Impeding Macrophage Entry into Hypoxic Tumor Areas by Sema3A/Nrp1 Signaling Blockade Inhibits Angiogenesis and Restores Antitumor Immunity

Cancer Cell

Volumn 24, Issue 6, 2013, Pages 695-709

  Casazza, Andrea ^a,b   Laoui, Damya ^a,c   Wenes, Mathias ^a,b   Rizzolio, Sabrina ^d   Bassani, Nicklas ^a,b   Mambretti, Marco ^a,b   Deschoemaeker, Sofie ^a,b   VanGinderachter, JoA ^a,c   Tamagnone, Luca ^d   Mazzone, Massimiliano ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPILIN 1; SEMAPHORIN 3A; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE DELETION; HUMAN; HUMAN CELL; HYPOXEMIA; MACROPHAGE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY;

EID: 84891930215     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.11.007     Document Type: Article

References (54)

1. Bellon A., Luchino J., Haigh K., Rougon G., Haigh J., Chauvet S., Mann F. VEGFR2 (KDR/Flk1) signaling mediates axon growth in response to semaphorin 3E in the developing brain. Neuron 2010, 66:205-219.
2. Biankin A.V., Waddell N., Kassahn K.S., Gingras M.C., Muthuswamy L.B., Johns A.L., Miller D.K., Wilson P.J., Patch A.M., Wu J., et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012, 491:399-405. Australian Pancreatic Cancer Genome Initiative.
3. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
4. Blouw B., Song H., Tihan T., Bosze J., Ferrara N., Gerber H.P., Johnson R.S., Bergers G. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 2003, 4:133-146.
5. Bruder D., Probst-Kepper M., Westendorf A.M., Geffers R., Beissert S., Loser K., von Boehmer H., Buer J., Hansen W. Neuropilin-1: a surface marker of regulatory Tcells. Eur. J. Immunol. 2004, 34:623-630.
6. Burke B., Giannoudis A., Corke K.P., Gill D., Wells M., Ziegler-Heitbrock L., Lewis C.E. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am. J. Pathol. 2003, 163:1233-1243.
7. Casazza A., Fu X., Johansson I., Capparuccia L., Andersson F., Giustacchini A., Squadrito M.L., Venneri M.A., Mazzone M., Larsson E., et al. Systemic and targeted delivery of semaphorin 3A inhibits tumor angiogenesis and progression in mouse tumor models. Arterioscler. Thromb. Vasc. Biol. 2011, 31:741-749.
8. Catalano A. The neuroimmune semaphorin-3A reduces inflammation and progression of experimental autoimmune arthritis. J.Immunol. 2010, 185:6373-6383.
9. Catalano A., Caprari P., Moretti S., Faronato M., Tamagnone L., Procopio A. Semaphorin-3A is expressed by tumor cells and alters T-cell signal transduction and function. Blood 2006, 107:3321-3329.
10. Coussens L.M., Zitvogel L., Palucka A.K. Neutralizing tumor-promoting chronic inflammation: a magic bullet?. Science 2013, 339:286-291.
11. De Palma M., Lewis C.E. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 2013, 23:277-286.
12. de Wit J., Verhaagen J. Proteoglycans as modulators of axon guidance cue function. Adv. Exp. Med. Biol. 2007, 600:73-89.
13. De Wit J., De Winter F., Klooster J., Verhaagen J. Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol. Cell. Neurosci. 2005, 29:40-55.
14. Delgoffe G.M., Woo S.R., Turnis M.E., Gravano D.M., Guy C., Overacre A.E., Bettini M.L., Vogel P., Finkelstein D., Bonnevier J., et al. Stability and function of regulatory Tcells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 2013, 501:252-256.
15. Doedens A.L., Stockmann C., Rubinstein M.P., Liao D., Zhang N., DeNardo D.G., Coussens L.M., Karin M., Goldrath A.W., Johnson R.S. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 2010, 70:7465-7475.
