Improved Treatment Efficacy of Antiangiogenic Therapy when Combined with Picornavirus Vaccination in the GL261 Glioma Model

详细信息    查看全文

• 作者：Danielle N. Renner ; Courtney S. Malo ; Fang Jin ; Ian F. Parney…
• 关键词：Glioma ; Combination therapy ; Antiangiogenic ; Tumor invasiveness ; Immunotherapy
• 刊名：Neurotherapeutics
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：13
• 期：1
• 页码：226-236
• 全文大小：5,680 KB
• 参考文献：1.Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. Angiogenesis in brain tumours. Nat Rev Neurosci 2007;8:610-622.CrossRef PubMed
  2.Soda Y, Myskiw C, Rommel A, Verma IM. Mechanisms of neovascularization and resistance to anti-angiogenic therapies in glioblastoma multiforme. J Mol Med (Berl) 2013;91:439-448.CrossRef
  3.Holash J, Maisonpierre PC, Compton D, et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 1999;284:1994-1998.CrossRef PubMed
  4.Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843-845.CrossRef PubMed
  5.Plate KH, Breier G, Weich HA, Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992;359:845-848.CrossRef PubMed
  6.Kim KJ, Li B, Winer J, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 1993;362:841-844.CrossRef PubMed
  7.Chaudhry IH, O'Donovan DG, Brenchley PE, Reid H, Roberts IS. Vascular endothelial growth factor expression correlates with tumour grade and vascularity in gliomas. Histopathology 2001;39:409-415.CrossRef PubMed
  8.Oehring RD, Miletic M, Valter MM, et al. Vascular endothelial growth factor (VEGF) in astrocytic gliomas--a prognostic factor? J Neurooncol 1999;45:117-125.CrossRef PubMed
  9.Presta LG, Chen H, O'Connor SJ, et al. Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res 1997;57:4593-4599.PubMed
  10.Cohen MH, Shen YL, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme. Oncologist 2009;14:1131-1138.CrossRef PubMed
  11.Norden AD, Drappatz J, Muzikansky A, et al. An exploratory survival analysis of anti-angiogenic therapy for recurrent malignant glioma. J Neurooncol 2009;92:149-155.CrossRef PubMed
  12.Friedman HS, Prados MD, Wen PY, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009;27:4733-4740.CrossRef PubMed
  13.Vredenburgh JJ, Desjardins A, Herndon JE, 2nd, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 2007;25:4722-4729.CrossRef PubMed
  14.Kreisl TN, Zhang W, Odia Y, et al. A phase II trial of single-agent bevacizumab in patients with recurrent anaplastic glioma. Neuro Oncol 2011;13:1143-1150.PubMedCentral CrossRef PubMed
  15.Chinot OL, Wick W, Mason W, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 2014;370:709-722.CrossRef PubMed
  16.Gilbert MR, Dignam JJ, Armstrong TS, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 2014;370:699-708.PubMedCentral CrossRef PubMed
  17.Lu KV, Bergers G. Mechanisms of evasive resistance to anti-VEGF therapy in glioblastoma. CNS Oncol 2013;2:49-65.PubMedCentral CrossRef PubMed
  18.Nagpal S, Harsh G, Recht L. Bevacizumab improves quality of life in patients with recurrent glioblastoma. Chemother Res Pract 2011;2011:602812.PubMedCentral PubMed
  19.Holash J, Davis S, Papadopoulos N, et al. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci U S A 2002;99:11393-11398.PubMedCentral CrossRef PubMed
  20.Lockhart AC, Rothenberg ML, Dupont J, et al. Phase I study of intravenous vascular endothelial growth factor trap, aflibercept, in patients with advanced solid tumors. J Clin Oncol 2010;28:207-214.PubMedCentral CrossRef PubMed
  21.Papadopoulos N, Martin J, Ruan Q, et al. Binding and neutralization of vascular endothelial growth factor (VEGF) and related ligands by VEGF Trap, ranibizumab and bevacizumab. Angiogenesis 2012;15:171-185.PubMedCentral CrossRef PubMed
  22.Yu L, Wu X, Cheng Z, et al. Interaction between bevacizumab and murine VEGF-A: a reassessment. Invest Ophthalmol Visual Sci 2008;49:522-527.CrossRef
  23.Ferrara N, Hillan KJ, Gerber H-P, Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 2004;3:391-400.CrossRef PubMed
  24.Gomez-Manzano C, Holash J, Fueyo J, et al. VEGF Trap induces antiglioma effect at different stages of disease. Neuro Oncol 2008;10:940-945.PubMedCentral CrossRef PubMed
  25.de Groot JF, Lamborn KR, Chang SM, et al. Phase II study of aflibercept in recurrent malignant glioma: a North American Brain Tumor Consortium study. J Clin Oncol 2011;29:2689-2695.PubMedCentral CrossRef PubMed
  26.Narayana A, Gruber D, Kunnakkat S, et al. A clinical trial of bevacizumab, temozolomide, and radiation for newly diagnosed glioblastoma. J Neurosurg 2012;116:341-345.CrossRef PubMed
  27.de Groot JF, Fuller G, Kumar AJ, et al. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro Oncol 2010;12:233-242.PubMedCentral CrossRef PubMed
  28.Zuniga RM, Torcuator R, Jain R, et al. Efficacy, safety and patterns of response and recurrence in patients with recurrent high-grade gliomas treated with bevacizumab plus irinotecan. J Neurooncol 2009;91:329-336.CrossRef PubMed
  29.Rubenstein JL, Kim J, Ozawa T, et al. Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2000;2:306-314.PubMedCentral CrossRef PubMed
  30.Lamszus K, Kunkel P, Westphal M. Invasion as limitation to anti-angiogenic glioma therapy. Acta Neurochir Suppl 2003;88:169-177.PubMed
  31.Keunen O, Johansson M, Oudin A, et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci U S A 2011;108:3749-3754.PubMedCentral CrossRef PubMed
  32.Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15:220-231.PubMedCentral CrossRef PubMed
  33.Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J Neurosurg 2009;110:572-582.PubMedCentral CrossRef PubMed
