Semaphorin 4A exerts a proangiogenic effect by enhancing vascular endothelial growth factor - A expression in macrophages

Journal of Immunology

Volumn 188, Issue 8, 2012, Pages 4081-4092

  Meda, Claudia ^a,b   Molla, Fabiola ^c   De Pizzol, Maria ^d,e   Regano, Donatella ^a,b   Maione, Federica ^a,b   Capano, Stefania ^a,b   Locati, Massimo ^d,e   Mantovani, Alberto ^d,e   Latini, Roberto ^c   Bussolino, Federico ^a,b   Giraudo, Enrico ^a,b  

^a CANDIOLO CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; LIPOPOLYSACCHARIDE; LYSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PLEXIN; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN KINASE B; PROTEIN PLEXINB2; PROTEIN PLEXIND1; SEMAPHORIN; SEMAPHORIN 4A PROTEIN; THIOGLYCOLIC ACID; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; HEART MUSCLE ISCHEMIA; HUMAN; HUMAN CELL; IN VIVO STUDY; MACROPHAGE ACTIVATION; MACROPHAGE MIGRATION; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PERITONITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CHEMOKINES; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE TISSUE PROTEINS; PERITONITIS; REPERFUSION INJURY; SEMAPHORINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84860316750     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101435     Document Type: Article

References (65)

1. Carmeliet, P., and M. Tessier-Lavigne. 2005. Common mechanisms of nerve and blood vessel wiring. Nature 436: 193-200. (Pubitemid 41021263)
2. Kikutani, H., and A. Kumanogoh. 2003. Semaphorins in interactions between T cells and antigen-presenting cells. Nat. Rev. Immunol. 3: 159-167. (Pubitemid 37328693)
3. Serini, G., D. Ambrosi, E. Giraudo, A. Gamba, L. Preziosi, and F. Bussolino. 2003. Modeling the early stages of vascular network assembly. EMBO J. 22: 1771-1779. (Pubitemid 36460134)
4. Chabbert-de Ponnat, I., A. Marie-Cardine, R. J. Pasterkamp, V. Schiavon, L. Tamagnone, N. Thomasset, A. Bensussan, and L. Boumsell. 2005. Soluble CD100 functions on human monocytes and immature dendritic cells require plexin C1 and plexin B1, respectively. Int. Immunol. 17: 439-447. (Pubitemid 40568119)
5. Tamagnone, L., S. Artigiani, H. Chen, Z. He, G. I. Ming, H. Song, A. Chedotal, M. L. Winberg, C. S. Goodman, M. Poo, et al. 1999. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99: 71-80. (Pubitemid 29468631)
6. Rohm, B., A. Ottemeyer, M. Lohrum, and A. W. Püschel. 2000. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 93: 95-104. (Pubitemid 30216499)
7. Dickson, B. J. 2002. Molecular mechanisms of axon guidance. Science 298: 1959-1964. (Pubitemid 35425245)
8. He, Z., and M. Tessier-Lavigne. 1997. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90: 739-751. (Pubitemid 27357965)
9. Huber, A. B., A. L. Kolodkin, D. D. Ginty, and J. F. Cloutier. 2003. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 26: 509-563. (Pubitemid 37064943)
10. de Castro, F., L. Hu, H. Drabkin, C. Sotelo, and A. Chédotal. 1999. Chemoattraction and chemorepulsion of olfactory bulb axons by different secreted semaphorins. J. Neurosci. 19: 4428-4436. (Pubitemid 29241094)
11. Polleux, F., T. Morrow, and A. Ghosh. 2000. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404: 567-573. (Pubitemid 30205047)
12. Kolodkin, A. L., D. J. Matthes, and C. S. Goodman. 1993. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75: 1389-1399.
13. Neufeld, G., and O. Kessler. 2008. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat. Rev. Cancer 8: 632-645.
14. Casazza, A., V. Finisguerra, L. Capparuccia, A. Camperi, J. M. Swiercz, S. Rizzolio, C. Rolny, C. Christensen, A. Bertotti, I. Sarotto, et al. 2010. Sema3E-Plexin D1 signaling drives human cancer cell invasiveness and meta- static spreading in mice. [Published erratum appears in 2011 J. Clin Invest. 121: 2945.]
