Antibody blockade of Semaphorin 4D promotes immune infiltration into tumor and enhances response to other immunomodulatory therapies

Cancer Immunology Research

Volumn 3, Issue 6, 2015, Pages 698-701

  Evans, Elizabeth E ^a   Jonason, Alan S ^a   Bussler, Holm ^a   Torno, Sebold ^a   Veeraraghavan, Janaki ^a   Reilly, Christine ^a   Doherty, Michael A ^a   Seils, Jennifer ^a   Winter, Laurie A ^a   Mallow, Crystal ^a   Kirk, Renee ^a   Howell, Alan ^a   Giralico, Susan ^a   Scrivens, Maria ^a   Klimatcheva, Katya ^a   Fisher, Terrence L ^a   Bowers, William J ^a   Paris, Mark ^a   Smith, Ernest S ^a   Zauderer, Maurice ^a  

^a VACCINEX INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; IMMUNOMODULATING AGENT; MONOCLONAL ANTIBODY; PD 1 ANTIBODY; SEMAPHORIN 4D ANTIBODY; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BLOCKING ANTIBODY; CD100 ANTIGEN; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EPIDERMAL GROWTH FACTOR RECEPTOR 2; LEUKOCYTE ANTIGEN; PROGRAMMED DEATH 1 RECEPTOR; SEMAPHORIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CELL INFILTRATION; CELLULAR DISTRIBUTION; COLON CANCER; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG RESPONSE; FEMALE; IMMUNOGENICITY; MONOTHERAPY; MOUSE; NONHUMAN; PHAGOCYTE; PROTEIN EXPRESSION; SPLEEN CELL; TUMOR MICROENVIRONMENT; TUMOR REJECTION; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIGEN PRESENTING CELL; BREAST NEOPLASMS; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOTHERAPY; LYMPHOCYTE SUBPOPULATION; METABOLISM; MORTALITY; NEOPLASMS; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, MONOCLONAL; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CTLA-4 ANTIGEN; CYCLOPHOSPHAMIDE; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOMODULATION; IMMUNOTHERAPY; LYMPHOCYTE SUBSETS; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; NEOPLASMS; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTOR, ERBB-2; SEMAPHORINS; TUMOR BURDEN; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84961879818     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0171     Document Type: Article

References (50)

