Neuropilins in neoplasms: Expression, regulation, and function

Experimental Cell Research

Volumn 312, Issue 5, 2006, Pages 584-593

  Bielenberg, Diane R ^a   Pettaway, Curtis A ^b   Takashima, Seiji ^c   Klagsbrun, Michael ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Angiogenesis; Endothelial cells; Keratinocytes; Lymphatic endothelial cells; Melanoma; Metastasis; Neuropilin; Prostate carcinoma; Semaphorin; VEGF

Indexed keywords

ANGIOGENESIS INHIBITOR; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR; DOXYCYCLINE; EPIDERMAL GROWTH FACTOR; FLUOROURACIL; GEMCITABINE; NEUROPILIN 1; NEUROPILIN 2; SEMAPHORIN 3A; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; VASCULOTROPIN;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; BRAIN ISCHEMIA; BREAST CANCER; CANCER GRADING; CANCER RESISTANCE; CANCER SURVIVAL; CARCINOGENESIS; CARCINOMA; CELL DIFFERENTIATION; CELL FATE; CELL MIGRATION; DIGESTIVE SYSTEM CANCER; DOWN REGULATION; ENDOTHELIUM CELL; EPITHELIUM CELL; GENE SILENCING; HUMAN; LIGAND BINDING; MELANOMA; METASTASIS; MICROENVIRONMENT; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; SENSORY NERVE CELL; TRANSCRIPTION REGULATION; TUMOR GROWTH; UPREGULATION;

EID: 33344474679     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.11.024     Document Type: Review

References (83)

1. H. Fujisawa From the discovery of neuropilin to the determination of its adhesion sites Adv. Exp. Med. Biol. 515 2002 1 12
2. 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
3. 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
4. M. Klagsbrun, S. Takashima, and R. Mamluk The role of neuropilin in vascular and tumor biology Adv. Exp. Med. Biol. 515 2002 33 48
5. R. Mamluk, Z. Gechtman, M.E. Kutcher, N. Gasiunas, J. Gallagher, and M. Klagsbrun Neuropilin-1 binds vascular endothelial growth factor 165 placenta growth factor-2, and heparin via its b1b2 domain J. Biol. Chem. 277 2002 24818 24825
6. H. 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
7. M.L. Gagnon, D.R. Bielenberg, Z. Gechtman, H.Q. Miao, S. Takashima, S. Soker, and M. Klagsbrun Identification of a natural soluble neuropilin-1 that binds vascular endothelial growth factor: in vivo expression and antitumor activity Proc. Natl. Acad. Sci. U. S. A. 97 2000 2573 2578
8. 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
9. 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
10. Semaphorin Nomenclature Committee Unified nomenclature for the semaphorins/collapsins Cell 97 1999 551 552
11. Z. He, and M. Tessier-Lavigne Neuropilin is a receptor for the axonal chemorepellent Semaphorin III Cell 90 1997 739 751
12. J.A. Raper Semaphorins and their receptors in vertebrates and invertebrates Curr. Opin. Neurobiol. 10 2000 88 94
13. A. Bagri, and M. Tessier-Lavigne Neuropilins as Semaphorin receptors: in vivo functions in neuronal cell migration and axon guidance Adv. Exp. Med. Biol. 515 2002 13 31
14. C. Gu, B.J. Limberg, G.B. Whitaker, B. Perman, D.J. Leahy, J.S. Rosenbaum, D.D. Ginty, and A.L. Kolodkin 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
15. R.H. Adams, M. Lohrum, A. Klostermann, H. Betz, and A.W. Puschel The chemorepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing EMBO J. 16 1997 6077 6086
