Hypoxia induces tumor and endothelial cell migration in a Semaphorin 3F- and VEGF-dependent manner via transcriptional repression of their common receptor Neuropilin 2

References

• Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003; 9:677 - 684
   PubMed Web of Science ®Google Scholar
• Hirota K, Semenza GL. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit Rev Oncol Hematol 2006; 59:15 - 26
   PubMed Web of Science ®Google Scholar
• Fong GH. Mechanisms of adaptive angiogenesis to tissue hypoxia. Angiogenesis 2008; 11:121 - 140
   PubMed Web of Science ®Google Scholar
• Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16:4604 - 4613
   PubMed Web of Science ®Google Scholar
• Ryan HE, Lo J, Johnson RS. HIF-1alpha is required for solid tumor formation and embryonic vascularization. EMBO J 1998; 17:3005 - 3015
   PubMed Web of Science ®Google Scholar
• Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995; 270:1230 - 1237
   PubMed Web of Science ®Google Scholar
• Jiang BH, Semenza GL, Bauer C, Marti HH. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol 1996; 271:1172 - 1180
   PubMed Web of Science ®Google Scholar
• Klagsbrun M, Eichmann A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 2005; 16:535 - 548
   PubMed Web of Science ®Google Scholar
• Ellis LM. The role of neuropilins in cancer. Mol Cancer Ther 2006; 5:1099 - 1107
   PubMed Web of Science ®Google Scholar
• Guttmann-Raviv N, Kessler O, Shraga-Heled N, Lange T, Herzog Y, Neufeld G. The neuropilins and their role in tumorigenesis and tumor progression. Cancer Lett 2006; 231:1 - 11
   PubMed Web of Science ®Google Scholar
• Gaur P, Bielenberg DR, Samuel S, Bose D, Zhou Y, Gray MJ, et al. Role of class 3 semaphorins and their receptors in tumor growth and angiogenesis. Clin Cancer Res 2009; 15:6763 - 6770
   PubMed Web of Science ®Google Scholar
• Kessler O, Shraga-Heled N, Lange T, Gutmann-Raviv N, Sabo E, Baruch L, et al. Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res 2004; 64:1008 - 1015
   PubMed Web of Science ®Google Scholar
• Bielenberg DR, Hida Y, Shimizu A, Kaipainen A, Kreuter M, Kim CC, et al. Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype. J Clin Invest 2004; 114:1260 - 1271
   PubMed Web of Science ®Google Scholar
• Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998; 92:735 - 745
   PubMed Web of Science ®Google Scholar
• Geretti E, Shimizu A, Klagsbrun M. Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis. Angiogenesis 2008; 11:31 - 39
   PubMed Web of Science ®Google Scholar
• Kawamura H, Li X, Goishi K, van Meeteren LA, Jakobsson L, Cebe-Suarez S. Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood 2008; 112:3638 - 3649
   PubMed Web of Science ®Google Scholar
• Favier B, Alam A, Barron P, Bonnin J, Laboudie P, Fons P, et al. Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood 2006; 108:1243 - 1250
   PubMed Web of Science ®Google Scholar
• Klagsbrun M, Takashima S, Mamluk R. The role of neuropilin in vascular and tumor biology. Adv Exp Med Biol 2002; 515:33 - 48
   PubMed Web of Science ®Google Scholar
• Bielenberg DR, Pettaway CA, Takashima S, Klagsbrun M. Neuropilins in neoplasms: expression, regulation and function. Exp Cell Res 2006; 312:584 - 593
   PubMed Web of Science ®Google Scholar
• Miao HQ, Lee P, Lin H, Soker S, Klagsbrun M. Neuropilin-1 expression by tumor cells promotes tumor angiogenesis and progression. FASEB J 2000; 14:2532 - 2539
   PubMed Web of Science ®Google Scholar
• Parikh AA, Fan F, Liu WB, Ahmad SA, Stoeltzing O, Reinmuth N, et al. Neuropilin-1 in human colon cancer: expression, regulation and role in induction of angiogenesis. Am J Pathol 2004; 164:2139 - 2151
   PubMed Web of Science ®Google Scholar
• Hu B, Guo P, Bar-Joseph I, Imanishi Y, Jarzynka MJ, Bogler O, et al. Neuropilin-1 promotes human glioma progression through potentiating the activity of the HGF/SF autocrine pathway. Oncogene 2007; 26:5577 - 5586
   PubMed Web of Science ®Google Scholar
• Dallas NA, Gray MJ, Xia L, Fan F, van Buren G 2nd, Gaur P, et al. Neuropilin-2-mediated tumor growth and angiogenesis in pancreatic adenocarcinoma. Clin Cancer Res 2008; 14:8052 - 8060
   PubMed Web of Science ®Google Scholar
• Gray MJ, Van Buren G, Dallas NA, Xia L, Wang X, Yang AD, et al. Therapeutic targeting of neuropilin-2 on colorectal carcinoma cells implanted in the murine liver. J Natl Cancer Inst 2008; 100:109 - 120
   PubMedGoogle Scholar
• Handa A, Tokunaga T, Tsuchida T, Lee YH, Kijima H, Yamazaki H, et al. Neuropilin-2 expression affects the increased vascularization and is a prognostic factor in osteosarcoma. Int J Oncol 2000; 17:291 - 295
   PubMed Web of Science ®Google Scholar
• Hansel DE, Wilentz RE, Yeo CJ, Schulick RD, Montgomery E, Maitra A. Expression of neuropilin-1 in high-grade dysplasia, invasive cancer and metastases of the human gastrointestinal tract. Am J Surg Pathol 2004; 28:347 - 356
