The neuropilins and their role in tumorigenesis and tumor progression

Cancer Letters

Volumn 231, Issue 1, 2006, Pages 1-11

  Guttmann Raviv, Noga ^a   Kessler, Ofra ^a   Shraga Heled, Niva ^a   Lange, Tali ^a   Herzog, Yael ^a   Neufeld, Gera ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Angiogenesis; Invasion; Metastasis; Neuropilin 1; Neuropilin 2; Plexin; Review; Semaphorin; Tumor progression; Tumorigenesis

Indexed keywords

MEMBRANE RECEPTOR; NEUROPILIN; PLEXIN; SEMAPHORIN 3A; VASCULOTROPIN;

ANGIOGENESIS; CANCER CELL; CARCINOGENESIS; CELL TYPE; ENDOTHELIUM CELL; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; SHORT SURVEY; TUMOR CELL; TUMOR GROWTH;

EID: 28844483828     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2004.12.047     Document Type: Review

References (90)

1. A.L. Kolodkin, D.V. Levengood, E.G. Rowe, Y.T. Tai, R.J. Giger, and D.D. Ginty Neuropilin is a semaphorin III receptor Cell 90 1997 753 762
2. Z. He, and M. Tessier-Lavigne Neuropilin is a receptor for the axonal chemorepellent Semaphorin III Cell 90 1997 739 751
3. C. Gu, Y. Yoshida, J. Livet, D.V. Reimert, F. Mann, and J. Merte Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins Science 307 2005 265 268
4. R.J. Giger, E.R. Urquhart, S.K. Gillespie, D.V. Levengood, D.D. Ginty, and A.L. Kolodkin Neuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity Neuron 21 1998 1079 1092
5. T. Takahashi, F. Nakamura, Z. Jin, R.G. Kalb, and S.M. Strittmatter Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors Nat. Neurosci. 1 1998 487 493
6. F. Nakamura, M. Tanaka, T. Takahashi, R.G. Kalb, and S.M. Strittmatter Neuropilin-1 extracellular domains mediate semaphorin D/III- induced growth cone collapse Neuron 21 1998 1093 1100
7. T. Takahashi, A. Fournier, F. Nakamura, L.H. Wang, Y. Murakami, and R.G. Kalb Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors Cell 99 1999 59 69
8. L. Tamagnone, S. Artigiani, H. Chen, Z. He, G.I. Ming, and H. Song Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates Cell 99 1999 71 80
9. F. Suto, Y. Murakami, F. Nakamura, Y. Goshima, and H. Fujisawa Identification and characterization of a novel mouse plexin, plexin-A4 Mech. Dev. 120 2003 385 396
10. T. Takahashi, and S.M. Strittmatter PlexinA1 Autoinhibition by the plexin sema domain Neuron 29 2001 429 439
11. B. Rohm, A. Ottemeyer, M. Lohrum, and A.W. Pueschel Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A Mech. Dev. 93 2000 95 104
12. J. Torres-Vazquez, A.D. Gitler, S.D. Fraser, J.D. Berk, N.P. Van, and M.C. Fishman Semaphorin-plexin signaling guides patterning of the developing vasculature Dev. Cell 7 2004 117 123
13. A.D. Gitler, M.M. Lu, and J.A. Epstein PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development Dev. Cell 7 2004 107 116
14. L. Wang, H. Zeng, P. Wang, S. Soker, and D. Mukhopadhyay Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration J. Biol. Chem. 278 2003 48848 48860
15. H.B. Cai, and R.R. Reed Cloning and characterization of neuropilin-1-interacting protein: a PSD-95/Dlg/ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1 J. Neurosci. 19 1999 6519 6527
16. V. Castellani, A. Chedotal, M. Schachner, C. Faivre-Sarrailh, and G. Rougon Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance Neuron 27 2000 237 249