16. A.W. Puschel The function of neuropilin/plexin complexes Adv. Exp. Med. Biol. 515 2002 71 80
17. A. Yaron, P.H. Huang, H.J. Cheng, and M. Tessier-Lavigne Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins Neuron 45 2005 513 523
18. 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
19. 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 34588
20. S. Soker, H.Q. Miao, M. Nomi, S. Takashima, and M. Klagsbrun VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding J. Cell. Biochem. 85 2002 357 368
21. P.M. Becker, J. Waltenberger, R. Yachechko, T. Mirzapoiazova, J.S. Sham, C.G. Lee, J.A. Elias, and A.D. Verin Neuropilin-1 regulates vascular endothelial growth factor-mediated endothelial permeability Circ. Res. 96 2005 1257 1265
22. R. Mamluk, M. Detmar, M. Klagsbrun, and D.R. Bielenberg Soluble neuropilin targeted to the skin inhibits vascular permeability Angiogenesis 8 2005 217 227
23. M. Klagsbrun, and A. Eichmann A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis Cytokine Growth Factor Rev. 16 2005 535 548
24. A. Eichmann, F.L. Noble, M. Autiero, and P. Carmeliet Guidance of vascular and neural network formation Curr. Opin. Neurobiol. 15 2005 108 115
25. H. Chen, Z. He, A. Bagri, and M. Tessier-Lavigne Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins Neuron 21 1998 1283 1290
26. T. Kawasaki, T. Kitsukawa, Y. Bekku, Y. Matsuda, M. Sanbo, T. Yagi, and H. Fujisawa A requirement for neuropilin-1 in embryonic vessel formation Development 126 1999 4895 4902
27. L. Yuan, D. Moyon, L. Pardanaud, C. Breant, M.J. Karkkainen, K. Alitalo, and A. Eichmann Abnormal lymphatic vessel development in neuropilin 2 mutant mice Development 129 2002 4797 4806
28. 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
29. F. le Noble, D. Moyon, L. Pardanaud, L. Yuan, V. Djonov, R. Matthijsen, C. Breant, V. Fleury, and A. Eichmann Flow regulates arterial-venous differentiation in the chick embryo yolk sac Development 131 2004 361 375
30. S. Kwei, G. Stavrakis, M. Takahas, G. Taylor, M.J. Folkman, M.A. Gimbrone Jr., and G. Garcia-Cardena Early adaptive responses of the vascular wall during venous arterialization in mice Am. J. Pathol. 164 2004 81 89
31. D.R. Bielenberg, Y. Hida, A. Shimizu, A. Kaipainen, M. Kreuter, C.C. Kim, and M. Klagsbrun Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype J. Clin. Invest. 114 2004 1260 1271
32. S. Takashima, M. Kitakaze, M. Asakura, H. Asanuma, S. Sanada, F. Tashiro, H. Niwa, J. Miyazaki Ji, S. Hirota, Y. Kitamura, T. Kitsukawa, H. Fujisawa, M. Klagsbrun, and M. Hori Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis Proc. Natl. Acad. Sci. U. S. A. 99 2002 3657 3662
33. T. Cohen, Y. Herzog, A. Brodzky, J.K. Greenson, S. Eldar, Z. Gluzman-Poltorak, G. Neufeld, and M.B. Resnick Neuropilin-2 is a novel marker expressed in pancreatic islet cells and endocrine pancreatic tumours J. Pathol. 198 2002 77 82
34. 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
35. J. Harper, L.C. Gerstenfeld, and M. Klagsbrun Neuropilin-1 expression in osteogenic cells: down-regulation during differentiation of osteoblasts into osteocytes J. Cell. Biochem. 81 2001 82 92
