The new era progress in immunotherapy of glioma

doi:10.3969/j.issn.1672-6731.2019.11.003

Abstract

Abstract:

Glioma is the most common primary tumor of central nervous system (CNS), about 50% of which is extremely malignant glioblastoma (GBM). GBM is the most common primary malignant brain tumors in adults. Surgery, radiotherapy and chemotherapy (most with temozolomide) are regarded as the conventional treatments, but they failed to significantly prolong the survival of GBM patients. The standard treatment of GBM lacks of specificity, and tumor cells are resistant to radiotherapy or alkylating agents, thus recurrence of GBM is inevitably and the overall prognosis is quite poor. Currently, tumor immunotherapy is emerging and booming, which provides more treating options for GBM. This study, hence, reviews the current status of immunotherapy among the comprehensive treatments of glioma, at the same time indicates the potential targets of immunotherapy, further to update treatment strategies and explain the potential for the resistance of immunotherapy.

Key words: Glioma, Immunotherapy, Cancer vaccine, Immunosuppressive agents, Genes,viral, Review

摘要：

胶质瘤为临床常见的原发性中枢神经系统恶性肿瘤，约50%为恶性程度极高的胶质母细胞瘤。传统治疗方法包括外科手术、放射治疗和以替莫唑胺为主的药物化疗，但这些方法均未获得显著延长胶质母细胞瘤患者生存期的效果。目前针对胶质母细胞瘤的标准治疗方案缺乏特异性，肿瘤细胞对放射治疗和烷化剂易产生抵抗，肿瘤复发不可避免，整体预后较差。随着免疫治疗的兴起，目前关于胶质瘤免疫治疗的基础与临床试验方兴未艾，对迄今发表的胶质瘤免疫治疗进展进行综述，有助于了解免疫治疗在胶质瘤综合治疗中的地位和免疫治疗的潜在靶点，以更新治疗策略及阐述免疫治疗耐药的原因。

关键词: 神经胶质瘤, 免疫疗法, 癌症疫苗, 免疫抑制剂, 基因,病毒, 综述

ZHAO Bing-hao, WANG Ya-ning, ZHOU Li-zhou, DAI Cong-xin, WANG Yu, MA Wen-bin. The new era progress in immunotherapy of glioma[J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2019, 19(11): 807-818.

赵炳昊, 王雅宁, 周李周, 代从新, 王裕, 马文斌. 新时代胶质瘤免疫治疗研究进展[J]. 中国现代神经疾病杂志, 2019, 19(11): 807-818.

/ / Recommend / Download Citations

URL: https://journal11.magtechjournal.com/cjcnn/EN/10.3969/j.issn.1672-6731.2019.11.003

