, 10.1093/jnci/93.4.309 Maxwell, 1997, Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth, Proc Natl Acad Sci USA, 94, 8104, 10.1073/pnas.94.15.8104 Tang, 2004, Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis, Cancer Cell, 6, 485, 10.1016/j.ccr.2004.09.026 Das, 2005, A hypoxia-driven vascular endothelial growth factor/Flt1 autocrine loop interacts with hypoxia-inducible factor-1alpha through mitogen-activated protein kinase/extracellular signal-regulated kinase 1/2 pathway in neuroblastoma, Cancer Res, 65, 7267, 10.1158/0008-5472.CAN-04-4575 Gerber, 1997, Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia, J Biol Chem, 272, 23659, 10.1074/jbc.272.38.23659 Ryan, 1998, HIF-1 alpha is required for solid tumor formation and embryonic vascularization, EMBO J, 17, 3005, 10.1093/emboj/17.11.3005 Burri, 2003, Significant correlation of hypoxia-inducible factor-1alpha with treatment outcome in cervical cancer treated with radical radiotherapy, Int J Radiat Oncol Biol Phys, 56, 494, 10.1016/S0360-3016(02)04579-0 Schindl, 2002, Overexpression of hypoxia-inducible factor 1alpha is associated with an unfavorable prognosis in lymph node-positive breast cancer, Clin Cancer Res, 8, 1831 Birner, 2001, Expression of hypoxia-inducible factor 1alpha in epithelial ovarian tumors: its impact on prognosis and on response to chemotherapy, Clin Cancer Res, 7, 1661 Sivridis, 2002, Association of hypoxia-inducible factors 1alpha and 2alpha with activated angiogenic pathways and prognosis in patients with endometrial carcinoma, Cancer, 95, 1055, 10.1002/cncr.10774 Takahashi, 2003, Hypoxia-inducible factor-1alpha expression and angiogenesis in gastrointestinal stromal tumor of the stomach, Oncol Rep, 10, 797 Koukourakis, 2001, Hypoxia inducible factor (HIF-1a and HIF-2a) expression in early esophageal cancer and response to photodynamic therapy and radiotherapy, Cancer Res, 61, 1830 Koukourakis, 2001, Hypoxia-regulated carbonic anhydrase-9 (CA9) relates to poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy, Clin Cancer Res, 7, 3399 Giatromanolaki, 2001, Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival, Br J Cancer, 85, 881, 10.1054/bjoc.2001.2018 Beasley, 2002, Hypoxia-inducible factors HIF-1alpha and HIF-2alpha in head and neck cancer: relationship to tumor biology and treatment outcome in surgically resected patients, Cancer Res, 62, 2493 Volm, 2000, Hypoxia-inducible factor (HIF-1) and its relationship to apoptosis and proliferation in lung cancer, Anticancer Res, 20, 1527 Melillo, 2004, HIF-1: a target for cancer, ischemia and inflammation—too good to be true?, Cell Cycle, 3, 154, 10.4161/cc.3.2.689 Yeo, 2004, New anticancer strategies targeting HIF-1, Biochem Pharmacol, 68, 1061, 10.1016/j.bcp.2004.02.040 Giaccia, 2003, HIF-1 as a target for drug development, Nat Rev Drug Discov, 2, 803, 10.1038/nrd1199 Semenza, 2003, Targeting HIF-1 for cancer therapy, Nat Rev Cancer, 3, 721, 10.1038/nrc1187 Brown, 1996, Hypoxia-specific cytotoxins in cancer therapy, Semin Radiat Oncol, 6, 22, 10.1016/S1053-4296(96)80033-6 Post, 2004, Cancer therapy with a replicating oncolytic adenovirus targeting the hypoxic microenvironment of tumors, Clin Cancer Res, 10, 8603, 10.1158/1078-0432.CCR-04-1432 Post, 2003, A novel hypoxia-inducible factor (HIF) activated oncolytic adenovirus for cancer therapy, Oncogene, 22, 2065, 10.1038/sj.onc.1206464 Birner, 2000, Lymphatic microvessel density in epithelial ovarian cancer: its impact on prognosis, Anticancer Res, 20, 2981 Bos, 2003, Levels of hypoxia-inducible factor-1alpha independently predict prognosis in patients with lymph node negative breast carcinoma, Cancer, 97, 1573, 10.1002/cncr.11246 Zagzag, 2000, Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression, Cancer, 88, 2606, 10.1002/1097-0142(20000601)88:11<2606::AID-CNCR25>3.3.CO;2-N Belozerov, 2005, Hypoxia inducible factor-1: a novel target for cancer therapy, Anticancer Drugs, 16, 901, 10.1097/01.cad.0000180116.85912.69 Welsh, 2004, Antitumor activity and pharmacodynamic properties of PX-478, an inhibitor of hypoxia-inducible factor-1alpha, Mol Cancer Ther, 3, 233, 10.1158/1535-7163.233.3.3 Koh, 2008, Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1alpha, Mol Cancer Ther, 7, 90, 10.1158/1535-7163.MCT-07-0463 Welsh, 2003, Hypoxia inducible factor as a cancer drug target, Curr Cancer Drug Targets, 3, 391, 10.2174/1568009033481732 Kaelin, 2002, Molecular basis of the VHL hereditary cancer syndrome, Nat Rev Cancer, 2, 673, 10.1038/nrc885 Ferrara, 2004, Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer, Nat Rev Drug Discov, 3, 391, 10.1038/nrd1381 Yang, 2003, A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer, N Engl J Med, 349, 427, 10.1056/NEJMoa021491 Motzer, 2007, Sunitinib versus interferon alfa in metastatic renal-cell carcinoma, N Engl J Med, 356, 115, 10.1056/NEJMoa065044 Hudson, 2002, Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin, Mol Cell Biol, 22, 7004, 10.1128/MCB.22.20.7004-7014.2002 Hudes, 2007, Global ARCC Trial. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma, N Engl J Med, 356, 2271, 10.1056/NEJMoa066838 Motzer, 2008, RAD001 vs. placebo in patients with metastatic renal cell carcinoma (RCC) after progression on VEGFr-TKI therapy: results from a randomized, double-blind, multicenter Phase-III study, J Clin Oncol, 26, 10.1200/jco.2008.26.15_suppl.lba5026 Papandreou, 2006, HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption, Cell Metab, 3, 187, 10.1016/j.cmet.2006.01.012 Brown, 2004, Exploiting tumour hypoxia in cancer treatment, Nat Rev Cancer, 4, 437, 10.1038/nrc1367 Cairns, 2007, Metabolic targeting of hypoxia and HIF1 in solid tumors can enhance cytotoxic chemotherapy, Proc Natl Acad Sci USA, 104, 9445, 10.1073/pnas.0611662104 Takabuchi, 2004, The inhibitory effect of sodium nitroprusside on HIF-1 activation is not dependent on nitric oxide-soluble guanylyl cyclase pathway, Biochem Biophys Res Commun, 324, 417, 10.1016/j.bbrc.2004.09.064 Melillo, 2006, Meeting report: exploiting the tumor microenvironment for therapeutics, Cancer Res, 66, 4558, 10.1158/0008-5472.CAN-06-0069 Rapisarda, 2004, Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications, Cancer Res, 64, 1475, 10.1158/0008-5472.CAN-03-3139 Beppu, 2005, Topotecan blocks hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression induced by insulin-like growth factor-I in neuroblastoma cells, Cancer Res, 65, 4775, 10.1158/0008-5472.CAN-04-3332