17. V. Castellani, E. De Angelis, S. Kenwrick, and G. Rougon Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A Eur. Mol. Biol. Org. J. 21 2002 6348 6357
18. F. Polleux, T. Morrow, and A. Ghosh Semaphorin 3A is a chemoattractant for cortical apical dendrites Nature 404 2000 567 573
19. Z. Gluzman-Poltorak, T. Cohen, M. Shibuya, and G. Neufeld Vascular endothelial growth factor receptor-1 and neuropilin-2 form complexes J. Biol. Chem. 276 2001 18688 18694
20. G. Fuh, K.C. Garcia, and A.M. De Vos The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor Flt-1 J. Biol. Chem. 275 2000 26690 26695
21. D. Bagnard, C. Vaillant, S.T. Khuth, N. Dufay, M. Lohrum, and A.W. Puschel Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor J. Neurosci. 21 2001 3332 3341
22. G.B. Whitaker, B.J. Limberg, and J.S. Rosenbaum 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. 276 2001 25520 25531
23. S. Soker, H.Q. Miao, M. Nomi, S. Takashima, and M. Klagsbrun VEGF(165) mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF(165)-receptor binding J. Cell. Biochem. 85 2002 357 368
24. C. Gu, B.J. Limberg, G.B. Whitaker, B. Perman, D.J. Leahy, and J.S. Rosenbaum Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165 J. Biol. Chem. 277 2002 18069 18076
25. S. Soker, S. Takashima, H.Q. Miao, G. Neufeld, and M. Klagsbrun Neuropilin-1 is expressed by endothelial and tumor cells as an isoform specific receptor for vascular endothelial growth factor Cell 92 1998 735 745
26. M. Rossignol, M.L. Gagnon, and M. Klagsbrun Genomic organization of human neuropilin-1 and neuropilin-2 genes: identification and distribution of splice variants and soluble isoforms Genomics 70 2000 211 222
27. M.L. Gagnon, D.R. Bielenberg, Z. Gechtman, H.Q. Miao, S. Takashima, and S. Soker Identification of a natural soluble neuropilin-1 that binds vascular endothelial growth factor: in vivo expression and antitumor activity Proc. Natl Acad. Sci. USA 97 2000 2573 2578
28. F.C. Cackowski, L. Xu, B. Hu, and S.Y. Cheng Identification of two novel alternatively spliced neuropilin-1 isoforms Genomics 84 2004 82 94
29. Y. Yamada, N. Takakura, H. Yasue, H. Ogawa, H. Fujisawa, and T. Suda Exogenous clustered neuropilin 1 enhances vasculogenesis and angiogenesis Blood 97 2001 1671 1678
30. L. Trusolino, and P.M. Comoglio Scatter-factor and semaphorin receptors: cell signalling for invasive growth Nat. Rev. Cancer 2 2002 289 300
31. S. Giordano, S. Corso, P. Conrotto, S. Artigiani, G. Gilestro, and D. Barberis The semaphorin 4D receptor controls invasive growth by coupling with Met Nat. Cell Biol. 4 2002 720 724
32. T. Toyofuku, H. Zhang, A. Kumanogoh, N. Takegahara, F. Suto, and J. Kamei Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, plexin-A1, with off-tack and vascular endothelial growth factor receptor type 2 Genes Dev. 18 2004 435 447
33. T. Toyofuku, H. Zhang, A. Kumanogoh, N. Takegahara, M. Yabuki, and K. Harada Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling Nat. Cell Biol. 2004
34. H. Usui, M. Taniguchi, T. Yokomizo, and T. Shimizu Plexin-A1 and plexin-B1 specifically interact at their cytoplasmic domains Biochem. Biophys. Res. Commun. 300 2003 927 931
35. M.L. Winberg, L. Tamagnone, J. Bai, P.M. Comoglio, D. Montell, and C.S. Goodman The transmembrane protein off-track associates with plexins and functions downstream of semaphorin signaling during axon guidance Neuron 32 2001 53 62
