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Commentary

VEGF-A121a binding to Neuropilins – A concept revisited

ORCID Icon & ORCID Icon
Pages 204-214 | Received 02 May 2017, Accepted 24 Aug 2017, Published online: 02 Nov 2017

References

  • Kut C, Mac Gabhann F, Popel AS. Where is VEGF in the body? A meta-analysis of VEGF distribution in cancer. Br J Cancer. 2007;97:978-85. doi:10.1038/sj.bjc.6603923. PMID:17912242.
  • Guo HF, Vander Kooi CW. Neuropilin Functions as an Essential Cell Surface Receptor. J Biol Chem. 2015;290:29120-6. doi:10.1074/jbc.R115.687327. PMID:26451046.
  • Vempati P, Popel AS, Mac Gabhann F. Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning. Cytokine Growth Factor Rev. 2014;25:1-19. doi:10.1016/j.cytogfr.2013.11.002. PMID:24332926.
  • Grunewald FS, Prota AE, Giese A, Ballmer-Hofer K. Structure-function analysis of VEGF receptor activation and the role of coreceptors in angiogenic signaling. Biochimica Et Biophysica Acta-Proteins and Proteomics. 2010;1804:567-80. doi:10.1016/j.bbapap.2009.09.002.
  • Gengrinovitch S, Berman B, David G, Witte L, Neufeld G, Ron D. Glypican-1 is a VEGF(165) binding proteoglycan that acts as an extracellular chaperone for VEGF(165). J Biol Chem. 1999;274:10816-22. doi:10.1074/jbc.274.16.10816. PMID:10196157.
  • Teran M, Nugent MA. Synergistic Binding of Vascular Endothelial Growth Factor-A and Its Receptors to Heparin Selectively Modulates Complex Affinity. J Biol Chem. 2015;290:16451-62. doi:10.1074/jbc.M114.627372. PMID:25979342.
  • Jakobsson L, Kreuger J, Holmborn K, Lundin L, Eriksson I, Kjellen L, Claesson-Welsh L. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev Cell. 2006;10:625-34. doi:10.1016/j.devcel.2006.03.009. PMID:16678777.
  • Nowak DG, Woolard J, Amin EM, Konopatskaya O, Saleem MA, Churchill AJ, Ladomery MR, Harper SJ, Bates DO. Expression of pro- and anti-angiogenic isoforms of VEGF is differentially regulated by splicing and growth factors. J Cell Sci. 2008;121:3487-95. doi:10.1242/jcs.016410. PMID:18843117.
  • Delcombel R, Janssen L, Vassy R, Gammons M, Haddad O, Richard B, Letourneur D, Bates D, Hendricks C, Waltenberger J, et al. New prospects in the roles of the C-terminal domains of VEGF-A and their cooperation for ligand binding, cellular signaling and vessels formation. Angiogenesis. 2013;16:353-71. doi:10.1007/s10456-012-9320-y. PMID:23254820.
  • Kawamura H, Li X, Harper SJ, Bates DO, Claesson-Welsh L. Vascular endothelial growth factor (VEGF)-A165b is a weak in vitro agonist for VEGF receptor-2 due to lack of coreceptor binding and deficient regulation of kinase activity. Cancer Res. 2008;68:4683-92. doi:10.1158/0008-5472.CAN-07-6577. PMID:18559514.
  • Soker S, Fidder H, Neufeld G, Klagsbrun M. Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF(165) via its exon 7-encoded domain. J Biol Chem. 1996;271:5761-7. doi:10.1074/jbc.271.10.5761. PMID:8621443.
  • 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;92:735-45. doi:10.1016/S0092-8674(00)81402-6. PMID:9529250.
  • GitayGoren H, Cohen T, Tessler S, Soker S, Gengrinovitch S, Rockwell P, Klagsbrun M, Levi BZ, Neufeld G. Selective binding of VEGF(121) to one of the three vascular endothelial growth factor receptors of vascular endothelial cells. J Biol Chem. 1996;271:5519-23. doi:10.1074/jbc.271.10.5519. PMID:8621410.
  • Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G. Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165 [corrected]. J Biol Chem. 2000;275:18040-5. doi:10.1074/jbc.M909259199. PMID:10748121.
  • Shraga-Heled N, Kessler O, Prahst C, Kroll J, Augustin H, Neufeld G. Neuropilin-1 and neuropilin-2 enhance VEGF121 stimulated signal transduction by the VEGFR-2 receptor. FASEB J. 2007;21:915-26. doi:10.1096/fj.06-6277com. PMID:17185751.
  • Peters K, Richards FM. Chemical cross-linking: reagents and problems in studies of membrane structure. Annu Rev Biochem 1977;46:523-51. doi:10.1146/annurev.bi.46.070177.002515. PMID:409338.
  • Vander Kooi CW, Jusino MA, Perman B, Neau DB, Bellamy HD, Leahy DJ. Structural basis for ligand and heparin binding to neuropilin B domains. Proc Natl Acad Sci U S A. 2007;104:6152-7. doi:10.1073/pnas.0700043104. PMID:17405859.
  • Parker MW, Xu P, Li X, Vander Kooi CW. Structural basis for selective vascular endothelial growth factor-A (VEGF-A) binding to neuropilin-1. J Biol Chem. 2012;287:11082-9. doi:10.1074/jbc.M111.331140. PMID:22318724.
  • Teesalu T, Sugahara KN, Kotamraju VR, Ruoslahti E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci U S A. 2009;106:16157-62. doi:10.1073/pnas.0908201106. PMID:19805273.
  • Starzec A, Ladam P, Vassy R, Badache S, Bouchemal N, Navaza A, du Penhoat CH, Perret GY. Structure-function analysis of the antiangiogenic ATWLPPR peptide inhibiting VEGF(165) binding to neuropilin-1 and molecular dynamics simulations of the ATWLPPR/neuropilin-1 complex. Peptides. 2007;28:2397-402. doi:10.1016/j.peptides.2007.09.013. PMID:17983687.
  • Parker MW, Linkugel AD, Goel HL, Wu T, Mercurio AM, Vander Kooi CW. Structural basis for VEGF-C binding to neuropilin-2 and sequestration by a soluble splice form. Structure. 2015;23:677-87. doi:10.1016/j.str.2015.01.018. PMID:25752543.
  • Fairbrother WJ, Champe MA, Christinger HW, Keyt BA, Starovasnik MA. Solution structure of the heparin-binding domain of vascular endothelial growth factor. Structure with Folding & Design 1998;6:637-48. doi:10.1016/S0969-2126(98)00065-3..
  • Suarez SC, Pieren M, Cariolato L, Arn S, Hoffmann U, Bogucki A, Manlius C, Wood J, Ballmer-Hofer K. A VEGF-A splice variant defective for heparan sulfate and neuropilin-1 binding shows attenuated signaling through VEGFR-2. Cell Mol Life Sci. 2006;63:2067-77. doi:10.1007/s00018-006-6254-9. PMID:16909199.
  • von Wronski MA Raju N, Pillai R, Bogdan NJ, Marinelli ER, Nanjappan P, Ramalingam K, Arunachalam T, Eaton S, Linder KE, et al. Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J Biol Chem. 2006;281:5702-10. doi:10.1074/jbc.M511941200. PMID:16371354.
  • Jia H, Bagherzadeh A, Hartzoulakis B, Jarvis A, Lohr M, Shaikh S, Aqil R, Cheng L, Tickner M, Esposito D, et al. Characterization of a bicyclic peptide neuropilin-1 (NP-1) antagonist (EG3287) reveals importance of vascular endothelial growth factor exon 8 for NP-1 binding and role of NP-1 in KDR signaling. J Biol Chem. 2006;281:13493-502. doi:10.1074/jbc.M512121200. PMID:16513643.