15. J. Clin. Invest. 120: 2684-2698.
16. Maione, F., F. Molla, C. Meda, R. Latini, L. Zentilin, M. Giacca, G. Seano, G. Serini, F. Bussolino, and E. Giraudo. 2009. Semaphorin 3A is an endogenous angiogenesis inhibitor that blocks tumor growth and normalizes tumor vasculature in transgenic mouse models. J. Clin. Invest. 119: 3356-3372.
17. Basile, J. R., T. Afkhami, and J. S. Gutkind. 2005. Semaphorin 4D/plexin-B1 induces endothelial cell migration through the activation of PYK2, Src, and the phosphatidylinositol 3-kinase-Akt pathway. Mol. Cell. Biol. 25: 6889-6898. (Pubitemid 41105890)
18. Sierra, J. R., S. Corso, L. Caione, V. Cepero, P. Conrotto, A. Cignetti, W. Piacibello, A. Kumanogoh, H. Kikutani, P. M. Comoglio, et al. 2008. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages. J. Exp. Med. 205: 1673-1685. (Pubitemid 351962030)
19. Püschel, A. W., R. H. Adams, and H. Betz. 1995. Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14: 941-948.
20. Kumanogoh, A., S. Marukawa, K. Suzuki, N. Takegahara, C. Watanabe, E. Ch'ng, I. Ishida, H. Fujimura, S. Sakoda, K. Yoshida, and H. Kikutani. 2002. Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2. Nature 419: 629-633.
21. Toyofuku, T., M. Yabuki, J. Kamei, M. Kamei, N. Makino, A. Kumanogoh, and M. Hori. 2007. Semaphorin-4A, an activator for T-cell-mediated immunity, suppresses angiogenesis via Plexin-D1. EMBO J. 26: 1373-1384. (Pubitemid 46398711)
22. Yukawa, K., T. Tanaka, T. Bai, T. Ueyama, K. Owada-Makabe, Y. Tsubota, M. Maeda, K. Suzuki, H. Kikutani, and A. Kumanogoh. 2005. Semaphorin 4A induces growth cone collapse of hippocampal neurons in a Rho/Rho-kinase-dependent manner. Int. J. Mol. Med. 16: 115-118.
23. Yukawa, K., T. Tanaka, K. Yoshida, N. Takeuchi, T. Ito, H. Takamatsu, H. Kikutani, and A. Kumanogoh. 2010. Sema4A induces cell morphological changes through B-type plexin-mediated signaling. Int. J. Mol. Med. 25: 225-230.
24. Kumanogoh, A., T. Shikina, K. Suzuki, S. Uematsu, K. Yukawa, S. Kashiwamura, H. Tsutsui, M. Yamamoto, H. Takamatsu, E. P. Ko-Mitamura, et al. 2005. Non-redundant roles of Sema4A in the immune system: defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. Immunity 22: 305-316. (Pubitemid 40387473)
25. Smith, E. P., K. Shanks, M. M. Lipsky, L. J. DeTolla, A. D. Keegan, and S. P. Chapoval. 2011. Expression of neuroimmune semaphorins 4A and 4D and their receptors in the lung is enhanced by allergen and vascular endothelial growth factor. BMC Immunol. 12: 30.
26. Bing, R. J. 2001. Myocardial ischemia and infarction: growth of ideas. Cardiovasc. Res. 51: 13-20. (Pubitemid 32523050)
27. Frangogiannis, N. G., C. W. Smith, and M. L. Entman. 2002. The inflammatory response in myocardial infarction. Cardiovasc. Res. 53: 31-47. (Pubitemid 34020764)
28. Nian, M., P. Lee, N. Khaper, and P. Liu. 2004. Inflammatory cytokines and postmyocardial infarction remodeling. Circ. Res. 94: 1543-1553. (Pubitemid 38856961)
29. Piper, H. M., K. Meuter, and C. Schäfer. 2003. Cellular mechanisms of ischemia-reperfusion injury. Ann. Thorac. Surg. 75: S644-S648. (Pubitemid 36184543)
30. Bussolino, F., M. F. Di Renzo, M. Ziche, E. Bocchietto, M. Olivero, L. Naldini, G. Gaudino, L. Tamagnone, A. Coffer, and P. M. Comoglio. 1992. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J. Cell Biol. 119: 629-641.
31. Valdembri, D., P. T. Caswell, K. I. Anderson, J. P. Schwarz, I. König, E. Astanina, F. Caccavari, J. C. Norman, M. J. Humphries, F. Bussolino, and G. Serini. 2009. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol. 7: e25.
