Role of class 3 semaphorins and their receptors in tumor growth and angiogenesis

Clinical Cancer Research

Volumn 15, Issue 22, 2009, Pages 6763-6770

  Gaur, Puja ^a   Bielenberg, Diane R ^b   Samuel, Shaija ^a   Bose, Debashish ^a   Zhou, Yunfei ^a   Gray, Michael J ^a   Dallas, Nikolaos A ^a   Fan, Fan ^a   Xia, Ling ^a   Lu, Jia ^a   Ellis, Lee M ^a  

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

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; NEUROPILIN 1; NEUROPILIN 2; PLEXIN; SEMAPHORIN 3A; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; CANCER INHIBITION; CELL MIGRATION; CELL MOTILITY; HETEROZYGOSITY LOSS; HUMAN; METASTASIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR GROWTH;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIGANDS; MODELS, BIOLOGICAL; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NERVE TISSUE PROTEINS; NEUROPILINS; SEMAPHORINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 72549108629     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-09-1810     Document Type: Review

References (70)

1. Luo Y, Raible D, Raper JA. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 1993;75:217-227 (Pubitemid 23320286)
2. 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. J Biol Chem 2000;275:29922.
3. 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 (Pubitemid 34274903)
4. 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
5. 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
6. Pan Q, Chanthery Y, Liang WC, et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007;11:53-67. (Pubitemid 46054517)
7. Neufeld G, Kessler O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat Rev Cancer 2008;8: 632-645
8. Raper JA. Semaphorins and their receptors in vertebrates and invertebrates. Curr Opin Neurobiol 2000;10:88-94.
9. Bachelder RE, Lipscomb EA, Lin X, et al. Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells. Cancer Res 2003;63:5230-5233
10. Tamagnone L, Comoglio PM. To move or not to move? Semaphorin signalling in cell migration. EMBO Rep 2004;5:356-361 (Pubitemid 38618276)
11. Gu C, Yoshida Y, Livet J, et al. Semaphorin 3E and plexin-D1 control vascular pattern independentlyof neuropilins. Science 2005;307:265-268
12. Serini G, Maione F, Giraudo E, Bussolino F. Semaphorins and tumor angiogenesis. Angiogenesis 2009;12:187-193
13. Nasarre P, Constantin B, Rouhaud L, et al. Semaphorin SEMA3F and VEGF have opposing effects on cell attachment and spreading. Neoplasia 2003;5:83-92. (Pubitemid 36151061)
14. Nasarre P, Kusy S, Constantin B, et al. Semaphorin SEMA3F has a repulsing activityon breast cancer cells and inhibits E-cadherinmediated cell adhesion. Neoplasia 2005;7:180-189 (Pubitemid 40315995)
15. Tomizawa Y, Sekido Y, Kondo M, et al. 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 2001;98:13954-13959
16. Banu N, Teichman J, Dunlap-Brown M, Villegas G, Tufro A. Semaphorin 3C regulates endothelial cell function byi ncreasing integrin activity. FASEB J 2006;20:2150-2152
17. Martin-Satue M, Blanco J. Identification of semaphorin E gene expression in metastatic human lung adenocarcinoma cells bymRNA differential display. J Surg Oncol 1999;72:18-23. (Pubitemid 29446936)
18. Cai H, Reed RR. 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 1999;19:6519-6527 (Pubitemid 29347451)
19. Ellis LM. The role of neuropilins in cancer. Mol Cancer Ther 2006;5:1099-1107
20. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed byen - dothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998;92:735-745
21. Herzog Y, Kalcheim C, Kahane N, Reshef R, Neufeld G. Differential expression of neuropilin- 1 and neuropilin-2 in arteries and veins. Mech Dev 2001;109:115-119 (Pubitemid 33035924)
22. You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY. Suppression of Notch signalling bythe COUP-TFII transcription factor regulates vein identity. Nature 2005;435:98-104.
23. Yuan L, Moyon D, Pardanaud L, et al. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 2002;129: 4797-4806