  • Mineur P, Colige AC, Deroanne CF, Dubail J, Kesteloot F, Habraken Y, Noel A, Voo S, Waltenberger J, Lapiere CM, et al. Newly identified biologically active and proteolysis-resistant VEGF-A isoform VEGF111 is induced by genotoxic agents. J Cell Biol. 2007;179:1261-73. doi:10.1083/jcb.200703052. PMID:18086921.
  • Pan Q, Chathery Y, Wu Y, Rathore N, Tong RK, Peale F, Bagri A, Tessier-Lavigne M, Koch AW, Watts RJ. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J Biol Chem. 2007;282:24049-56. doi:10.1074/jbc.M703554200. PMID:17575273.
  • Barton R, Driscoll A, Flores S, Mudbhari D, Collins T, Iovine MK, Berger BW. Cysteines in the Neuropilin-2 MAM Domain Modulate Receptor Homooligomerization and Signal Transduction. Biopolymers. 2015;104:371-8. doi:10.1002/bip.22619. PMID:25656526.
  • Roth L, Nasarre C, Dirrig-Grosch S, Aunis D, Cremel G, Hubert P, Bagnard D. Transmembrane domain interactions control biological functions of neuropilin-1. Mol Biol Cell. 2008;19:646-54. doi:10.1091/mbc.E07-06-0625. PMID:18045991.
  • Shintani Y, Takashima S, Asano Y, Kato H, Liao YL, Yamazaki S, Tsukamoto O, Seguchi O, Yamamoto H, Fukushima T, et al. Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling. Embo J. 2006;25:3045-55. doi:10.1038/sj.emboj.7601188. PMID:16763549.
  • Vintonenko N, Pelaez-Garavito I, Buteau-Lozano H, Toullec A, Lidereau R, Perret GY, Bieche I, Perrot-Applanat M. Overexpression of VEGF189 in breast cancer cells induces apoptosis via NRP1 under stress conditions. Cell Adh Migr. 2011;5:332-43. doi:10.4161/cam.5.4.17287. PMID:21897119.
  • Kawamura H, Li XJ, Goishi K, van Meeteren LA, Jakobsson L, Cebe-Suarez S, Shimizu A, Edholm D, Ballmer-Hofer K, Kjellen L, et al. Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood. 2008;112:3638-49. doi:10.1182/blood-2007-12-125856. PMID:18664627.
  • Parker MW, Xu P, Guo HF, Vander Kooi CW. Mechanism of selective VEGF-A binding by neuropilin-1 reveals a basis for specific ligand inhibition. PLoS One. 2012;7:e49177. doi:10.1371/journal.pone.0049177. PMID:23145112.
  • Korff T, Augustin HG. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci. 1999;112:3249-58. PMID:10504330.
  • Korff T, Kimmina S, Martiny-Baron G, Augustin HG. Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. Faseb J. 2001;15:447-57. doi:10.1096/fj.00-0139com. PMID:11156960.
  • Bishop JR, Schuksz M, Esko JD. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature. 2007;446:1030-7. doi:10.1038/nature05817. PMID:17460664.
  • El-Sheikh A, Liu C, Huang HN, Edgington TS. A novel vascular endothelial growth factor heparin-binding domain substructure binds to glycosaminoglycans in vivo and localizes to tumor microvascular endothelium. Cancer Res. 2002;62:7118-23. PMID:12460934.
  • Thacker BE, Seamen E, Lawrence R, Parker MW, Xu Y, Liu J, Vander Kooi CW, Esko JD. Expanding the 3-O-Sulfate Proteome–Enhanced Binding of Neuropilin-1 to 3-O-Sulfated Heparan Sulfate Modulates Its Activity. ACS Chem Biol. 2016;11:971-80. doi:10.1021/acschembio.5b00897. PMID:26731579.
  • Xu D, Fuster MM, Lawrence R, Esko JD. Heparan sulfate regulates VEGF165- and VEGF121-mediated vascular hyperpermeability. J Biol Chem. 2011;286:737-45. doi:10.1074/jbc.M110.177006. PMID:20974861.
