Successful inhibition of tumor development by specific class-3 semaphorins is associated with expression of appropriate semaphorin receptors by tumor cells

PLoS ONE

Volumn 3, Issue 9, 2008, Pages

  Kigel, Boaz ^a   Varshavsky, Asya ^a   Kessler, Ofra ^a   Neufeld, Gera ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; FIBRONECTIN; LENTIVIRUS VECTOR; RECEPTOR PROTEIN; RECOMBINANT PROTEIN; SEMAPHORIN; SEMAPHORIN 3A; SEMAPHORIN 3D; SEMAPHORIN 3E; SEMAPHORIN 3G; SEMAPHORIN RECEPTOR; UNCLASSIFIED DRUG; ANGIOGENESIS INHIBITOR; NEUROPILIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GENE THERAPY; CANCER INHIBITION; CELL ADHESION; CELL PROLIFERATION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; DRUG RESEARCH; FEMALE; HUMAN; HUMAN CELL; MALIGNANT NEOPLASTIC DISEASE; MONOTHERAPY; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR VASCULARIZATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL ADHESION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; MODELS, GENETIC; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEUROPILIN-1; SEMAPHORINS;

EID: 53749086983     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003287     Document Type: Article

References (47)

1. Neufeld G, Cohen T, Shraga N, Lange T, Kessler O, et al. (2002) The neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis. Trends Cardiovasc Med 12: 13-19.
2. Neufeld G, Kessler O (2008) The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat Rev Cancer 8: 632-645.
3. Gitay-Goren H, Cohen T, Tessler S, Soker S, Gengrinovitch S, et al. (1996) Selective binding of VEGF121 to one of the three VEGF receptors of vascular endothelial cells. J Biol Chem 271: 5519-5523.
4. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform specific receptor for vascular endothelial growth factor. Cell 92: 735-745.
5. Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G (2000) 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: 18040-18045.
6. Sulpice E, Plouet J, Berge M, Allanic D, Tobelem G, et al. (2007) Neuropilin-1 and neuropilin-2 act as coreceptors, potentiating proangiogenic activity. Blood 111: 2036-2045.
7. Pan Q, Chanthery Y, Liang WC, Stawicki S, Mak J, et al. (2007) Blocking Neuropilin-1 Function Has an Additive Effect with Anti-VEGF to Inhibit Tumor Growth. Cancer Cell 11: 53-67.
8. Caunt M, Mak J, Liang WC, Stawicki S, Pan Q, et al. (2008) Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 13: 331-342.
9. Gu C, Yoshida Y, Livet J, Reimert DV, Mann F, et al. (2005) Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307: 265-268.
10. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, et al. (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99: 59-69.
11. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, et al. (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99: 71-80.
12. Kolodkin AL (1996) Semaphorins: mediators of repulsive growth cone guidance. Trends Cell Biol 6: 15-22.
13. Tomizawa Y, Sekido Y, Kondo M, Gao B, Yokota J, et al. (2001) 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: 13954-13959.
14. Xiang R, Davalos AR, Hensel CH, Zhou XJ, Tse C, et al. (2002) Semaphorin 3F Gene from Human 3p21.3 Suppresses Tumor Formation in Nude Mice. Cancer Res 62: 2637-2643.
15. Kessler O, Shraga-Heled N, Lange T, Gutmann-Raviv N, Sabo E, et al. (2004) Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res 64: 1008-1015.
16. Bielenberg DR, Hida Y, Shimizu A, Kaipainen A, Kreuter M, et al. (2004) Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype. J Clin Invest 114: 1260-1271.
17. Acevedo LM, Barillas S, Weis SM, Gothert JR, Cheresh DA (2008) Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 111: 2674-2680.
18. Nasarre P, Kusy S, Constantin B, Castellani V, Drabkin HA, et al. (2005) Semaphorin SEMA3F has a repulsing activity on breast cancer cells and inhibits E-cadherin-mediated cell adhesion. Neoplasia 7: 180-189.
19. Guttmann-Raviv N, Shraga-Heled N, Varshavsky A, Guimaraes-Sternberg C, Kessler O, et al. (2007) Semaphorin-3A and Semaphorin-3F Work Together to Repel Endothelial Cells and to Inhibit Their Survival by Induction of Apoptosis. J Biol Chem 282: 26294-26305.
20. Akiri G, Sabo E, Dafni H, Vadasz Z, Kartvelishvily Y, et al. (2003) Lysyl Oxidase-related Protein-1 Promotes Tumor Fibrosis and Tumor Progression in Vivo. Cancer Res 63: 1657-1666.
21. Vermeulen PB, Gasparini G, Fox SB, Toi M, Martin L, et al. (1996) Quantification of angiogenesis in solid human tumours: an international consensus on the methodology and criteria of evaluation. Eur J Cancer 32A: 2474-2484.