36. C.S. Goodman, A.L. Kolodkin, Y. Luo, A.W. Pueschel, and J.A. Raper Unified nomenclature for the semaphorins collapsins Cell 97 1999 551 552
37. L. Feiner, A.M. Koppel, H. Kobayashi, and J.A. Raper Secreted chick semaphorins bind recombinant neuropilin with similar affinities but bind different subsets of neurons in situ Neuron 19 1997 539 545
38. C.A. Love, K. Harlos, N. Mavaddat, S.J. Davis, D.I. Stuart, and E.Y. Jones The ligand-binding face of the semaphorins revealed by the high-resolution crystal structure of SEMA4D Nat. Struct. Biol. 10 2003 843 848
39. A. Antipenko, J.P. Himanen, K. van Leyen, V. Nardi-Dei, J. Lesniak, and W.A. Barton Structure of the semaphorin-3A receptor binding module Neuron 39 2003 589 598
40. A.M. Koppel, and J.A. Raper Collapsin-1 covalently dimerizes, and dimerization is necessary for collapsing activity J. Biol. Chem. 273 1998 15708 15713
41. A. Klostermann, M. Lohrum, R.H. Adams, and A.W. Puschel The chemorepulsive activity of the axonal guidance signal semaphorin D requires dimerization J. Biol. Chem. 273 1998 7326 7331
42. J. De Wit, and J. Verhaagen Role of semaphorins in the adult nervous system Prog. Neurobiol. 71 2003 249 267
43. L. Tamagnone, and P.M. Comoglio To move or not to move? Eur. Mol. Biol. Org. Rep. 5 2004 356 361
44. A. Kumanogoh, and H. Kikutani Roles of the semaphorin family in immune regulation Adv. Immunol. 81 2003 173 198
45. L. Feiner, A.L. Webber, C.B. Brown, M.M. Lu, L. Jia, and P. Feinstein Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption Development 128 2001 3061 3070
46. G. Neufeld, T. Cohen, S. Gengrinovitch, and Z. Poltorak Vascular endothelial growth factor (VEGF) and its receptors Fed. Am. Soc. Exp. Biol. J. 13 1999 9 22
47. S. Gengrinovitch, S.M. Greenberg, T. Cohen, H. Gitay-Goren, P. Rockwell, and T.E. Maione Platelet factor-4 inhibits the mitogenic activity of VEGF-121 and VEGF-165 using several concurrent mechanisms J. Biol. Chem. 270 1995 15059 15065
48. H.T. Zhang, P. Craft, P.A.E. Scott, M. Ziche, H.A. Weich, and A.L. Harris Enhancement of tumor growth and vascular density by transfection of vascular endothelial cell growth factor into MCF-7 human breast carcinoma cells J. Nat. Cancer Inst. 87 1995 213 219
49. J. Wilting, R. Birkenhager, A. Eichmann, H. Kurz, G. Martinybaron, and D. Marme VEGF(121) induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of the chorioallantoic membrane Dev. Biol. 176 1996 76 85
50. P. Carmeliet, Y.S. Ng, D. Nuyens, G. Theilmeier, K. Brusselmans, and I. Cornelissen Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188 Nat. Med. 5 1999 495 502
51. H. Gitay-Goren, T. Cohen, S. Tessler, S. Soker, S. Gengrinovitch, and P. Rockwell Selective binding of VEGF121 to one of the three VEGF receptors of vascular endothelial cells J. Biol. Chem. 271 1996 5519 5523
52. S. Soker, H. Fidder, G. Neufeld, and M. Klagsbrun Characterization of novel VEGF binding proteins associated with tumor cells that bind VEGF165 but not VEGF121 J. Biol. Chem. 271 1996 5761 5767
53. H. Chen, A. Chedotal, Z. He, C.S. Goodman, and M. Tessier-Lavigne 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 19 1997 547 559
54. Z. Gluzman-Poltorak, T. Cohen, Y. Herzog, and G. Neufeld Neuropilin-2 and neuropilin-1 are receptors for 165-amino acid long form of vascular endothelial growth factor (VEGF) and of placenta growth factor-2, but only neuropilin-2 functions as a receptor for the 145 amino acid form of VEGF J. Biol. Chem. 275 2000 18040 18045