  • Chiang MK, Flanagan JG. INTERACTIONS BETWEEN THE FLK-1 RECEPTOR, VASCULAR ENDOTHELIAL GROWTH-FACTOR, AND CELL-SURFACE PROTEOGLYCAN IDENTIFIED WITH A SOLUBLE RECEPTOR REAGENT. Growth Factors 1995;12:1-10. doi:10.3109/08977199509003208. PMID:8527158.
  • Dougher AM, Wasserstrom H, Torley L, Shridaran L, Westdock P, Hileman RE, Fromm JR, Anderberg R, Lyman S, Linhardt RJ, et al. Identification of a heparin binding peptide on the extracellular domain of the KDR VEGF receptor. Growth Factors 1997;14:257-68. doi:10.3109/08977199709021524. PMID:9386990.
  • Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 1993;90:10705-9. doi:10.1073/pnas.90.22.10705. PMID:8248162.
  • Cohen T, Gitaygoren H, Sharon R, Shibuya M, Halaban R, Levi BZ, Neufeld G. Vegf(121), a Vascular Endothelial Growth-Factor (Vegf) Isoform Lacking Heparin-Binding Ability, Requires Cell-Surface Heparan Sulfates for Efficient Binding to the Vegf Receptors of Human-Melanoma Cells. J Biol Chem. 1995;270:11322-6. doi:10.1074/jbc.270.19.11322. PMID:7744769.
  • Park M, Lee ST. The fourth immunoglobulin-like loop in the extracellular domain of FLT-1, a VEGF receptor, includes a major heparin-binding site. Biochem Biophys Res Commun. 1999;264:730-4. doi:10.1006/bbrc.1999.1580. PMID:10544000.
  • Mamluk R, Gechtman Z, Kutcher ME, Gasiunas N, Gallagher J, Klagsbrun M. Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J Biol Chem. 2002;277:24818-25. doi:10.1074/jbc.M200730200. PMID:11986311.
  • Tessler S, Rockwell P, Hicklin D, Cohen T, Levi BZ, Witte L, Lemischka IR, Neufeld G. Heparin Modulates the Interaction of Vegf(165) with Soluble and Cell-Associated Flk-1 Receptors. J Biol Chem. 1994;269:12456-61. PMID:8175651.
  • Fuh G, Garcia KC, de Vos AM. The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor flt-1. J Biol Chem. 2000;275:26690-5. PMID:10842181.
  • Gelfand MV, Hagan N, Tata A, Oh WJ, Lacoste B, Kang KT, Kopycinska J, Bischoff J, Wang JH, Gu C. Neuropilin-1 functions as a VEGFR2 co-receptor to guide developmental angiogenesis independent of ligand binding. Elife. 2014;3:e03720. doi:10.7554/eLife.03720. PMID:25244320.
  • Prahst C, Heroult M, Lanahan AA, Uziel N, Kessler O, Shraga-Heled N, Simons M, Neufeld G, Augustin HG. Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1. J Biol Chem. 2008;283:25110-4. doi:10.1074/jbc.C800137200. PMID:18628209.
  • Sarabipour S, Ballmer-Hofer K, Hristova K. VEGFR-2 conformational switch in response to ligand binding. Elife. 2016;5:e13876. doi:10.7554/eLife.13876. PMID:27052508.
  • Sarabipour S. Parallels and Distinctions in FGFR, VEGFR, and EGFR Mechanisms of Transmembrane Signaling. Biochemistry. 2017;56:3159-73. doi:10.1021/acs.biochem.7b00399. PMID:28621531.
  • Finger C, Escher C, Schneider D. The single transmembrane domains of human receptor tyrosine kinases encode self-interactions. Sci Signal. 2009;2:ra56. doi:10.1126/scisignal.2000547. PMID:19797273.
