Ligand-induced internalization selects use of common receptor neuropilin-1 by VEGF165 and semaphorin3A

Blood

Volumn 107, Issue 10, 2006, Pages 3892-3901

  Narazaki, Masashi ^a   Tosato, Giovanna ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; NEUROPILIN 1; SEMAPHORIN 3A; VASCULOTROPIN 121; VASCULOTROPIN 165;

ARTICLE; CELL ADHESION; CELL CULTURE; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPORT; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; RECEPTOR BINDING; STATISTICAL ANALYSIS;

EID: 33646552427     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-10-4113     Document Type: Article

References (55)

1. Serini G, Bussolino F. Common cues in vascular and axon guidance. Physiology (Bethesda). 2004;19:348-354.
2. Weinstein BM. Vessels and nerves: marching to the same tune. Cell. 2005;120:299-302.
3. Storkebaum E, Lambrechts D, Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays. 2004;26:943-954.
4. Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature. 2005;436:193-200.
5. Kolodkin AL, Matthes DJ, Goodman CS. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell. 1993;75:1389-1399.
6. Tessier-Lavigne M, Goodman CS. The molecular biology of axon guidance. Science. 1996;274:1123-1133.
7. Pasterkamp RJ, Kolodkin AL. Semaphorin junction: making tracks toward neural connectivity. Curr Opin Neurobiol. 2003;13:79-89.
8. Tamagnone L, Comoglio PM. Signalling by semaphorin receptors: cell guidance and beyond. Trends Cell Biol. 2000;10:377-383.
9. Gu C, Yoshida Y, Livet J, et al. Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science. 2005;307:265-268.
10. He Z, Tessier-Lavigne M. Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell. 1997;90:739-751.
11. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD. Neuropilin is a semaphorin III receptor. Cell. 1997;90:753-762.
12. Feiner L, Koppel AM, Kobayashi H, Raper JA. Secreted chick semaphorins bind recombinant neuropilin with similar affinities but bind different subsets of neurons in situ. Neuron. 1997;19:539-545.
13. Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM. Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat Neurosci. 1998;1:487-493.
14. Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron. 1997;19:547-559.
15. Gitler AD, Lu MM, Epstein JA. PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell. 2004;7:107-116.
16. Takahashi T, Strittmatter SM. Plexina1 autoinhibition by the plexin sema domain. Neuron. 2001;29:429-439.
17. Yaron A, Huang PH, Cheng HJ, Tessier-Lavigne M. Differential requirement for plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 semaphorins. Neuron. 2005;45:513-523.
18. Serini G, Valdembri D, Zanivan S, et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature. 2003;424:391-397.
19. Gabrilovich DI, Chen HL, Girgis KR, et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med. 1996;2:1096-1103.
20. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676.
21. Rosenstein JM, Krum JM. New roles for VEGF in nervous tissue: beyond blood vessels. Exp Neurol. 2004;187:246-253.
22. 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.
23. Soker S, Fidder H, Neufeld G, Klagsbrun M. Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J Biol Chem. 1996;271:5761-5767.
24. Soker S, Miao HQ, Nomi M, Takashima S, Klagsbrun M. VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J Cell Biochem. 2002;85:357-368.
25. Makinen T, Olofsson B, Karpanen T, et al. Differential binding of vascular endothelial growth factor B splice and proteolytic isoforms to neuropilin-1. J Biol Chem. 1999;274:21217-21222.
26. Migdal M, Huppertz B, Tessler S, et al. Neuropilin-1 is a placenta growth factor-2 receptor. J Biol Chem. 1998;273:22272-22278.
27. 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;277:24818-24825.
28. Wise LM, Veikkola T, Mercer AA, et al. Vascular endothelial growth factor (VEGF)-like protein from orf virus NZ2 binds to VEGFR2 and neuropilin-1. Proc Natl Acad Sci U S A. 1999;96:3071-3076.