55. J. Shen, R. Samul, J. Zimmer, H. Liu, X. Liang, and S. Hackett Deficiency of neuropilin 2 suppresses VEGF-induced retinal neovascularization Mol. Med. 10 2004 12 18
56. M. Migdal, B. Huppertz, S. Tessler, A. Comforti, M. Shibuya, and R. Reich Neuropilin-1 is a placenta growth factor-2 receptor J. Biol. Chem. 273 1998 22272 22278
57. T. Makinen, B. Olofsson, T. Karpanen, U. Hellman, S. Soker, and M. Klagsbrun Differential binding of vascular endothelial growth factor B splice and proteolytic isoforms to neuropilin-1 J. Biol. Chem. 274 1999 21217 21222
58. M.J. Karkkainen, A. Saaristo, L. Jussila, K.A. Karila, E.C. Lawrence, and K. Pajusola A model for gene therapy of human hereditary lymphedema Proc. Natl Acad. Sci. USA 98 2001 12677 12682
59. U. Eriksson, and K. Alitalo Structure, expression and receptor-binding properties of novel vascular endothelial growth factors Curr. Top. Microbiol. Immunol. 237 1999 41 57
60. J.E. Park, H.H. Chen, J. Winer, K.A. Houck, and N. Ferrara Placenta growth factor - potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk- 1/KDR J. Biol. Chem. 269 1994 25646 25654
61. T. Kawasaki, T. Kitsukawa, Y. Bekku, Y. Matsuda, M. Sanbo, and T. Yagi A requirement for neuropilin-1 in embryonic vessel formation Development 126 1999 4895 4902
62. J. Folkman What is the evidence that tumors are angiogenesis dependent J. Nat. Cancer Inst. 82 1990 4 7
63. H.Q. Miao, P. Lee, H. Lin, S. Soker, and M. Klagsbrun Neuropilin-1 expression by tumor cells promotes tumor angiogenesis and progression Fed. Am. Soc. Exp. Biol. J. 14 2000 2532 2539
64. R.J. Pasterkamp, and A.L. Kolodkin Semaphorin junction: making tracks toward neural connectivity Curr. Opin. Neurobiol. 13 2003 79 89
65. H.Q. Miao, S. Soker, L. Feiner, J.L. Alonso, J.A. Raper, and M. Klagsbrun 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. 146 1999 233 242
66. G. Serini, D. Valdembri, S. Zanivan, G. Morterra, C. Burkhardt, and F. Caccavari Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function Nature 424 2003 391 397
67. D. Bates, G.I. Taylor, J. Minichiello, P. Farlie, A. Cichowitz, and N. Watson Neurovascular congruence results from a shared patterning mechanism that utilizes semaphorin3A and neuropilin-1 Dev. Biol. 255 2003 77 98
68. A. Latil, I. Bieche, S. Pesche, A. Valeri, G. Fournier, and O. Cussenot VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms Int. J. Cancer 89 2000 167 171
69. A.A. Parikh, F. Fan, W.B. Liu, S.A. Ahmad, O. Stoeltzing, and N. Reinmuth Neuropilin-1 in human colon cancer: expression, regulation, and role in induction of angiogenesis Am. J. Pathol. 164 2004 2139 2151
70. P.M. Lacal, C.M. Failla, E. Pagani, T. Odorisio, C. Schietroma, and S. Falcinelli Human melanoma cells secrete and respond to placenta growth factor and vascular endothelial growth factor J. Invest. Dermatol. 115 2000 1000 1007
71. K. Fukahi, M. Fukasawa, G. Neufeld, J. Itakura, and M. Korc Aberrant expression of neuropilin-1 and -2 in human pancreatic cancer cells Clin. Cancer Res. 10 2004 581 590
72. R.E. Bachelder, E.A. Lipscomb, X. Lin, M.A. Wendt, N.H. Chadborn, and B.J. Eickholt Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells Cancer Res. 63 2003 5230 5233