  • Cudmore MJ, Hewett PW, Ahmad S, Wang KQ, Cai M, Al-Ani B, Fujisawa T, Ma B, Sissaoui S, Ramma W, et al. The role of heterodimerization between VEGFR-1 and VEGFR-2 in the regulation of endothelial cell homeostasis. Nat Commun. 2012;3:972. doi:10.1038/ncomms1977. PMID:22828632.
  • Favier B, Alam A, Barron P, Bonnin J, Laboudie P, Fons P, Mandron M, Herault JP, Neufeld G, Savi P, et al. Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood. 2006;108:1243-50. doi:10.1182/blood-2005-11-4447. PMID:16621967.
  • Dixelius J, Makinen T, Wirzenius M, Karkkainen MJ, Wernstedt C, Alitalo K, Claesson-Welsh L. Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites. J Biol Chem. 2003;278:40973-9. doi:10.1074/jbc.M304499200. PMID:12881528.
  • Huang K, Andersson C, Roomans GM, Ito N, Claesson-Welsh L. Signaling properties of VEGF receptor-1 and -2 homo- and heterodimers. Int J Biochem Cell Biol. 2001;33:315-24. doi:10.1016/S1357-2725(01)00019-X. PMID:11312102.
  • Senes A, Gerstein M, Engelman DM. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J Mol Biol. 2000;296:921-36. doi:10.1006/jmbi.1999.3488. PMID:10677292.
  • Russ WP, Engelman DM. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol. 2000;296:911-9. doi:10.1006/jmbi.1999.3489. PMID:10677291.
  • Whitaker GB, Limberg BJ, Rosenbaum JS. Vascular endothelial growth factor receptor-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of VEGF(165) and VEGF(121). J Biol Chem. 2001;276:25520-31. doi:10.1074/jbc.M102315200. PMID:11333271.
  • von Wronski MA Tweedle MF, Nunn AD. Binding of the C-terminal amino acids of VEGF121 directly with neuropilin-1 should be considered. FASEB J. 2007;21:1292; author reply 3. doi:10.1096/fj.07-0504ufm. PMID:17470574.
  • Keyt BA, Nguyen HV, Berleau LT, Duarte CM, Park J, Chen H, Ferrara N. Identification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors. Generation of receptor-selective VEGF variants by site-directed mutagenesis. J Biol Chem. 1996;271:5638-46.
  • Gu C, Limberg BJ, Whitaker GB, Perman B, Leahy DJ, Rosenbaum JS, Ginty DD, Kolodkin AL. Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J Biol Chem. 2002;277:18069-76. doi:10.1074/jbc.M201681200. PMID:11886873.
  • Appleton BA, Wu P, Maloney J, Yin J, Liang WC, Stawicki S, Mortara K, Bowman KK, Elliott JM, Desmarais W, et al. Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding. EMBO J. 2007;26:4902-12. doi:10.1038/sj.emboj.7601906. PMID:17989695.
  • Herzog B, Pellet-Many C, Britton G, Hartzoulakis B, Zachary IC. VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation. Mol Biol Cell. 2011;22:2766-76. doi:10.1091/mbc.E09-12-1061. PMID:21653826.
  • Sawma P, Roth L, Blanchard C, Bagnard D, Cremel G, Bouveret E, Duneau JP, Sturgis JN, Hubert P. Evidence for New Homotypic and Heterotypic Interactions between Transmembrane Helices of Proteins Involved in Receptor Tyrosine Kinase and Neuropilin Signaling. J Mol Biol. 2014;426:4099-111. doi:10.1016/j.jmb.2014.10.007. PMID:25315821.
  • Esko JD, Zhang LJ. Influence of core protein sequence on glycosaminoglycan assembly. Curr Opin Struct Biol. 1996;6:663-70. doi:10.1016/S0959-440X(96)80034-0. PMID:8913690.
  • Antoniu SA, Kolb MR. Intedanib, a triple kinase inhibitor of VEGFR, FGFR and PDGFR for the treatment of cancer and idiopathic pulmonary fibrosis. IDrugs. 2010;13:332-45. PMID:20432191.