24. Karpanen T, Heckman CA, Keskitalo S, et al. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J 2006;20: 1462-1472
25. Appleton BA, Wu P, Maloney J, et al. Structural studies of neuropilin/antibodycomplexes provide insights into semaphorin and VEGF binding. EMBO J 2007;26:4902-4912
26. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008;8:579-591
27. Pan Q, Chathery Y, Wu Y, et al. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J Biol Chem 2007;282: 24049-24056 (Pubitemid 47328044)
28. Aizawa H, Wakatsuki S, Ishii A, et al. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat Neurosci 2001;4:367-373
29. Atwal JK, Singh KK, Tessier-Lavigne M, Miller FD, Kaplan DR. Semaphorin 3F antagonizes neurotrophin-induced phosphatidylinositol 3- kinase and mitogen-activated protein kinase kinase signaling: a mechanism for growth cone collapse. J Neurosci 2003;23:7602-7609
30. Jin Z, Strittmatter SM. Rac1 mediates collapsin- 1-induced growth cone collapse. JNeurosci 1997; 17:6256-6263
31. Serini G, Valdembri D, Zanivan S, et al. Class 3 semaphorins control vascular morphogenesis byinhibiting integrin function. Nature 2003;424: 391-397 (Pubitemid 36917481)
32. Barberis D, Artigiani S, Casazza A, et al. Plexin signaling hampers integrin-based adhesion, leading to ñ-kinase independent cell rounding, and inhibiting lamellipodia extension and cell motility. FASEB J 2004;18:592-594
33. Shimizu A, Mammoto A, Italiano JE, Jr., et al. ABL2/ARG tyrosine kinase mediates SEMA3Finduced ñA inactivation and cytoskeleton collapse in human glioma cells. J Biol Chem 2008; 283:27230-27238
34. Acevedo LM, Barillas S, Weis SM, Gothert JR, Cheresh DA. Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeabilityf actor. Blood 2008;111: 2674-2680
35. Bielenberg DR, Hida Y, Shimizu A, et al. Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorlyvasc ularized, encapsulated, nonmetastatic tumor phenotype. J Clin Invest 2004;114:1260-1271 (Pubitemid 40385297)
36. Guttmann-Raviv N, Shraga-Heled N, Varshavsky A, Guimaraes-Sternberg C, Kessler O, Neufeld G. Semaphorin-3A and semaphorin-3F work together to repel endothelial cells and to inhibit their survival byind uction of apoptosis. J Biol Chem 2007;282:26294-26305
37. Kessler O, Shraga-Heled N, Lange T, et al. Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res 2004;64:1008-1015
38. Kigel B, Varshavsky A , Kessler O, Neufeld G. Successful inhibition of tumor development bys pecific class-3 semaphorins is associated with expression of appropriate semaphorin receptors bytumor cells. PLoS ONE 2008;3:e3287.
39. Roche J, Boldog F, Robinson M, et al. Distinct 3p21.3 deletions in lung cancer and identification of a new human semaphorin. Oncogene 1996;12:1289-1297 (Pubitemid 26128926)
40. Sekido Y, Bader S, Latif F, 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 U S A 1996;93:4120-4125 (Pubitemid 26146727)
41. Futamura M, Kamino H, Miyamoto Y, et al. Possible role of semaphorin 3F, a candidate tumor suppressor gene at 3p21.3, in p53-regulated tumor angiogenesis suppression. Cancer Res 2007;67:1451-1460 (Pubitemid 46383370)
42. KusyS, Potiron V, Zeng C, et al. Promoter characterization of semaphorin SEMA3F, a tumor suppressor gene. Biochim Biophys Acta 2005;1730:66-76. (Pubitemid 41008614)
43. Tse C, Xiang RH, Bracht T, Naylor SL. Human semaphorin 3B (SEMA3B) located at chromosome 3p21.3 suppresses tumor formation in an adenocarcinoma cell line. Cancer Res 2002;62:542-546 (Pubitemid 34106429)
44. Xiang R, Davalos AR, Hensel CH, Zhou XJ, Tse C, Naylor SL. Semaphorin 3F gene from human 3p21.3 suppresses tumor formation in nude mice. Cancer Res 2002;62:2637-2643 (Pubitemid 34462746)
45. 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 (Pubitemid 36827308)
46. Herman JG, Meadows GG. Increased class 3 semaphorin expression modulates the invasive and adhesive properties of prostate cancer cells. Int J Oncol 2007;30:1231-1238