1. Peranzoni E, Rivas-Caicedo A, Bougherara H, Salmon H, Donnadieu E. Positive and negative influence of the matrix architecture. Cell Mol Life Sci 2013;70:4431-48.
2. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653-60.
3. Atreya I, Neurath MF. Immune cells in colorectal cancer: prognostic relevance and therapeutic strategies. Expert Rev Anticancer Ther 2008;8:561-72.
4. Galon JA. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013;39:11-26.
5. Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013;39:782-95.
6. Hartmann N, Giese N, Giese T, Poschke I, Offringa R, Werner J, et al. Prevailing role of contact guidance in intrastromal T-cell trapping in human pancreatic cancer. Clin Cancer Res 2014;20:3422-33.
7. Giraudon P, Vincent P, Vuaillat C. T-cells in neuronal injury and repair: semaphorins and related T-cell signals. Neuromolecular Med 2005;7:207-16.
8. Worzfeld T, Offermans S. Semaphorins and plexins as therapeutic targets. Nat Rev 2014;13:603-21.
9. Mendez-da-Cruz DA, Lepelletier Y, Brignier AC, Smaniotto S, Renand A, Milpied P, et al. Neuropilins, semaphorins, and their role in thymocyte development. Neuroimmunomodulation 2009;1153:20-8.
10. Takamatsu H, Takegahara N, Nakagawa Y, Tomura M, Taniguchi M, Friedel RH, et al. Semaphorins guide the entry of dendritic cells into the lymphatics by activating myosin II. Nat Immunol 2010;11:594-601.
11. Casazza A, Laoui D, Wenes M, Rizzolio S, Bassani N, Mambretti M, et al. Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity. Cancer Cell 2013;24:695-709.
12. Delaire S, Billard C, Tordjman R, Chédotal A, Elhabazi A, Bensussan A, et al. Biological activity of soluble CD100. II. soluble CD100, similarly to H-SemaIII, inhibits immune cell migration. J Immunol 2001;166:4348-54.
13. Sun Q, Zhou H, Binmadi NO, Basile JR. Hypoxia-inducible factor-1-mediated regulation of semaphorin 4D affects tumor growth and vascularity. J Biol Chem 2009;284:32066-74.
14. Bosco M, Pierobon D, Blengio F, Raggi F, Vanni C, Gattorno M, et al. Hypoxia modulates the gene expression profile of immunoregulatory receptors in human mature dendritic cells: identification of TREM-1 as a novel hypoxic marker in vitro and in vivo. Blood 2011;117:2625-39.
15. Elvidge G, Glenny L, Appelhoff R, Ratcliffe P, Ragoussis J, Gleadle J. Concordant regulation of gene expression by hypoxia and 2-oxoglutaratedependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 2006;281:15215-26.
16. Sierra JR, Corso S, Caione L, Cepero V, Conrotto P, Cignetti A. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages. J Exp Med 2008;205:1673-85.
17. Kikutani H, Kumanogoh A. Semaphorins in interactions between T cells and antigen-presenting cells. Nat Rev Immunol 2003;3:159-67.
18. Basile JR, Holmbeck K, Bugge TH, Gutkind JS. MT1-MMP controls tumorinduced angiogenesis through the release of semaphorin 4D. J Biol Chem 2007;282:6899-905.
19. Hall KT, Boumsell L, Schultze JL, Boussiotis VA, Dorfman DM, Cardoso AA, et al. Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation. Proc Natl Acad Sci U S A 1996;93:11780-5.
20. Basile JR, Castilho RM, Williams VP, Gutkind JS. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc Natl Acad Sci U S A 2006;103:9017-22.
21. Worzfeld T, Swiercz JM, Looso M, Straub BK, Sivaraj KK, Offermanns S. ErbB-2 signals through Plexin-B1 to promote breast cancer metastasis. J Clin Invest 2012;122:1296-305.
22. Valente G, Nicotra G, Arrondini M, Castino R, Capparuccia L, Prat M, et al. Co-expression of plexin B1 and Met in human breast and ovary tumours enhances the risk of progression. Cell Oncol 2009;31:423-36.
23. Campos M, Campos SG, Ribeiro GG, Eguchi FC, Da Silva SR, De Oliveira CZ, et al. Ki-67 and CD100 immunohistochemical expression is associated with local recurrence and poor prognosis in soft tissue sarcomas, respectively. Oncol Lett 2013;5:1527-35.
24. Ch'ng ES, Kumanogoh A. Roles of Sema4D and Plexin-B1 in tumor progression. Mol Cancer 2010;9:251.
25. Kato S, Kubota K, Shimamura T, Shinohara Y, Kobayashi N, Watanabe S, et al. Semaphorin 4D, a lymphocyte semaphorin, enhancestumor cell motility through binding its receptor, plexinB1, in pancreatic cancer. Cancer Sci 2011;102:2029-37.
