Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype

Journal of Clinical Investigation

Volumn 114, Issue 9, 2004, Pages 1260-1271

  Bielenberg, Diane R ^a   Hida, Yasuhiro ^a   Shimizu, Akio ^a   Kaipainen, Arja ^a   Kreuter, Michael ^b   Kim, Caroline Choi ^a   Klagsbrun, Michael ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMETASTATIC AGENT; CHEMOREPELLENT; COLLAGEN; FIBRONECTIN; NEUROPILIN 2; SEMAPHORIN; SEMAPHORIN 3F; UNCLASSIFIED DRUG; CD31 ANTIGEN; MEMBRANE PROTEIN; NERVE PROTEIN; SEMA3F PROTEIN, HUMAN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EPIDERMIS CELL; FIBROBLAST; GENE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LYMPH VESSEL ENDOTHELIUM; MALE; MELANOMA; METASTASIS; METASTASIS INHIBITION; MOUSE; NERVE CELL INHIBITION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SEMA3F GENE; STROMA CELL; TUMOR CELL; VASCULARIZATION; ANIMAL; BIOSYNTHESIS; CELL ADHESION; CELL MOTION; CELL PROLIFERATION; DOSE RESPONSE; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUNG; LYMPH NODE METASTASIS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NICK END LABELING; NORTHERN BLOTTING; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD31; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COLLAGEN; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; LUNG; LYMPHATIC METASTASIS; MALE; MEMBRANE PROTEINS; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; NERVE TISSUE PROTEINS; NEUROPILIN-2; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION;

EID: 85047693077     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI21378     Document Type: Article

References (62)