  34.Barcia C, Jr., Gomez A, Gallego-Sanchez JM, et al. Infiltrating CTLs in human glioblastoma establish immunological synapses with tumorigenic cells. Am J Pathol 2009;175:786-798.PubMedCentral CrossRef PubMed
  35.Suidan GL, Dickerson JW, Chen Y, et al. CD8 T cell-initiated vascular endothelial growth factor expression promotes central nervous system vascular permeability under neuroinflammatory conditions. J Immunol 2010;184:1031-1040.PubMedCentral CrossRef PubMed
  36.Argaw AT, Asp L, Zhang J, et al. Astrocyte-derived VEGF-A drives blood
  ain barrier disruption in CNS inflammatory disease. J Clin Invest 2012;122:2454-2468.PubMedCentral CrossRef PubMed
  37.Ueda R, Fujita M, Zhu X, et al. Systemic inhibition of transforming growth factor-beta in glioma-bearing mice improves the therapeutic efficacy of glioma-associated antigen peptide vaccines. Clin Cancer Res 2009;15:6551-6559.PubMedCentral CrossRef PubMed
  38.Xiong Z, Ohlfest JR. Topical imiquimod has therapeutic and immunomodulatory effects against intracranial tumors. J Immunother 2011;34:264-269.PubMedCentral CrossRef PubMed
  39.Cantini G, Pisati F, Mastropietro A, et al. A critical role for regulatory T cells in driving cytokine profiles of Th17 cells and their modulation of glioma microenvironment. Cancer Immunol Immunother 2011;60:1739-1750.CrossRef PubMed
  40.Ausman JI, Shapiro WR, Rall DP. Studies on the chemotherapy of experimental brain tumors: development of an experimental model. Cancer Res 1970;30:2394-2400.PubMed
  41.Maes W, Van Gool SW. Experimental immunotherapy for malignant glioma: lessons from two decades of research in the GL261 model. Cancer Immunol Immunother 2011;60:153-160.CrossRef PubMed
  42.Ohlfest JR, Andersen BM, Litterman AJ, et al. Vaccine injection site matters: qualitative and quantitative defects in CD8 T cells primed as a function of proximity to the tumor in a murine glioma model. J Immunol 2013;190:613-620.PubMedCentral CrossRef PubMed
  43.Renner DN, Jin F, Litterman AJ, et al. Effective treatment of established GL261 murine gliomas through picornavirus vaccination-enhanced tumor antigen-specific CD8+ T cell responses. PLoS One 2015;10:e0125565.PubMedCentral CrossRef PubMed
  44.Pavelko KD, Bell MP, Karyampudi L, et al. The epitope integration site for vaccine antigens determines virus control while maintaining efficacy in an engineered cancer vaccine. Mol Ther 2013;21:1087-1095.PubMedCentral CrossRef PubMed
  45.Johnson HL, Chen Y, Jin F, et al. CD8 T cell-initiated blood
  ain barrier disruption is independent of neutrophil support. J Immunol 2012;189:1937-1945.PubMedCentral CrossRef PubMed
  46.Pirko I, Johnson AJ. Neuroimaging of demyelination and remyelination models. Curr Top Microbiol Immunol 2008;318:241-266.PubMed
  47.Xu T, Chen J, Lu Y, Wolff JE. Effects of bevacizumab plus irinotecan on response and survival in patients with recurrent malignant glioma: a systematic review and survival-gain analysis. BMC Cancer 2010;10:252.PubMedCentral CrossRef PubMed
  48.Lockman PR, Mittapalli RK, Taskar KS, et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res 2010;16:5664-5678.PubMedCentral CrossRef PubMed
  49.Prins RM, Soto H, Konkankit V, et al. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res 2011;17:1603-1615.PubMedCentral CrossRef PubMed
  50.Wheeler CJ, Black KL, Liu G, et al. Vaccination elicits correlated immune and clinical responses in glioblastoma multiforme patients. Cancer Res 2008;68:5955-5964.CrossRef PubMed
  51.Schuessler A, Smith C, Beagley L, et al. Autologous T-cell therapy for cytomegalovirus as a consolidative treatment for recurrent glioblastoma. Cancer Res 2014;74:3466-3476.CrossRef PubMed
  52.Iwama T, Yamada H, Sakai N, et al. Correlation between magnetic resonance imaging and histopathology of intracranial glioma. Neurol Res 1991;13:48-54.PubMed
  53.Chen XZ, Yin XM, Ai L, Chen Q, Li SW, Dai JP. Differentiation between brain glioblastoma multiforme and solitary metastasis: qualitative and quantitative analysis based on routine MR imaging. AJNR Am J Neuroradiol 2012;33;1907-1912.CrossRef PubMed
  54.Hammoud MA, Sawaya R, Shi W, Thall PF, Leeds NE. Prognostic significance of preoperative MRI scans in glioblastoma multiforme. J Neurooncol 1996;27;65-73.CrossRef PubMed
  55.Pishko GL, Muldoon LL, Pagel MA, Schwartz DL, Neuwelt EA. Vascular endothelial growth factor blockade alters magnetic resonance imaging biomarkers of vascular function and decreases barrier permeability in a rat model of lung cancer brain metastasis. Fluids Barriers CNS 2015;12:5.PubMedCentral CrossRef PubMed
  56.Muldoon LL, Gahramanov S, Li X, Marshall DJ, Kraemer DF, Neuwelt EA. Dynamic magnetic resonance imaging assessment of vascular targeting agent effects in rat intracerebral tumor models. Neuro Oncol 2011;13:51-60.PubMedCentral CrossRef PubMed
  57.Du R, Lu KV, Petritsch C, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008;13:206-220.PubMedCentral CrossRef PubMed
  58.Hodi FS, Lawrence D, Lezcano C, et al. Bevacizumab plus ipilimumab in patients with metastatic melanoma. Cancer Immunol Res 2014;2:632-642.PubMedCentral CrossRef PubMed
  59.Mansfield AS, Nevala WK, Lieser EA, Leontovich AA, Markovic SN. The immunomodulatory effects of bevacizumab on systemic immunity in patients with metastatic melanoma. Oncoimmunology 2013;2:e24436.PubMedCentral CrossRef PubMed
  60.Huang Y, Yuan J, Righi E, et al. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci U S A 2012;109:17561-17566.PubMedCentral CrossRef PubMed
  
