This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.
Transcript
1
Immune Consequences of Decreasing Tumor Vasculature with Antiangiogenic Tyrosine Kinase Inhibitors in Combination with Therapeutic Vaccines
Benedetto Farsaci1*, Renee N. Donahue1*, Michael A. Coplin1, Italia Grenga1, Lauren M. Lepone1, Alfredo A. Molinolo2, and James W. Hodge1
Authors’ Affiliations: 1Laboratory of Tumor Immunology and Biology, Center for Cancer Research, National Cancer Institute, and 2Oral and Pharyngeal Cancer Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD, USA
*Authors contributed equally to this manuscript. Running Title: Effects of antiangiogenic agents plus vaccine in the tumor microenvironment Keywords: TKI, sunitinib, sorafenib, vaccine, immunotherapy, angiogenesis, cancer Corresponding Author: James W. Hodge, Laboratory of Tumor Immunology and Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, 10 Center Drive, Room 8B13, Bethesda, MD 20892, USA. Phone: (301) 496-0631; Fax: (301) 496-2756; Email: [email protected]
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
1. Farsaci B, Higgins JP, Hodge JW. Consequence of dose scheduling of sunitinib on host immune response elements and vaccine combination therapy. Int J Cancer. 2012;130:1948-59.
2. Bose A, Taylor JL, Alber S, Watkins SC, Garcia JA, Rini BI, et al. Sunitinib facilitates the activation and recruitment of therapeutic anti-tumor immunity in concert with specific vaccination. Int J Cancer. 2011;129:2158-70.
3. Gabrilovich D, Ishida T, Oyama T, Ran S, Kravtsov V, Nadaf S, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood. 1998;92:4150-66.
4. Dineen SP, Lynn KD, Holloway SE, Miller AF, Sullivan JP, Shames DS, et al. Vascular endothelial growth factor receptor 2 mediates macrophage infiltration into orthotopic pancreatic tumors in mice. Cancer Res. 2008;68:4340-6.
5. Beatty G, Paterson Y. IFN-gamma-dependent inhibition of tumor angiogenesis by tumor-infiltrating CD4+ T cells requires tumor responsiveness to IFN-gamma. J Immunol. 2001;166:2276-82.
6. Porta C, Rimoldi M, Raes G, Brys L, Ghezzi P, Di Liberto D, et al. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci U S A. 2009;106:14978-83.
7. Qin Z, Schwartzkopff J, Pradera F, Kammertoens T, Seliger B, Pircher H, et al. A critical requirement of interferon gamma-mediated angiostasis for tumor rejection by CD8+ T cells. Cancer Res. 2003;63:4095-100.
8. Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res. 2009;15:2148-57.
9. Ko JS, Rayman P, Ireland J, Swaidani S, Li G, Bunting KD, et al. Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res. 2010;70:3526-36.
10. Clarke P, Mann J, Simpson JF, Rickard-Dickson K, Primus FJ. Mice transgenic for human carcinoembryonic antigen as a model for immunotherapy. Cancer Res. 1998;58:1469-77.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
11. Schmitz J, Reali E, Hodge JW, Patel A, Davis G, Schlom J, et al. Identification of an interferon-gamma-inducible carcinoembryonic antigen (CEA) CD8(+) T-cell epitope, which mediates tumor killing in CEA transgenic mice. Cancer Res. 2002;62:5058-64.
12. Robbins PF, Kantor JA, Salgaller M, Hand PH, Fernsten PD, Schlom J. Transduction and expression of the human carcinoembryonic antigen gene in a murine colon carcinoma cell line. Cancer Res. 1991;51:3657-62.
13. Milross CG, Tucker SL, Mason KA, Hunter NR, Peters LJ, Milas L. The effect of tumor size on necrosis and polarographically measured pO2. Acta Oncol. 1997;36:183-9.
14. Hodge JW, Poole DJ, Aarts WM, Gomez Yafal A, Gritz L, Schlom J. Modified vaccinia virus ankara recombinants are as potent as vaccinia recombinants in diversified prime and boost vaccine regimens to elicit therapeutic antitumor responses. Cancer Res. 2003;63:7942-9.
15. Hodge JW, Grosenbach DW, Aarts WM, Poole DJ, Schlom J. Vaccine therapy of established tumors in the absence of autoimmunity. Clin Cancer Res. 2003;9:1837-49.
16. Hodge JW, Sabzevari H, Yafal AG, Gritz L, Lorenz MG, Schlom J. A triad of costimulatory molecules synergize to amplify T-cell activation. Cancer Res. 1999;59:5800-7.
17. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 2007;356:125-34.
18. Whitesides TE, Jr., Haney TC, Harada H, Holmes HE, Morimoto K. A simple method for tissue pressure determination. Arch Surg. 1975;110:1311-3.
19. Gotink KJ, Verheul HM. Anti-angiogenic tyrosine kinase inhibitors: what is their mechanism of action? Angiogenesis. 2010;13:1-14.
20. Finke JH, Rini B, Ireland J, Rayman P, Richmond A, Golshayan A, et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin Cancer Res. 2008;14:6674-82.
21. Ardiani A, Farsaci B, Rogers CJ, Protter A, Guo Z, King TH, et al. Combination therapy with a second-generation androgen receptor antagonist and a metastasis vaccine improves survival in a spontaneous prostate cancer model. Clin Cancer Res. 2013;19:6205-18.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
22. Ardiani A, Gameiro SR, Palena C, Hamilton DH, Kwilas A, King TH, et al. Vaccine-Mediated Immunotherapy Directed against a Transcription Factor Driving the Metastatic Process. Cancer Res. 2014.