1. Kolodkin, A.L., et al. 1997. Neuropilin is a semaphorin III receptor. Cell. 90:753-762.
2. Soker, S., Takashima, S., Miao, H.Q., Neufeld, G., and 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.
3. Gagnon, M.L., et al. 2000. 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. 97:2573-2578.
4. Harper, J., Gerstenfeld, L.C., and Klagsbrun, M. 2001. Neuropilin-1 expression in osteogenic cells: down-regulation during differentiation of osteoblasts into osteocytes. J. Cell. Biochem. 81:82-92.
5. Chen, H., Chedotal, A., He, Z., Goodman, C.S., and 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.
6. Rossignol, M., Beggs, A.H., Pierce, E.A., and Klagsbrun, M. 1999. Human neuropilin-1 and neuropilin-2 map to 10p12 and 2q34, respectively. Genomics. 57:459-460.
7. Herzog, Y., Kalcheim, C., Kahane, N., Reshef, R., and Neufeld, G. 2001. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech. Dev. 109:115-119.
8. Yuan, L., et al. 2002. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development. 129:4797-4806.
9. Chen, H., He, Z., Bagri, A., and Tessier-Lavigne, M. 1998. Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron. 21:1283-1290.
10. Chedotal, A., et al. 1998. Semaphorins III and IV repel hippocampal axons via two distinct receptors. Development. 125:4313-4323.
11. He, Z., and Tessier-Lavigne, M. 1997. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell. 90:739-751.
12. Giger, R.J., et al. 1998. Neuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity. Neuron. 21:1079-1092.
13. Klagsbrun, M., Takashima, S., and Mamluk, R. 2002. The role of neuropilin in vascular and tumor biology. Adv. Exp. Med. Biol. 515:33-48.
14. Takahashi, T., et al. 1999. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell. 99:59-69.
15. Soker, S., Miao, H.Q., Nomi, M., Takashima, S., and Klagsbrun, M. 2002. VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J. Cell. Biochem. 85:357-368.
16. Kitsukawa, T., et al. 1997. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 19:995-1005.
17. Takashima, S., et al. 2002. 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. 99:3657-3662.
18. Lee, P., et al. 2002. Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish. Proc. Natl. Acad. Sci. U. S. A. 99:10470-10475.
19. Miao, H.Q., Lee, P., Lin, H., Soker, S., and Klagsbrun, M. 2000. Neuropilin-1 expression by tumor cells promotes tumor angiogenesis and progression. FASEB J. 14:2532-2539.
20. Parikh, A.A., et al. 2004. Neuropilin-1 in human colon cancer: expression, regulation, and role in induction of angiogenesis. Am. J. Pathol. 164:2139-2151.
21. Miao, H.Q., et al. 1999. 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. 146:233-242.
22. Serini, G., et al. 2003. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature. 424:391-397.
23. Bates, D., et al. 2003. Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev. Biol. 255:77-98.
24. Kessler, O., et al. 2004. Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res. 64:1008-1015.
25. Sekido, Y., et al. 1996. 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. 93:4120-4125.
26. Roche, J., et al. 1996. Distinct 3p21.3 deletions in lung cancer and identification of a new human semaphorin. Oncogene. 12:1289-1297.
27. Tomizawa, Y., 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.
28. Tse, C., Xiang, R.H., Bracht, T., and Naylor, S.L. 2002. Human Semaphorin 3B (SEMA3B) located at chromosome 3p21.3 suppresses tumor formation in an adenocarcinoma cell line. Cancer Res. 62:542-546.
29. Xiang, R., et al. 2002. Semaphorin 3F gene from human 3p21.3 suppresses tumor formation in nude mice. Cancer Res. 62:2637-2643.
30. McCarty, M.F., Bielenberg, D., Donawho, C., Bucana, C.D., and Fidler, I.J. 2002. Evidence for the causal role of endogenous interferon-alpha/beta in the regulation of angiogenesis, tumorigenicity, and metastasis of cutaneous neoplasms. Clin. Exp. Metastasis. 19:609-615.
31. Fidler, I.J. 1996. Critical determinants of melanoma metastasis. J. Investig. Dermatol. Symp. Proc. 1:203-208.
32. Detmar, M., and Hirakawa, S. 2002. The formation of lymphatic vessels and its importance in the setting of malignancy. J. Exp. Med. 196:713-718.
33. Hong, Y.K., et al. 2002. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn. 225:351-357.
34. Xiang, R.H., et al. 1996. Isolation of the human semaphorin III/F gene (SEMA3F) at chromosome 3p21, a region deleted in lung cancer. Genomics. 32:39-48.
35. Clarkson, K.S., Sturdgess, I.C., and Molyneux, A.J. 2001. The usefulness of tyrosinase in the immunohistochemical assessment of melanocytic lesions: a comparison of the novel T311 antibody (anti-tyrosinase) with S-100, HMB45, and A103 (anti-melan-A). J. Clin. Pathol. 54:196-200.
36. Fidler, I.J. 1990. Critical factors in the biology of human cancer metastasis: twenty-eighth G.H.A. Clowes memorial award lecture. Cancer Res. 50:6130-6138.
37. Nasarre, P., et al. 2003. Semaphorin SEMA3F and VEGF have opposing effects on cell attachment and spreading. Neoplasia. 5:83-92.
38. Jin, H., and Varner, J. 2004. Integrins: roles in cancer development and as treatment targets. Br. J. Cancer. 90:561-565.
39. McCarty, M.F., et al. 2003. Epidermal hyperplasia overlying human melanoma correlates with tumour depth and angiogenesis. Melanoma Res. 13:379-387.
40. Bielenberg, D.R., et al. 1998. Molecular regulation of UVB-induced cutaneous angiogenesis. J. Invest. Dermatol. 111:864-872.
41. Hasan, J., Byers, R., and Jayson, G.C. 2002. Intratumoural microvessel density in human solid tumours. Br. J. Cancer. 86:1566-1577.
42. Srivastava, A., Laidler, P., Davies, R.P., Horgan, K., and Hughes, L.E. 1988. The prognostic significance of tumor vascularity in intermediate-thickness (0.76-4.0 mm thick) skin melanoma. A quantitative histologic study. Am. J. Pathol. 133:419-423.
43. Ferrara, N., Gerber, H.P., and LeCouter, J. 2003. The biology of VEGF and its receptors. Nat. Med. 9:669-676.
44. Rehn, M., et al. 2001. Interaction of endostatin with integrins implicated in angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 98:1024-1029.
45. Kim, Y.M., et al. 2000. Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase. Cancer Res. 60:5410-5413.
46. Dhanabal, M., et al. 1999. Endostatin induces endothelial cell apoptosis. J. Biol. Chem. 274:11721-11726.
47. Kusy, S., et al. 2003. Redundant functions but temporal and regional regulation of two alternatively spliced isoforms of Semaphorin 3F in the nervous system. Mol. Cell. Neurosci. 24:409-418.
48. Stacker, S.A., Achen, M.G., Jussila, L., Baldwin, M.E., and Alitalo, K. 2002. Lymphangiogenesis and cancer metastasis. Nat. Rev. Cancer. 2:573-583.
49. Dadras, S.S., et al. 2003. Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am. J. Pathol. 162:1951-1960.
50. Rohm, B., Ottemeyer, A., Lohrum, M., and Puschel, A.W. 2000. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 93:95-104.
51. Zanata, S.M., Hovatta, I., Rohm, B., and Puschel, A.W. 2002. Antagonistic effects of Rnd1 and RhoD GTPases regulate receptor activity in Semaphorin 3A-induced cytoskeletal collapse. J. Neurosci. 22:471-477.
52. Mitsui, N., et al. 2002. Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J. 21:3274-3285.
53. Shih, J.Y., et al. 2001. Collapsin response mediator protein-1 and the invasion and metastasis of cancer cells. J. Natl. Cancer Inst. 93:1392-1400.
54. Kozlowski, J.M., Hart, I.R., Fidler, I.J., and Hanna, N. 1984. A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J. Natl. Cancer Inst. 72:913-917.
55. Dinney, C.P., et al. 1995. Isolation and characterization of metastatic variants from human transitional cell carcinoma passaged by orthotopic implantation in athymic nude mice. J. Urol. 154:1532-1538.
56. Pettaway, C.A., et al. 1996. Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin. Cancer Res. 2:1627-1636.
57. Isaacs, J.T., Isaacs, W.B., Feitz, W.F., and Scheres, J. 1986. Establishment and characterization of seven Dunning rat prostatic cancer cell lines and their use in developing methods for predicting metastatic abilities of prostatic cancers. Prostate. 9:261-281.
58. Jussila, L., et al. 1998. Lymphatic endothelium and Kaposi's sarcoma spindle cells detected by antibodies against the vascular endothelial growth factor receptor-3. Cancer Res. 58:1599-1604.
59. Cornil, I., Man, S., Fernandez, B., and Kerbel, R. 1989. Enhanced tumorigenicity, melanogenesis, and metastases of a human malignant melanoma after implantation in nude mice. J. Natl. Cancer Inst. 81:938-944.
60. Komminoth, P. 2002. Detection of mRNA in tissue sections using DIG-labeled RNA and oligonucleotide probes. In Nonradioactive in situ hybridization application manual. D. Eisel, S. Grunewald-Janho, and B. Kruchen, editors. Roche Applied Science. Indianapolis, Indiana, USA. 149-163.
61. Dong, Z., et al. 1999. Suppression of angiogenesis, tumorigenicity, and metastasis by human prostate cancer cells engineered to produce interferon-beta. Cancer Res. 59:872-879.
62. Soker, S., Gollamudi-Payne, S., Fidder, H., Charmahelli, H., and Klagsbrun, M. 1997. 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. 272:31582-31588.