32. Naldini, A., D. Leali, A. Pucci, E. Morena, F. Carraro, B. Nico, D. Ribatti, and M. Presta. 2006. Cutting edge: IL-1beta mediates the proangiogenic activity of osteopontin-activated human monocytes. J. Immunol. 177: 4267-4270. (Pubitemid 44469753)
33. Tsou, C. L., W. Peters, Y. Si, S. Slaymaker, A. M. Aslanian, S. P. Weisberg, M. Mack, and I. F. Charo. 2007. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117: 902-909. (Pubitemid 46556746)
34. Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274: 10689-10692.
35. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91: 295-298. (Pubitemid 27467959)
36. Gu, C., Y. Yoshida, J. Livet, D. V. Reimert, F. Mann, J. Merte, C. E. Henderson, T. M. Jessell, A. L. Kolodkin, and D. D. Ginty. 2005. Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307: 265-268. (Pubitemid 40116243)
37. Geissmann, F., C. Auffray, R. Palframan, C. Wirrig, A. Ciocca, L. Campisi, E. Narni-Mancinelli, and G. Lauvau. 2008. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol. Cell Biol. 86: 398-408. (Pubitemid 351948210)
38. Fong, G. H. 2009. Regulation of angiogenesis by oxygen sensing mechanisms. J. Mol. Med. 87: 549-560.
39. Ahmed, Z., and R. Bicknell. 2009. Angiogenic signalling pathways. Methods Mol. Biol. 467: 3-24.
40. Harmey, J. H., E. Dimitriadis, E. Kay, H. P. Redmond, and D. Bouchier-Hayes. 1998. Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor beta-1. Ann. Surg. Oncol. 5: 271-278. (Pubitemid 28249320)
41. Botero, T. M., M. G. Mantellini, W. Song, C. T. Hanks, and J. E. Nör. 2003. Effect of lipopolysaccharides on vascular endothelial growth factor expression in mouse pulp cells and macrophages. Eur. J. Oral Sci. 111: 228-234. (Pubitemid 37465514)
42. Burke, B., A. Giannoudis, K. P. Corke, D. Gill, M. Wells, L. Ziegler-Heitbrock, and C. E. Lewis. 2003. Hypoxia-induced gene expression in human macro-phages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am. J. Pathol. 163: 1233-1243. (Pubitemid 37175073)
43. Barleon, B., S. Sozzani, D. Zhou, H. A. Weich, A. Mantovani, and D. Marmé. 1996. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 87: 3336-3343. (Pubitemid 26115364)
44. Murakami, M., Y. Zheng, M. Hirashima, T. Suda, Y. Morita, J. Ooehara, H. Ema, G. H. Fong, and M. Shibuya. 2008. VEGFR1 tyrosine kinase signaling promotes lymphangiogenesis as well as angiogenesis indirectly via macrophage recruitment. Arterioscler. Thromb. Vasc. Biol. 28: 658-664. (Pubitemid 351651323)
45. Yang, Z. F., R. T. Poon, Y. Luo, C. K. Cheung, D. W. Ho, C. M. Lo, and S. T. Fan. 2004. Up-regulation of vascular endothelial growth factor (VEGF) in small-for-size liver grafts enhances macrophage activities through VEGF receptor 2-dependent pathway. J. Immunol. 173: 2507-2515. (Pubitemid 39063109)
46. Kigel, B., A. Varshavsky, O. Kessler, and G. Neufeld. 2008. Successful inhibition of tumor development by specific class-3 semaphorins is associated with expression of appropriate semaphorin receptors by tumor cells. PLoS ONE 3: e3287.
47. Rolny, C., L. Capparuccia, A. Casazza, M. Mazzone, A. Vallario, A. Cignetti, E. Medico, P. Carmeliet, P. M. Comoglio, and L. Tamagnone. 2008. The tumor suppressor semaphorin 3B triggers a prometastatic program mediated by interleukin 8 and the tumor microenvironment. J. Exp. Med. 205: 1155-1171. (Pubitemid 351679690)
48. Ramachandran, A., S. Jha, and D. J. Lefer. 2008. REVIEW paper: pathophysiology of myocardial reperfusion injury: the role of genetically engineered mouse models. Vet. Pathol. 45: 698-706.