• 作者单位：Danielle N. Renner (1)
  Courtney S. Malo (2)
  Fang Jin (2)
  Ian F. Parney (2) (3)
  Kevin D. Pavelko (2)
  Aaron J. Johnson (2) (4)
  
  1. Neurobiology of Disease Graduate Program, Mayo Clinic, Rochester, MN, USA
  2. Department of Immunology, Mayo Clinic, Rochester, MN, USA
  3. Department of Neurosurgery, Mayo Clinic, Rochester, MN, USA
  4. Department of Neurology, Mayo Clinic, Rochester, MN, USA
  
• 刊物主题：Neurosciences; Neurology; Neurosurgery; Neurobiology;
• 出版者：Springer US
• ISSN：1878-7479

文摘

The addition of antiangiogenic therapy to the standard-of-care treatment regimen for recurring glioblastoma has provided some clinical benefits while also delineating numerous caveats, prompting evaluation of the elicited alterations to the tumor microenvironment. Of critical importance, given the steadily increasing incorporation of immunotherapeutic approaches clinically, is an enhanced understanding of the interplay between angiogenic and immune response pathways within tumors. In the present study, the GL261 glioma mouse model was used to determine the effects of antiangiogenic treatment in an immune-competent host. Following weekly systemic administration of aflibercept, an inhibitor of vascular endothelial growth factor, tumor volume was assessed by magnetic resonance imaging and changes to the tumor microenvironment were determined. Treatment with aflibercept resulted in reduced tumor burden and increased survival compared with controls. Additionally, decreased vascular permeability and preservation of the integrity of tight junction proteins were observed. Treated tumors also displayed hallmarks of anti-angiogenic evasion, including marked upregulation of vascular endothelial growth factor expression and increased tumor invasiveness. Aflibercept was then administered in combination with a picornavirus-based antitumor vaccine and tumor progression was evaluated. This combination therapy significantly delayed tumor progression and extended survival beyond that observed for either therapy alone. As such, this work demonstrates the efficacy of combined antiangiogenic and immunotherapy approaches for treating established gliomas and provides a foundation for further evaluation of the effects of antiangiogenic therapy in the context of endogenous or vaccine-induced inflammatory responses. Key Words Glioma Combination therapy Antiangiogenic Tumor invasiveness Immunotherapy