47. 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 (Pubitemid 39038364)
48. KusyS, Nasarre P, Chan D, et al. Selective suppression of in vivo tumorigenicityby semaphorin SEMA3F in lung cancer cells. Neoplasia 2005; 7:457-465
49. Potiron V, Nasarre P, Roche J, Healy C, Boumsell L. Semaphorin signaling in the immune system. Adv Exp Med Biol 2007;600:132-144
50. Osada R, Horiuchi A, Kikuchi N, et al. Expression of semaphorins, vascular endothelial growth factor, and their common receptor neuropilins and allelic 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
51. Muller MW, Giese NA, Swiercz JM, et al. Association of axon guidance factor semaphorin 3A with poor outcome in pancreatic cancer. Int J Cancer 2007;121:2421-2433
52. Potiron VA, Roche J, Drabkin HA. Semaphorins and their receptors in lung cancer. Cancer Lett 2009;273:1-14.
53. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathwayi n tumor growth and angiogenesis. J Clin Oncol 2005; 23:1011-1027 (Pubitemid 46202320)
54. Dallas NA, Fan F, Gray MJ, et al. Functional significance of vascular endothelial growth factor receptors on gastrointestinal cancer cells. Cancer Metastasis Rev 2007;26:433-441
55. Luttun A, Brusselmans K, Fukao H, et al. Loss of placental growth factor protects mice against vascular permeabilityin pathological conditions. Biochem Biophys Res Commun 2002;295:428-434 (Pubitemid 34785852)
56. Luttun A, Tjwa M, Carmeliet P. Placental growth factor (PlGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann N Y Acad Sci 2002;979:80-93.
57. Luttun A, Tjwa M, Moons L, et al. Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis byanti- Flt1. Nat Med 2002; 8:831-840 (Pubitemid 34887247)
58. Fischer C, Jonckx B, Mazzone M, et al. Anti- PlGF inhibits growth of VEGF(R)-inhibitorresistant tumors without affecting healthy vessels. Cell 2007;131:463-475
59. Fan F, Wey JS, McCarty MF, et al. Expression and function of vascular endothelial growth factor receptor-1 on human colorectal cancer cells. Oncogene 2005;24:2647-2653 (Pubitemid 40593092)
60. Wey JS, Fan F, Gray MJ, et al. Vascular endothelial growth factor receptor-1 promotes migration and invasion in pancreatic carcinoma cell lines. Cancer 2005;104:427-438
61. Yang AD, Camp ER, Fan F, et al. Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells. Cancer Res 2006;66:46-51. (Pubitemid 43166007)
62. Bates RC, Goldsmith JD, Bachelder RE, et al. Flt-1-dependent survival characterizes the epithelial- mesenchymal transition of colonic organoids. Curr Biol 2003;13:1721-1727
63. Maeda K, Chung YS, Ogawa Y, et al. Prognostic value of vascular endothelial growth factor expression in gastric carcinoma. Cancer 1996; 77:858-863 (Pubitemid 26061277)
64. Geretti E, Shimizu A, Kurschat P, Klagsbrun M. Site-directed mutagenesis in the B-neuropilin-2 domain selectivelyenhances its affinity to VEGF165, but not to semaphorin 3F. J Biol Chem 2007;282:25698-25707
65. Narazaki M, Tosato G. Ligand-induced internalization selects use of common receptor neuropilin- 1 by VEGF165 and semaphorin3A. Blood 2006;107:3892-3901
66. Serini G, Napione L, Arese M, Bussolino F. Besides adhesion: new perspectives of integrin functions in angiogenesis. Cardiovasc Res 2008;78:213-222 (Pubitemid 351556107)
67. Catalano A, Caprari P, Moretti S, Faronato M, Tamagnone L, Procopio A. Semaphorin-3A is expressed bytum or cells and alters T-cell signal transduction and function. Blood 2006;107:3321-3329
68. Herman JG, Meadows GG. Transferrin reverses the anti-invasive activityof human prostate cancer cells that overexpress sema3E. Int J Oncol 2007;31:1267-1272
69. Christensen C, Ambartsumian N, Gilestro G, et al. Proteolytic processing converts the repelling signal Sema3E into an inducer of invasive growth and lung metastasis. Cancer Res 2005;65:6167-6177
70. Potiron VA, Sharma G, Nasarre P, et al. Semaphorin SEMA3F affects multiple signaling pathways in lung cancer cells. Cancer Res 2007;67: 8708-8715