36. P.H. Romeo, V. Lemarchandel, and R. Tordjman Neuropilin-1 in the immune system Adv. Exp. Med. Biol. 515 2002 49 54
37. J. Ara, P. Bannerman, F. Shaheen, and D.E. Pleasure Schwann cell-autonomous role of neuropilin-2 J. Neurosci. Res. 79 2005 468 475
38. E.J. Kim, H.Y. Park, M. Yaar, and B.A. Gilchrest Modulation of vascular endothelial growth factor receptors in melanocytes Exp. Dermatol. 14 2005 625 633
39. Z.G. Zhang, W. Tsang, L. Zhang, C. Powers, and M. Chopp Up-regulation of neuropilin-1 in neovasculature after focal cerebral ischemia in the adult rat J. Cereb. Blood Flow Metab. 21 2001 541 549
40. H. Fujita, B. Zhang, K. Sato, J. Tanaka, and M. Sakanaka Expressions of neuropilin-1, neuropilin-2 and semaphorin 3A mRNA in the rat brain after middle cerebral artery occlusion Brain Res. 914 2001 1 14
41. J. Shen, R. Samul, J. Zimmer, H. Liu, X. Liang, S. Hackett, and P.A. Campochiaro Deficiency of neuropilin 2 suppresses VEGF-induced retinal neovascularization Mol. Med. 10 2004 12 18
42. P. Ottino, J. Finley, E. Rojo, A. Ottlecz, G.N. Lambrou, H.E. Bazan, and N.G. Bazan Hypoxia activates matrix metalloproteinase expression and the VEGF system in monkey choroid-retinal endothelial cells: involvement of cytosolic phospholipase A2 activity Mol. Vision 10 2004 341 350
43. H. Oh, H. Takagi, A. Otani, S. Koyama, S. Kemmochi, A. Uemura, and Y. Honda Selective induction of neuropilin-1 by vascular endothelial growth factor (VEGF): a mechanism contributing to VEGF-induced angiogenesis Proc. Natl. Acad. Sci. U. S. A. 99 2002 383 388
44. E. Giraudo, L. Primo, E. Audero, H.P. Gerber, P. Koolwijk, S. Soker, M. Klagsbrun, N. Ferrara, and F. Bussolino Tumor necrosis factor-alpha regulates expression of vascular endothelial growth factor receptor-2 and of its co-receptor neuropilin-1 in human vascular endothelial cells J. Biol. Chem. 273 1998 22128 22135
45. M. Akagi, M. Kawaguchi, W. Liu, M.F. McCarty, A. Takeda, F. Fan, O. Stoeltzing, A.A. Parikh, Y.D. Jung, C.D. Bucana, P.F. Mansfield, D.J. Hicklin, and L.M. Ellis Induction of neuropilin-1 and vascular endothelial growth factor by epidermal growth factor in human gastric cancer cells Br. J. Cancer 88 2003 796 802
46. A.A. Parikh, F. Fan, W.B. Liu, S.A. Ahmad, O. Stoeltzing, N. Reinmuth, D. Bielenberg, C.D. Bucana, M. Klagsbrun, and L.M. Ellis Neuropilin-1 in human colon cancer: expression, regulation, and role in induction of angiogenesis Am. J. Pathol. 164 2004 2139 2151
47. A.A. Parikh, W.B. Liu, F. Fan, O. Stoeltzing, N. Reinmuth, C.J. Bruns, C.D. Bucana, D.B. Evans, and L.M. Ellis Expression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma Cancer 98 2003 720 729
48. M. Rossignol, J. Pouyssegur, and M. Klagsbrun Characterization of the neuropilin-1 promoter; gene expression is mediated by the transcription factor Sp1 J. Cell. Biochem. 88 2003 744 757
49. Y.K. Hong, N. Harvey, Y.H. Noh, V. Schacht, S. Hirakawa, M. Detmar, and G. Oliver Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate Dev. Dyn. 225 2002 351 357
50. L.R. You, F.J. Lin, C.T. Lee, F.J. DeMayo, M.J. Tsai, and S.Y. Tsai Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity Nature 435 2005 98 104
51. J.M. Coulson Transcriptional regulation: cancer, neurons and the REST Curr. Biol. 15 2005 R665 R668