16. Eltzschig H.K., Carmeliet P. Hypoxia and inflammation. N.Engl. J. Med. 2011, 364:656-665.
17. Fantin A., Vieira J.M., Gestri G., Denti L., Schwarz Q., Prykhozhij S., Peri F., Wilson S.W., Ruhrberg C. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010, 116:829-840.
18. Fantin A., Vieira J.M., Plein A., Denti L., Fruttiger M., Pollard J.W., Ruhrberg C. NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 2013, 121:2352-2362.
19. Fuster M.M., Esko J.D. The sweet and sour of cancer: glycans as novel therapeutic targets. Nat. Rev. Cancer 2005, 5:526-542.
20. Gerhardt H., Ruhrberg C., Abramsson A., Fujisawa H., Shima D., Betsholtz C. Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev. Dyn. 2004, 231:503-509.
21. Gu C., Rodriguez E.R., Reimert D.V., Shu T., Fritzsch B., Richards L.J., Kolodkin A.L., Ginty D.D. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 2003, 5:45-57.
22. Guthrie S. Axon guidance: starting and stopping with slit. Curr. Biol. 1999, 9:R432-R435.
23. + regulatory Tcells impairs mouse melanoma growth. J.Exp. Med. 2012, 209:2001-2016.
24. Hayashi M., Nakashima T., Taniguchi M., Kodama T., Kumanogoh A., Takayanagi H. Osteoprotection by semaphorin 3A. Nature 2012, 485:69-74.
25. Hong T.M., Chen Y.L., Wu Y.Y., Yuan A., Chao Y.C., Chung Y.C., Wu M.H., Yang S.C., Pan S.H., Shih J.Y., et al. Targeting neuropilin 1 as an antitumor strategy in lung cancer. Clin. Cancer Res. 2007, 13:4759-4768.
26. Janssen B.J., Malinauskas T., Weir G.A., Cader M.Z., Siebold C., Jones E.Y. Neuropilins lock secreted semaphorins onto plexins in a ternary signaling complex. Nat. Struct. Mol. Biol. 2012, 19:1293-1299.
27. Johansson M., Denardo D.G., Coussens L.M. Polarized immune responses differentially regulate cancer development. Immunol. Rev. 2008, 222:145-154.
28. Kolodkin A.L., Levengood D.V., Rowe E.G., Tai Y.T., Giger R.J., Ginty D.D. Neuropilin is a semaphorin III receptor. Cell 1997, 90:753-762.
29. Liang W.C., Dennis M.S., Stawicki S., Chanthery Y., Pan Q., Chen Y., Eigenbrot C., Yin J., Koch A.W., Wu X., et al. Function blocking antibodies to neuropilin-1 generated from a designed human synthetic antibody phage library. J.Mol. Biol. 2007, 366:815-829.
30. Lin E.Y., Jones J.G., Li P., Zhu L., Whitney K.D., Muller W.J., Pollard J.W. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 2003, 163:2113-2126.
31. Maione F., Molla F., Meda C., Latini R., Zentilin L., Giacca M., Seano G., Serini G., Bussolino F., Giraudo E. Semaphorin 3A is an endogenous angiogenesis inhibitor that blocks tumor growth and normalizes tumor vasculature in transgenic mouse models. J.Clin. Invest. 2009, 119:3356-3372.
32. Maione F., Capano S., Regano D., Zentilin L., Giacca M., Casanovas O., Bussolino F., Serini G., Giraudo E. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J.Clin. Invest. 2012, 122:1832-1848.
33. Mazzone M., Dettori D., Leite de Oliveira R., Loges S., Schmidt T., Jonckx B., Tian Y.M., Lanahan A.A., Pollard P., Ruiz de Almodovar C., et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009, 136:839-851.
34. Movahedi K., Laoui D., Gysemans C., Baeten M., Stangé G., Van den Bossche J., Mack M., Pipeleers D., In't Veld P., De Baetselier P., Van Ginderachter J.A. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010, 70:5728-5739.
35. Müller M.W., Giese N.A., Swiercz J.M., Ceyhan G.O., Esposito I., Hinz U., Büchler P., Giese T., Büchler M.W., Offermanns S., Friess H. Association of axon guidance factor semaphorin 3A with poor outcome in pancreatic cancer. Int. J. Cancer 2007, 121:2421-2433.