73. Y. Herzog, C. Kalcheim, N. Kahane, R. Reshef, and G. Neufeld Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins Mech. Dev. 109 2001 115 119
74. L. Yuan, D. Moyon, L. Pardanaud, C. Breant, M.J. Karkkainen, and K. Alitalo Abnormal lymphatic vessel development in neuropilin 2 mutant mice Development 129 2002 4797 4806
75. S. Takashima, M. Kitakaze, M. Asakura, H. Asanuma, S. Sanada, and F. Tashiro Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis Proc. Natl Acad. Sci. USA 99 2002 3657 3662
76. J. Roche, F. Boldog, M. Robinson, L. Robinson, M. Varella-Garcia, and M. Swanton Distinct 3p21.3 deletions in lung cancer and identification of a new human semaphorin Oncogene 12 1996 1289 1297
77. Y. Sekido, S. Bader, F. Latif, J.Y. Chen, F.M. Duh, and M.H. Wei 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 93 1996 4120 4125
78. R. Xiang, A.R. Davalos, C.H. Hensel, X.J. Zhou, C. Tse, and S.L. Naylor Semaphorin 3F gene from human 3p21.3 suppresses tumor formation in nude mice Cancer Res. 62 2002 2637 2643
79. P. Nasarre, B. Constantin, L. Rouhaud, T. Harnois, G. Raymond, and H.A. Drabkin Semaphorin SEMA3F and VEGF have opposing effects on cell attachment and spreading Neoplasia 5 2003 83 92
80. E. Brambilla, B. Constantin, H. Drabkin, and J. Roche Semaphorin SEMA3F localization in malignant human lung and cell lines: a suggested role in cell adhesion and cell migration Am. J. Pathol. 156 2000 939 950
81. O. Kessler, N. Shraga-Heled, T. Lange, N. Gutmann-Raviv, E. Sabo, and L. Baruch Semaphorin-3F is an inhibitor of tumor angiogenesis Cancer Res. 64 2004 1008 1015
82. D.R. Bielenberg, Y. Hida, A. Shimizu, A. Kaipainen, M. Kreuter, and C.C. Kim Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype J. Clin. Invest. 114 2004 1260 1271
83. E. Castro-Rivera, S. Ran, P. Thorpe, and J.D. Minna Semaphorin 3B (SEMA3B) induces apoptosis in lung and breast cancer, whereas VEGF165 antagonizes this effect Proc. Natl Acad. Sci. USA 101 2004 11432 11437
84. T. Yamada, R. Endo, M. Gotoh, and S. Hirohashi Identification of semaphorin E as a non-MDR drug resistance gene of human cancers Proc. Natl Acad. Sci. USA 94 1997 14713 14718
85. M. Martin-Satue, and J. Blanco Identification of semaphorin E gene expression in metastatic human lung adenocarcinoma cells by mRNA differential display J. Surg. Oncol. 72 1999 18 23
86. J. Rieger, W. Wick, and M. Weller Human malignant glioma cells express semaphorins and their receptors, neuropilins and plexins Glia 42 2003 379 389
87. C.R. Christensen, J. Klingelhofer, S. Tarabykina, E.F. Hulgaard, D. Kramerov, and E. Lukanidin Transcription of a novel mouse semaphorin gene, M-semaH, correlates with the metastatic ability of mouse tumor cell lines Cancer Res. 58 1998 1238 1244
88. D.O. Bates, T.G. Cui, J.M. Doughty, M. Winkler, M. Sugiono, and J.D. Shields VEGF(165)b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma Cancer Res. 62 2002 4123 4131
89. M. Meiron, R. Anunu, E.J. Scheinman, S. Hashmueli, and B.Z. Levi New isoforms of VEGF are translated from alternative initiation CUG codons located in its 5′UTR Biochem. Biophys. Res. Commun. 282 2001 1053 1060
90. S. Soker, S. Gollamudi-Payne, H. Fidder, H. Charmahelli, and M. Klagsbrun Inhibition of vascular endothelial growth factor (VEGF) induced endothelial cell proliferation by a peptide corresponding to the exon-7 encoded domain of VEGF165 J. Biol. Chem. 272 1997 31582 31588