29. Gu C, Limberg BJ, Whitaker GB, et al. Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J Biol Chem. 2002;277:18069-18076.
30. Kitsukawa T, Shimizu M, Sanbo M, et al. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 1997;19:995-1005.
31. Kawasaki T, Kitsukawa T, Bekku Y, et al. A requirement for neuropilin-1 in embryonic vessel formation. Development. 1999;126:4895-4902.
32. Gu C, Rodriguez ER, Reimert DV, et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell. 2003;5:45-57.
33. Takagi S, Kasuya Y, Shimizu M, et al. Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system. Dev Biol. 1995;170:207-222.
34. Miao HQ, Soker S, Feiner L, Alonso JL, Raper JA, Klagsbrun M. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J Cell Biol. 1999;146:233-242.
35. Sondell M, Lundborg G, Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci. 1999;19:5731-5740.
36. Salvucci O, Yao L, Villalba S, Sajewicz A, Pittaluga S, Tosato G. Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1. Blood. 2002;99:2703-2711.
37. Ruoslahti E, Vaheri A. Cell-to-cell contact and extracellular matrix. Curr Opin Cell Biol. 1997;9:605-607.
38. Fan J, Mansfield SG, Redmond T, Gordon-Weeks PR, Raper JA. The organization of F-actin and microtubules in growth cones exposed to a brain-derived collapsing factor. J Cell Biol. 1993;121:867-878.
39. West DC, Rees CG, Duchesne L, et al. Interactions of multiple heparin binding growth factors with neuropilin-1 and potentiation of the activity of fibroblast growth factor-2. J Biol Chem. 2005;280:13457-13464.
40. Lubarsky B, Krasnow MA. Tube morphogenesis: making and shaping biological tubes. Cell. 2003;112:19-28.
41. Takahashi T, Fournier A, Nakamura F, et al. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell. 1999;99:59-69.
42. Tordjman R, Ortega N, Coulombel L, Plouet J, Romeo PH, Lemarchandel V. Neuropilin-1 is expressed on bone marrow stromal cells: a novel interaction with hematopoietic cells? Blood. 1999;94:2301-2309.
43. Schwamborn JC, Fiore R, Bagnard D, Kappler J, Kaltschmidt C, Puschel AW. Semaphorin 3A stimulates neurite extension and regulates gene expression in PC12 cells. J Biol Chem. 2004;279:30923-30926.
44. 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;90:10705-10709.
45. Castellani V, Falk J, Rougon G. Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol Cell Neurosci. 2004;26:89-100.
46. Duval M, Bedard-Goulet S, Delisle C, Gratton JP. Vascular endothelial growth factor-dependent down-regulation of Flk-1/KDR involves Cbl-mediated ubiquitination: consequences on nitric oxide production from endothelial cells. J Biol Chem. 2003;278:20091-20097.
47. Kobayashi S, Sawano A, Nojima Y, Shibuya M, Maru Y. The c-Cbl/CD2AP complex regulates VEGF-induced endocytosis and degradation of Flt-1 (VEGFR-1). Faseb J. 2004;18:929-931.
48. Rechsteiner M, Rogers SW. PEST sequences and regulation by proteolysis. Trends Biochem Sci. 1996;21:267-271.
49. Cheng L, Jia H, Lohr M, et al. Anti-chemorepulsive effects of vascular endothelial growth factor and placental growth factor-2 in dorsal root ganglion neurons are mediated via neuropilin-1 and cyclooxygenase-derived prostanoid production. J Biol Chem. 2004;279:30654-30661.
50. Castro-Rivera E, Ran S, Thorpe P, Minna JD. Semaphorin 3B (SEMA3B) induces apoptosis in lung and breast cancer, whereas VEGF165 antagonizes this effect. Proc Natl Acad Sci U S A. 2004;101:11432-11437.
51. 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;275:18040-18045.
52. Tordjman R, Lepelletier Y, Lemarchandel V, et al. A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nat Immunol. 2002;3:477-482.
53. Yamada Y, Oike Y, Ogawa H, et al. Neuropilin-1 on hematopoietic cells as a source of vascular development. Blood. 2003;101:1801-1809.
54. Gabrilovich D, Ishida T, Oyama T, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood. 1998;92:4150-4166.
55. Kishimoto T, Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood. 1995;86:1243-1254.