52. T. Nakagawa, M. Abe, T. Yamazaki, H. Miyashita, H. Niwa, S. Kokubun, and Y. Sato HEX acts as a negative regulator of angiogenesis by modulating the expression of angiogenesis-related gene in endothelial cells in vitro Arterioscler., Thromb., Vasc. Biol. 23 2003 231 237
53. H. Yamagishi, E.N. Olson, and D. Srivastava The basic helix-loop-helix transcription factor, dHAND, is required for vascular development J. Clin. Invest. 105 2000 261 270
54. D. Watanabe, H. Takagi, K. Suzuma, I. Suzuma, H. Oh, H. Ohashi, S. Kemmochi, A. Uemura, T. Ojima, E. Suganami, N. Miyamoto, Y. Sato, and Y. Honda Transcription factor Ets-1 mediates ischemia- and vascular endothelial growth factor-dependent retinal neovascularization Am. J. Pathol. 164 2004 1827 1835
55. J.S. Wey, O. Stoeltzing, and L.M. Ellis Vascular endothelial growth factor receptors: expression and function in solid tumors Clin. Adv. Hematol. Oncol. 3 2005 37 45
56. G. Neufeld, N. Shraga-Heled, T. Lange, N. Guttmann-Raviv, Y. Herzog, and O. Kessler Semaphorins in cancer Front. Biosci. 10 2005 751 760
57. D.R. Bielenberg, P. Kurschat, and M. Klagsbrun Neuropilins, receptors central to angiogenesis and neuronal guidance W. Aird Comprehensive Treatise on Endothelial Biomedicine 2005 Cambridge Univ. Press Cambridge
58. T. Kawakami, T. Tokunaga, H. Hatanaka, H. Kijima, H. Yamazaki, Y. Abe, Y. Osamura, H. Inoue, Y. Ueyama, and M. Nakamura Neuropilin 1 and neuropilin 2 co-expression is significantly correlated with increased vascularity and poor prognosis in nonsmall cell lung carcinoma Cancer 95 2002 2196 2201
59. L. Qi, W.A. Robinson, B.M. Brady, and L.M. Glode Migration and invasion of human prostate cancer cells is related to expression of VEGF and its receptors Anticancer Res. 23 2003 3917 3922
60. A. Latil, I. Bieche, S. Pesche, A. Valeri, G. Fournier, O. Cussenot, and R. Lidereau VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms Int. J. Cancer 89 2000 167 171
61. P.J. Vanveldhuizen, M. Zulfiqar, S. Banerjee, R. Cherian, N.K. Saxena, A. Rabe, J.B. Thrasher, and S.K. Banerjee Differential expression of neuropilin-1 in malignant and benign prostatic stromal tissue Oncol. Rep. 10 2003 1067 1071
62. H.Q. Miao, P. Lee, H. Lin, S. Soker, and M. Klagsbrun Neuropilin-1 expression by tumor cells promotes tumor angiogenesis and progression FASEB J. 14 2000 2532 2539
63. L.E. Benjamin, D. Golijanin, A. Itin, D. Pode, and E. Keshet Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal J. Clin. Invest. 103 1999 159 165
64. D.E. Hansel, R.E. Wilentz, C.J. Yeo, R.D. Schulick, E. Montgomery, and A. Maitra Expression of neuropilin-1 in high-grade dysplasia, invasive cancer, and metastases of the human gastrointestinal tract Am. J. Surg. Pathol. 28 2004 347 356
65. M. Li, H. Yang, H. Chai, W.E. Fisher, X. Wang, F.C. Brunicardi, Q. Yao, and C. Chen Pancreatic carcinoma cells express neuropilins and vascular endothelial growth factor, but not vascular endothelial growth factor receptors Cancer 101 2004 2341 2350
66. M.J. Gray, J.S. Wey, A. Belcheva, M.F. McCarty, J.G. Trevino, D.B. Evans, L.M. Ellis, and G.E. Gallick Neuropilin-1 suppresses tumorigenic properties in a human pancreatic adenocarcinoma cell line lacking neuropilin-1 coreceptors Cancer Res. 65 2005 3664 3670