22. Vamesu S (2007) Angiogenesis and ER/PR status in primary breast cancer patients: an analysis of 158 needle core biopsies. Rom J Morphol Embryol 48: 25-31.
23. Adams RH, Lohrum M, Klostermann A, Betz H, Puschel AW (1997) The chemorepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing. EMBO J 16: 6077-6086.
24. Christensen C, Ambartsumian N, Gilestro G, Thomsen B, Comoglio P, et al. (2005) Proteolytic Processing Converts the Repelling Signal Sema3E into an Inducer of Invasive Growth and Lung Metastasis. Cancer Res 65: 6167-6177.
25. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RI, et al. (1997) Neuropilin is a semaphorin III receptor. Cell 90: 753-762.
26. Wolman MA, Liu Y, Tawarayama H, Shoji W, Halloran MC (2004) Repulsion and attraction of axons by Semaphorin3D are mediated by different neuropilins in vivo. J Neurosci 24: 8428-8435.
27. Yu HH, Moens CB (2005) Semaphorin signaling guides cranial neural crest cell migration in zebrafish. Dev Biol 280: 373-385.
28. Futamura M, Kamino H, Miyamoto Y, Kitamura N, Nakamura Y, et al. (2007) Possible Role of Semaphorin 3F, a Candidate Tumor Suppressor Gene at 3p21.3, in p53-Regulated Tumor Angiogenesis Suppression. Cancer Res 67: 1451-1460.
29. Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, et al. (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424: 391-397.
30. Bates D, Taylor GI, Minichiello J, Farlie P, Cichowitz A, et al. (2003) Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev Biol 255: 77-98.
31. Pavelock K, Braas KM, Ouafik L, Osol G, May V (2001) Differential Expression and Regulation of the Vascular Endothelial Growth Factor Receptors Neuropilin-1 and Neuropilin-2 in Rat Uterus. Endocrinology 142: 613-622.
32. Hamburger AW (1987) The human tumor clonogenic assay as a model system in cell biology. Int J Cell Cloning 5: 89-107.
33. Cifone MA (1982) In vitro growth characteristics associated with benign and metastatic variants of tumor cells. Cancer Metastasis Rev 1: 335-347.
34. Brummelkamp TR, Bernards R, Agami R (2002) Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2: 243-247.
35. Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M (1997) 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: 547-559.
36. Nasarre P, Constantin B, Rouhaud L, Harnois T, Raymond G, et al. (2003) Semaphorin SEMA3F and VEGF Have Opposing Effects on Cell Attachment and Spreading. Neoplasia 5: 83-92.
37. Taniguchi M, Masuda T, Fukaya M, Kataoka H, Mishina M, et al. (2005) Identification and characterization of a novel member of murine semaphorin family. Genes Cells 10: 785-792.
38. Tse C, Xiang RH, Bracht T, Naylor SL (2002) Human Semaphorin 3B (SEMA3B) Located at Chromosome 3p21.3 Suppresses Tumor Formation in an Adenocarcinoma Cell Line. Cancer Res 62: 542-546.
39. Acevedo LM, Weis SM, Cheresh DA (2008) Robo4 counteracts VEGF signaling. Nat Med 14: 372-373.
40. Ellis LM (2006) The role of neuropilins in cancer. Mol Cancer Ther 5: 1099-1107.
41. Zacchigna S, Pattarini L, Zentilin L, Moimas S, Carrer A, et al. (2008) Bone marrow cells recruited through the neuropilin-1 receptor promote arterial formation at the sites of adult neoangiogenesis in mice. J Clin Invest 118: 2062-2075.
42. Whitehurst B, Flister MJ, Bagaitkar J, Volk L, Bivens CM, et al. (2007) Anti-VEGF-A therapy reduces lymphatic vessel density and expression of VEGFR-3 in an orthotopic breast tumor model. Int J Cancer 121: 2181-2191.
43. Zhang W, Ran S, Sambade M, Huang X, Thorpe PE (2002) A monoclonal antibody that blocks VEGF binding to VEGFR2 (KDR/Flk-1) inhibits vascular expression of Flk-1 and tumor growth in an orthotopic human breast cancer model. Angiogenesis 5: 35-44.
44. Herman JG, Meadows GG (2007) Increased class 3 semaphorin expression modulates the invasive and adhesive properties of prostate cancer cells. Int J Oncol 30: 1231-1238.
45. Soker S, Miao HQ, Nomi M, Takashima S, Klagsbrun M (2002) VEGF(165) mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF(165)-receptor binding. J Cell Biochem 85: 357-368.
46. Bassi DE, Fu J, Lopez de CR, Klein-Szanto AJ (2005) Proprotein convertases: "master switches" in the regulation of tumor growth and progression. Mol Carcinog 44: 151-161.
47. Varshavsky A, Kessler O, Abramovitch S, Kigel B, Zaffryar S, et al. (2008) Semaphorin-3B Is an Angiogenesis Inhibitor That Is Inactivated by Furin-Like Pro-Protein Convertases. Cancer Res 68: 6922-6931.