49. Salogni, L., T. Musso, D. Bosisio, M. Mirolo, V. R. Jala, B. Haribabu, M. Locati, and S. Sozzani. 2009. Activin A induces dendritic cell migration through the polarized release of CXC chemokine ligands 12 and 14. Blood 113: 5848-5856.
50. Murakami, M., S. Iwai, S. Hiratsuka, M. Yamauchi, K. Nakamura, Y. Iwakura, and M. Shibuya. 2006. Signaling of vascular endothelial growth factor receptor-1 tyrosine kinase promotes rheumatoid arthritis through activation of monocytes/macrophages. Blood 108: 1849-1856. (Pubitemid 44394993)
51. Mitola, S., S. Sozzani, W. Luini, L. Primo, A. Borsatti, H. Weich, and F. Bussolino. 1997. Tat-human immunodeficiency virus-1 induces human monocyte chemotaxis by activation of vascular endothelial growth factor receptor-1. Blood 90: 1365-1372. (Pubitemid 27355407)
52. Mantovani, A., A. Sica, and M. Locati. 2007. New vistas on macrophage differentiation and activation. Eur. J. Immunol. 37: 14-16. (Pubitemid 46128780)
53. Mantovani, A., A. Sica, P. Allavena, C. Garlanda, and M. Locati. 2009. Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. Hum. Immunol. 70: 325-330.
54. Coussens, L. M., C. L. Tinkle, D. Hanahan, and Z. Werb. 2000. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103: 481-490.
55. Giraudo, E., M. Inoue, and D. Hanahan. 2004. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J. Clin. Invest. 114: 623-633. (Pubitemid 39578752)
56. Koch, A. E., P. J. Polverini, S. L. Kunkel, L. A. Harlow, L. A. DiPietro, V. M. Elner, S. G. Elner, and R. M. Strieter. 1992. Interleukin-8 as a macro-phage-derived mediator of angiogenesis. Science 258: 1798-1801.
57. Imtiyaz, H. Z., and M. C. Simon. 2010. Hypoxia-inducible factors as essential regulators of inflammation. Curr. Top. Microbiol. Immunol. 345: 105-120.
58. Kiriakidis, S., E. Andreakos, C. Monaco, B. Foxwell, M. Feldmann, and E. Paleolog. 2003. VEGF expression in human macrophages is NF-kappaB-dependent: studies using adenoviruses expressing the endogenous NF-kappaB inhibitor IkappaBalpha and a kinase-defective form of the IkappaB kinase 2. J. Cell Sci. 116: 665-674. (Pubitemid 36231305)
59. Jeon, S. H., B. C. Chae, H. A. Kim, G. Y. Seo, D. W. Seo, G. T. Chun, N. S. Kim, S. W. Yie, W. H. Byeon, S. H. Eom, et al. 2007. Mechanisms underlying TGF-beta1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis. J. Leukoc. Biol. 81: 557-566.
60. Primo, L., L. di Blasio, C. Roca, S. Droetto, R. Piva, B. Schaffhausen, and F. Bussolino. 2007. Essential role of PDK1 in regulating endothelial cell migration. J. Cell Biol. 176: 1035-1047. (Pubitemid 46506975)
61. Jiang, B. H., and L. Z. Liu. 2009. PI3K/PTEN signaling in angiogenesis and tumorigenesis. Adv. Cancer Res. 102: 19-65.
62. Koch, S., S. Tugues, X. Li, L. Gualandi, and L. Claesson-Welsh. 2011. Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 437: 169-183.
63. Phung, T. L., K. Ziv, D. Dabydeen, G. Eyiah-Mensah, M. Riveros, C. Perruzzi, J. Sun, R. A. Monahan-Earley, I. Shiojima, J. A. Nagy, et al. 2006. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10: 159-170. (Pubitemid 44175906)
64. Dhanabal, M., F. Wu, E. Alvarez, K. D. McQueeney, M. Jeffers, J. MacDougall, F. L. Boldog, C. Hackett, S. Shenoy, N. Khramtsov, et al. 2005. Recombinant semaphorin 6A-1 ectodomain inhibits in vivo growth factor and tumor cell line-induced angiogenesis. Cancer Biol. Ther. 4: 659-668. (Pubitemid 41351204)
65. Suzuki, K., T. Okuno, M. Yamamoto, R. J. Pasterkamp, N. Takegahara, H. Takamatsu, T. Kitao, J. Takagi, P. D. Rennert, A. L. Kolodkin, et al. 2007. Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin. Nature 446: 680-684. (Pubitemid 46606878)