36. Murdoch C., Lewis C.E. Macrophage migration and gene expression in response to tumor hypoxia. Int. J. Cancer 2005, 117:701-708.
37. Nawabi H., Briançon-Marjollet A., Clark C., Sanyas I., Takamatsu H., Okuno T., Kumanogoh A., Bozon M., Takeshima K., Yoshida Y., et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 2010, 24:396-410.
38. Niedergethmann M., Hildenbrand R., Wostbrock B., Hartel M., Sturm J.W., Richter A., Post S. High expression of vascular endothelial growth factor predicts early recurrence and poor prognosis after curative resection for ductal adenocarcinoma of the pancreas. Pancreas 2002, 25:122-129.
39. Nogi T., Yasui N., Mihara E., Matsunaga Y., Noda M., Yamashita N., Toyofuku T., Uchiyama S., Goshima Y., Kumanogoh A., Takagi J. Structural basis for semaphorin signalling through the plexin receptor. Nature 2010, 467:1123-1127.
40. Ottino P., Finley J., Rojo E., Ottlecz A., Lambrou G.N., Bazan H.E., Bazan N.G. Hypoxia activates matrix metalloproteinase expression and the VEGF system in monkey choroid-retinal endothelial cells: Involvement of cytosolic phospholipase A2 activity. Mol. Vis. 2004, 10:341-350.
41. Pan Q., Chanthery Y., Liang W.C., Stawicki S., Mak J., Rathore N., Tong R.K., Kowalski J., Yee S.F., Pacheco G., et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007, 11:53-67.
42. Pucci F., Venneri M.A., Biziato D., Nonis A., Moi D., Sica A., Di Serio C., Naldini L., De Palma M. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 2009, 114:901-914.
43. Püschel A.W., Adams R.H., Betz H. Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 1995, 14:941-948.
44. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
45. Rolny C., Mazzone M., Tugues S., Laoui D., Johansson I., Coulon C., Squadrito M.L., Segura I., Li X., Knevels E., et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 2011, 19:31-44.
46. Schwarz Q., Ruhrberg C. Neuropilin, you gotta let me know: should I stay or should I go?. Cell Adhes. Migr. 2010, 4:61-66.
47. Serini G., Valdembri D., Zanivan S., Morterra G., Burkhardt C., Caccavari F., Zammataro L., Primo L., Tamagnone L., Logan M., et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 2003, 424:391-397.
48. Soker S., Takashima S., Miao H.Q., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998, 92:735-745.
49. Takamatsu H., Takegahara N., Nakagawa Y., Tomura M., Taniguchi M., Friedel R.H., Rayburn H., Tessier-Lavigne M., Yoshida Y., Okuno T., et al. Semaphorins guide the entry of dendritic cells into the lymphatics by activating myosin II. Nat. Immunol. 2010, 11:594-600.
50. Takeda Y., Costa S., Delamarre E., Roncal C., Leite de Oliveira R., Squadrito M.L., Finisguerra V., Deschoemaeker S., Bruyère F., Wenes M., et al. Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature 2011, 479:122-126.
51. Tamagnone L. Emerging role of semaphorins as major regulatory signals and potential therapeutic targets in cancer. Cancer Cell 2012, 22:145-152.
52. Tordjman R., Lepelletier Y., Lemarchandel V., Cambot M., Gaulard P., Hermine O., Roméo P.H. A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nat. Immunol. 2002, 3:477-482.
53. Yacoub M., Coulon A., Celhay O., Irani J., Cussenot O., Fromont G. Differential expression of the semaphorin 3A pathway in prostatic cancer. Histopathology 2009, 55:392-398.
54. Zhang Z.G., Tsang W., Zhang L., Powers C., Chopp M. Up-regulation of neuropilin-1 in neovasculature after focal cerebral ischemia in the adult rat. J.Cereb. Blood Flow Metab. 2001, 21:541-549.