67. J.S. Wey, M.J. Gray, F. Fan, A. Belcheva, M.F. McCarty, O. Stoeltzing, R. Somcio, W. Liu, D.B. Evans, M. Klagsbrun, G.E. Gallick, and L.M. Ellis Overexpression of neuropilin-1 promotes constitutive MAPK signalling and chemoresistance in pancreatic cancer cells Br. J. Cancer 93 2005 233 241
68. S.C. Heffelfinger, M. Yan, R.B. Gear, J. Schneider, K. LaDow, and D. Warshawsky Inhibition of VEGFR2 prevents DMBA-induced mammary tumor formation Lab. Invest. 84 2004 989 998
69. R.E. Bachelder, A. Crago, J. Chung, M.A. Wendt, L.M. Shaw, G. Robinson, and A.M. Mercurio Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells Cancer Res. 61 2001 5736 5740
70. R.E. Bachelder, E.A. Lipscomb, X. Lin, M.A. Wendt, N.H. Chadborn, B.J. Eickholt, and A.M. Mercurio Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells Cancer Res. 63 2003 5230 5233
71. 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
72. G. Serini, D. Valdembri, S. Zanivan, G. Morterra, C. Burkhardt, F. Caccavari, L. Zammataro, L. Primo, L. Tamagnone, M. Logan, M. Tessier-Lavigne, M. Taniguchi, A.W. Puschel, and F. Bussolino Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function Nature 424 2003 391 397
73. D. Bates, G.I. Taylor, J. Minichiello, P. Farlie, A. Cichowitz, N. Watson, M. Klagsbrun, R. Mamluk, and D.F. Newgreen Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1 Dev. Biol. 255 2003 77 98
74. O. Kessler, N. Shraga-Heled, T. Lange, N. Gutmann-Raviv, E. Sabo, L. Baruch, M. Machluf, and G. Neufeld Semaphorin-3F is an inhibitor of tumor angiogenesis Cancer Res. 64 2004 1008 1015
75. Y. Tomizawa, Y. Sekido, M. Kondo, B. Gao, J. Yokota, J. Roche, H. Drabkin, M.I. Lerman, A.F. Gazdar, and J.D. Minna Inhibition of lung cancer cell growth and induction of apoptosis after reexpression of 3p21.3 candidate tumor suppressor gene SEMA3B Proc. Natl. Acad. Sci. U. S. A. 98 2001 13954 13959
76. C. Tse, R.H. Xiang, T. Bracht, and S.L. Naylor Human Semaphorin 3B (SEMA3B) located at chromosome 3p21.3 suppresses tumor formation in an adenocarcinoma cell line Cancer Res. 62 2002 542 546
77. 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. U. S. A. 101 2004 11432 11437
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. S. Kusy, P. Nasarre, D. Chan, V. Potiron, D. Meyronet, R.M. Gemmill, B. Constantin, H.A. Drabkin, and J. Roche Selective suppression of in vivo tumorigenicity by semaphorin SEMA3F in lung cancer cells Neoplasia 7 2005 457 465
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. P. Nasarre, B. Constantin, L. Rouhaud, T. Harnois, G. Raymond, H.A. Drabkin, N. Bourmeyster, and J. Roche Semaphorin SEMA3F and VEGF have opposing effects on cell attachment and spreading Neoplasia 5 2003 83 92
82. P. Kurschat, D. Bielenberg, M. Rossignol, A. Stahl, M. Klagsbrun, The neuron restrictive silencer factor NRSF/REST is a transcriptional repressor of neuropilin-1 and diminishes the ability of semaphorin 3A to inhibit keratinocyte migration, J. Biol. Chem. (in press) (Dec. 5, Epub ahead of print).
83. Y.K. Hong, and M. Detmar Prox1, master regulator of the lymphatic vasculature phenotype Cell Tissue Res. 314 2003 85 92