   PubMed Web of Science ®Google Scholar
• Kawakami T, Tokunaga T, Hatanaka H, Kijima H, Yamazaki H, Abe Y, et al. Neuropilin 1 and neuropilin 2 co-expression is significantly correlated with increased vascularity and poor prognosis in nonsmall cell lung carcinoma. Cancer 2002; 95:2196 - 2201
   PubMed Web of Science ®Google Scholar
• Kreuter M, Woelke K, Bieker R, Schliemann C, Steins M, Buechner T, et al. Correlation of neuropilin-1 overexpression to survival in acute myeloid leukemia. Leukemia 2006; 20:1950 - 1954
   PubMed Web of Science ®Google Scholar
• Lantuejoul S, Constantin B, Drabkin H, Brambilla C, Roche J, Brambilla E. Expression of VEGF, semaphorin SEMA3F, and their common receptors neuropilins NP1 and NP2 in preinvasive bronchial lesions, lung tumours and cell lines. J Pathol 2003; 200:336 - 347
   PubMed Web of Science ®Google Scholar
• Latil A, Bieche I, Pesche S, Valeri A, Fournier G, Cussenot O, et al. VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms. Int J Cancer 2000; 89:167 - 171
   PubMed Web of Science ®Google Scholar
• Bachelder RE, Crago A, Chung J, Wendt MA, Shaw LM, Robinson G, et al. Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells. Cancer Res 2001; 61:5736 - 5740
   PubMed Web of Science ®Google Scholar
• Roche J, Boldog F, Robinson M, Robinson L, Varella-Garcia M, Swanton M, et al. Distinct 3p21.3 deletions in lung cancer and identification of a new human semaphorin. Oncogene 1996; 12:1289 - 1297
   PubMed Web of Science ®Google Scholar
• Sekido Y, Bader S, Latif F, Chen JY, Duh FM, Wei MH, et al. Human semaphorins A(V) and IV reside in the 3p21.3 small cell lung cancer deletion region and demonstrate distinct expression patterns. Proc Natl Acad Sci USA 1996; 93:4120 - 4125
   PubMed Web of Science ®Google Scholar
• Shimizu A, Mammoto A, Italiano JE Jr, Pravda E, Dudley AC, Ingber DE, et al. ABL2/ARG tyrosine kinase mediates SEMA3F-induced RhoA inactivation and cytoskeleton collapse in human glioma cells. J Biol Chem 2008; 283:27230 - 27238
   PubMed Web of Science ®Google Scholar
• Coma S, Amin DN, Shimizu A, Lasorella A, Iavarone A, Klagsbrun M. Id2 promotes tumor cell migration and invasion through transcriptional repression of semaphorin 3F. Cancer Res 2010; 70:3823 - 3832
   PubMed Web of Science ®Google Scholar
• Wang GL, Semenza GL. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 1993; 82:3610 - 3615
   PubMed Web of Science ®Google Scholar
• Veschini L, Belloni D, Foglieni C, Cangi MG, Ferrarini M, Caligaris-Cappio F, et al. Hypoxia-inducible transcription factor-1alpha determines sensitivity of endothelial cells to the proteosome inhibitor bortezomib. Blood 2007; 109:2565 - 2570
   PubMed Web of Science ®Google Scholar
• Salnikow K, Donald SP, Bruick RK, Zhitkovich A, Phang JM, Kasprzak KS. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem 2004; 279:40337 - 40344
   PubMed Web of Science ®Google Scholar
• Hagen T, Taylor CT, Lam F, Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 2003; 302:1975 - 1978
   PubMed Web of Science ®Google Scholar
• Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol Cell Biol 1998; 18:3112 - 3119
   PubMed Web of Science ®Google Scholar
• Ozawa K, Kondo T, Hori O, Kitao Y, Stern DM, Eisenmenger W, et al. Expression of the oxygen-regulated protein ORP150 accelerates wound healing by modulating intracellular VEGF transport. J Clin Invest 2001; 108:41 - 50
   PubMed Web of Science ®Google Scholar
• Osada R, Horiuchi A, Kikuchi N, Ohira S, Ota M, Katsuyama Y, et al. Expression of semaphorins, vascular endothelial growth factor, and their common receptor neuropilins and alleic loss of semaphorin locus in epithelial ovarian neoplasms: increased ratio of vascular endothelial growth factor to semaphorin is a poor prognostic factor in ovarian carcinomas. Hum Pathol 2006; 37:1414 - 1425
   PubMed Web of Science ®Google Scholar
• Bae D, Lu S, Taglienti CA, Mercurio AM. Metabolic stress induces the lysosomal degradation of neuropilin-1 but not neuropilin-2. J Biol Chem 2008; 283:28074 - 28080
   Google Scholar
• Ding H, Wu X, Roncari L, Lau N, Shannon P, Nagy A, et al. Expression and regulation of neuropilin-1 in human astrocytomas. Int J Cancer 2000; 88:584 - 592
   PubMed Web of Science ®Google Scholar
• Rossignol M, Gagnon ML, Klagsbrun M. Genomic organization of human neuropilin-1 and neuropilin-2 genes: identification and distribution of splice variants and soluble isoforms. Genomics 2000; 70:211 - 222
   PubMed Web of Science ®Google Scholar
• Geretti E, van Meeteren LA, Shimizu A, Dudley AC, Claesson-Welsh L, Klagsbrun M. A mutated soluble neuropilin-2 B domain antagonizes vascular endothelial growth factor bioactivity and inhibits tumor progression.. Mol Cancer Res 2010; 8:1063 - 1073
   PubMed Web of Science ®Google Scholar