23. Kuwana M, Okazaki Y, Kodama H, Satoh T, Kawakami Y, Ikeda Y. Endothelial differentiation potential of human monocyte-derived multipotential cells. Stem Cells. 2006;24:2733-43.
24. Yamaguchi Y, Kuwana M. Proangiogenic hematopoietic cells of monocytic origin: roles in vascular regeneration and pathogenic processes of systemic sclerosis. Histol Histopathol. 2013;28:175-83.
25. Stylianopoulos T, Martin JD, Chauhan VP, Jain SR, Diop-Frimpong B, Bardeesy N, et al. Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors. Proc Natl Acad Sci U S A. 2012;109:15101-8.
26. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med. 2010;207:2439-53.
27. Doedens AL, Stockmann C, Rubinstein MP, Liao D, Zhang N, DeNardo DG, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 2010;70:7465-75.
28. Hayakawa Y, Takeda K, Yagita H, Smyth MJ, Van Kaer L, Okumura K, et al. IFN-gamma-mediated inhibition of tumor angiogenesis by natural killer T-cell ligand, alpha-galactosylceramide. Blood. 2002;100:1728-33.
29. Huang Y, Yuan J, Righi E, Kamoun WS, Ancukiewicz M, Nezivar J, et al. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci U S A. 2012;109:17561-6.
30. Dallas NA, Samuel S, Xia L, Fan F, Gray MJ, Lim SJ, et al. Endoglin (CD105): a marker of tumor vasculature and potential target for therapy. Clin Cancer Res. 2008;14:1931-7.
31. Li C, Issa R, Kumar P, Hampson IN, Lopez-Novoa JM, Bernabeu C, et al. CD105 prevents apoptosis in hypoxic endothelial cells. J Cell Sci. 2003;116:2677-85.
32. Glod J, Kobiler D, Noel M, Koneru R, Lehrer S, Medina D, et al. Monocytes form a vascular barrier and participate in vessel repair after brain injury. Blood. 2006;107:940-6.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
33. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62.
34. Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, Nusrat A. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J. 2005;19:923-33.
35. Boehm AL, Higgins J, Franzusoff A, Schlom J, Hodge JW. Concurrent vaccination with two distinct vaccine platforms targeting the same antigen generates phenotypically and functionally distinct T-cell populations. Cancer Immunol Immunother. 2010;59:397-408.
36. Zoglmeier C, Bauer H, Norenberg D, Wedekind G, Bittner P, Sandholzer N, et al. CpG blocks immunosuppression by myeloid-derived suppressor cells in tumor-bearing mice. Clin Cancer Res. 2011;17:1765-75.
37. Ortiz M, Lu L, Ramachandran I, Gabrilovich D. Myeloid-derived suppressor cells in the development of lung cancer. Cancer Immunol Res. 2013;2:50-8.
38. Chakour R, Allenbach C, Desgranges F, Charmoy M, Mauel J, Garcia I, et al. A new function of the Fas-FasL pathway in macrophage activation. J Leukoc Biol. 2009;86:81-90.
39. McKenney JK, Weiss SW, Folpe AL. CD31 expression in intratumoral macrophages: a potential diagnostic pitfall. Am J Surg Pathol. 2001;25:1167-73.
40. Lastres P, Bellon T, Cabanas C, Sanchez-Madrid F, Acevedo A, Gougos A, et al. Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen. Eur J Immunol. 1992;22:393-7.
41. Terme M, Pernot S, Marcheteau E, Sandoval F, Benhamouda N, Colussi O, et al. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res. 2013;73:539-49.
42. Chen ML, Yan BS, Lu WC, Chen MH, Yu SL, Yang PC, et al. Sorafenib relieves cell-intrinsic and cell-extrinsic inhibitions of effector T cells in tumor microenvironment to augment antitumor immunity. Int J Cancer. 2014;134:319-31.
43. Cabrera R, Ararat M, Xu Y, Brusko T, Wasserfall C, Atkinson MA, et al. Immune modulation of effector CD4+ and regulatory T cell function by sorafenib in patients with hepatocellular carcinoma. Cancer Immunol Immunother. 2013;62:737-46.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
44. Huang Y, Goel S, Duda DG, Fukumura D, Jain RK. Vascular normalization as an emerging strategy to enhance cancer immunotherapy. Cancer Res. 2013;73:2943-8.
45. Ardiani A, Gameiro SR, Palena C, Hamilton DH, Kwilas A, King TH, et al. Vaccine-mediated immunotherapy directed against a transcription factor driving the metastatic process. Cancer Res. 2014;74:1945-57.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076
Published OnlineFirst August 4, 2014.Cancer Immunol Res Benedetto Farsaci, Renee N Donahue, Michael A Coplin, et al. therapeutic vaccinesantiangiogenic tyrosine kinase inhibitors in combination with Immune consequences of decreasing tumor vasculature with
Updated version
10.1158/2326-6066.CIR-14-0076doi:
Access the most recent version of this article at:
To order reprints of this article or to subscribe to the journal, contact the AACR Publications
Permissions
Rightslink site. Click on "Request Permissions" which will take you to the Copyright Clearance Center's (CCC)
.http://cancerimmunolres.aacrjournals.org/content/early/2014/08/02/2326-6066.CIR-14-0076To request permission to re-use all or part of this article, use this link
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on August 4, 2014; DOI: 10.1158/2326-6066.CIR-14-0076