26. Conrotto P, Valdembri D, Corso S, Serini G, Tamagnone L, Comoglio PM, et al. Sema4D induces angiogenesis through Met recruitment by Plexin B1. Blood 2005;105:4321-9.
27. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999;99:71-80.
28. Giordano S, Corso S, Conrotto P, Artigiani S, Gilestro G, Barberis D, et al. The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat Cell Biol 2002;4:720-4.
29. Witherden DA, Watanabe M, Garijo O, Rieder SE, Sarkisyan G, Cronin SJ, et al. The CD100 receptor interacts with its plexin B2 ligand to regulate epidermal gammadelta T cell function. Immunity 2012;37:314-25.
30. Kumanogoh A, Suzuki K, Ch'ng E, Watanabe C, Marukawa S, Takegahara N, et al. Requirement for the lymphocyte semaphorin, CD100, in the induction of antigen-specific T cells and the maturation of dendritic cells. J Immunol 2002;169:1175-81.
31. Cui Y-L, Li H-K, Zhou H-Y, Zhang T, Li Q. Correlations of tumor-associated macrophage subtypes with liver metastases of colorectal cancer. Asian Pacific J Cancer Prev 2013;14:1003-7.
32. Almeida JL, Hill CR, Cole KD. Mouse cell line authentication. Cytotechnology 2014;66:133-47.
33. Huang AY. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc Natl Acad Sci U S A 1996;93:9730.
34. + regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007;56:641-8.
35. Lee H-W, Choi H-J, Ha S-J, Lee K-T, Kwon Y-G. Recruitment of monocytes/macrophages in different tumor microenvironments. Biochim Biophys Acta 2013;1835:170-9.
36. Page D, Postow M, Callahan M, Allison J, Wolchok J. Immune modulation in cancer with antibodies. Annu Rev Med 2014;65:185-202.
37. Harshman LC, Drake CG, Wargo JA, Sharma P, Bhardwaj N. Cancer immunotherapy highlights from the 2014 ASCO Meeting. Cancer Immunol Res 2014;2:714-9.
38. Duraiswamy J, Kaluza KM, Freeman GJ, Coukos G. Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T-cell rejection function in tumors. Cancer Res 2013;73:3591-603.
39. Ngiow SF, von Scheidt B, Akiba H, Yagita H, Teng MW, Smyth MJ. Anti-TIM3 antibody promotes T cell IFN-g-mediated antitumor immunity and suppresses established tumors. Cancer Res 2011;71:3540-51.
40. Tongu M, Harashima N, Monma H, Inao T, Yamada T, Kawauchi H, et al. Metronomic chemotherapy with low-dose cyclophosphamide plus gemcitabine can induce anti-tumor T cell immunity in vivo. Cancer Immunol Immunother 2013;62:383-91.
41. Zhou H, Yang Y-H, Basile JR. The Semaphorin 4D-Plexin-B1-RhoA signaling axis recruits pericytes and regulates vascular permeability through endothelial production of PDGF-B and ANGPTL4. Angiogenesis 2013;15:391-407.
42. Zielonka M, Krishnan R, Swiercz J, Offermans S. The IkB kinase complex is required for Plexin-B-mediated activation of RhoA. PLoS ONE 2014;9:e105661.
43. McClellan JL, Davis J, Steiner JL, Enos RT, Jung SH, Carson J A, et al. Linking tumor-associated macrophages, inflammation, and intestinal tumorigenesis: role of MCP-1. Am J Physiol Gastrointest Liver Physiol 2012;303:G1087-95.
44. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
45. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 2009;29:313-26.
46. + regulatory T cells. J Immunol 2006;177:896-904.
47. Engelhardt J, Boldajipour B, Beemiller P, Pandurangi P, Sorensen C, Werb Z, et al. Marginating dendritic cells of the tumor microenvironment crosspresent tumor antigens and stably engage tumor-specific T cells. Cancer Cell 2012;21:402-17.
48. Brahmer JR, Pardoll DM. Immune checkpoint inhibitors: making immunotherapy a reality for the treatment of lung cancer. Cancer Immunol Res 2013;1:85-91.
49. Smith ES, Jonason A, Reilly C, Veeraraghavan J, Fisher T, Doherty M, et al. SEMA4D compromises blood-brain barrier, activates microglia, and inhibits remyelination in neurodegenerative disease. Neurobiol Dis 2015;73:254-68.
50. Leonard JE, Fisher TL, Winter LA, Cornelius CA, Reilly C, Smith ES, et al. Nonclinical safety evaluation of VX15/2503; a humanized IgG4 anti-SEMA4D antibody. Mol Cancer Ther 2015;14:964-72.