https://journal11.magtechjournal.com/cjcnn/EN/Y2019/V19/I11/807

References

[1] Dolecek TA, Propp JM, Stroup NE, Kruchko C. CBTRUS statistical report:primary brain and central nervous system tumors diagnosed in the United States in 2005-2009[J]. Neuro Oncol, 2012, 5:v1-49.
[2] Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW. The 2016 World Health Organization classification of tumors of the central nervous system:a summary[J]. Acta Neuropathol, 2016, 131:803-820.
[3] Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J. Structural and functional features of central nervous system lymphatic vessels[J]. Nature, 2015, 523:337-341.
[4] Weller M, Wick W, Aldape K, Brada M, Berger M, Pfister SM, Nishikawa R, Rosenthal M, Wen PY, Stupp R, Reifenberger G. Glioma[J]. Nat Rev Dis Primers, 2015, 1:15017.
[5] Billingham RE, Brent L, Medawar PB. Actively acquired tolerance of foreign cells[J]. Nature, 1953, 172:603-606.
[6] Schiffer D, Mellai M, Bovio E, Annovazzi L. The neuropathological basis to the functional role of microglia/macrophages in gliomas[J]. Neurol Sci, 2017, 38:1571-1577.
[7] Preusser M, Lim M, Hafler DA, Reardon DA, Sampson JH. Prospects of immune checkpoint modulators in the treatment of glioblastoma[J]. Nat Rev Neurol, 2015, 11:504-514.
[8] Ma WB, Li YN, Wang RZ. Review and interpretation of key events in comprehensive diagnosis and treatment of glioma in the past 40 years[J]. Zhonghua Lin Chuang Yi Shi Za Zhi (Dian Zi Ban), 2013, 7:6217-6221.[马文斌,李永宁,王任直. 40年间胶质瘤综合诊疗的重要节点事件回顾及解读[J].中华临床医师杂志(电子版), 2013, 7:6217-6221.]
[9] Hirayama M, Nishimura Y. The present status and future prospects of peptide-based cancer vaccines[J]. Int Immunol, 2016, 28:319-328.
[10] Weller M, Kaulich K, Hentschel B, Felsberg J, Gramatzki D, Pietsch T, Simon M, Westphal M, Schackert G, Tonn JC, von Deimling A, Davis T, Weiss WA, Loeffler M, Reifenberger G, German Glioma Network. Assessment and prognostic significance of the epidermal growth factor receptor Ⅷ mutation in glioblastoma patients treated with concurrent and adjuvant temozolomide radiochemotherapy[J]. Int J Cancer, 2014, 134:2437-2447.
[11] Schuster J, Lai RK, Recht LD, Reardon DA, Paleologos NA, Groves MD, Mrugala MM, Jensen R, Baehring JM, Sloan A, Archer GE, Bigner DD, Cruickshank S, Green JA, Keler T, Davis TA, Heimberger AB, Sampson JH. A phase Ⅱ, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma:the ACT Ⅲ study[J]. Neuro Oncol, 2015, 17:854-861.
[12] Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, Gilbert MR, Herndon JE 2nd, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling RJ, Shi W, Vredenburgh JJ, Bigner DD. Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant Ⅲ peptide vaccination in patients with newly diagnosed glioblastoma[J]. J Clin Oncol, 2010, 28:4722-4729.
[13] Sampson JH, Aldape KD, Archer GE, Coan A, Desjardins A, Friedman AH, Friedman HS, Gilbert MR, Herndon JE, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling R, Shi W, Vredenburgh JJ, Bigner DD, Heimberger AB. Greater chemotherapy-induced lymphopenia enhances tumor-specific immune responses that eliminate EGFRvⅢ-expressing tumor cells in patients with glioblastoma[J]. Neuro Oncol, 2011, 13:324-333.
[14] Weller M, Butowski N, Tran DD, Recht LD, Lim M, Hirte H, Ashby L, Mechtler L, Goldlust SA, Iwamoto F, Drappatz J, O'Rourke DM, Wong M, Hamilton MG, Finocchiaro G, Perry J, Wick W, Green J, He Y, Turner CD, Yellin MJ, Keler T, Davis TA, Stupp R, Sampson JH, ACT Ⅳ trial investigators. Rindopepimut with temozolomide for patients with newly diagnosed, EGFRv Ⅲ-expressing glioblastoma (ACT Ⅳ):a randomised, double-blind, international phase 3 trial[J]. Lancet Oncol, 2017, 18:1373-1385.
[15] Reardon D, Schuster J, Tran D, Fink K, Nabors L, Li G, Lukas R, Desjardins A, Ashby L, Duic P, Aneiro L, Hawthorne T, Green J, Yellin M, Davis T, Sampson J. IT-30ReACT:a phase Ⅱ study of rindopepimut vaccine (CDX-110) plus bevacizumab in relapsed glioblastoma[J]. Neuro Oncol, 2014, 16(Suppl 5):116.
[16] Schumacher T, Bunse L, Pusch S, Sahm F, Wiestler B, Quandt J, Menn O, Osswald M, Oezen I, Ott M, Keil M, Bal β J, Rauschenbach K, Grabowska AK, Vogler I, Diekmann J, Trautwein N, Eichmüller SB, Okun J, Stevanovic S, Riemer AB, Sahin U, Friese MA, Beckhove P, von Deimling A, Wick W, Platten M. A vaccine targeting mutant IDH1 induces antitumour immunity[J]. Nature, 2014, 512:324-327.
[17] Fecci PE, Heimberger AB, Sampson JH. Immunotherapy for primary brain tumors:no longer a matter of privilege[J]. Clin Cancer Res, 2014, 20:5620-5629.
[18] Ampie L, Choy W, Lamano JB, Fakurnejad S, Bloch O, Parsa AT. Heat shock protein vaccines against glioblastoma:from bench to bedside[J]. J Neurooncol, 2015, 123:441-448.
[19] Crane CA, Han SJ, Ahn B, Oehlke J, Kivett V, Fedoroff A, Butowski N, Chang SM, Clarke J, Berger MS, McDermott MW, Prados MD, Parsa AT. Individual patient-specific immunity against high-grade glioma after vaccination with autologous tumor derived peptides bound to the 96 KD chaperone protein[J]. Clin Cancer Res, 2013, 19:205-214.
[20] Bloch O, Crane CA, Fuks Y, Kaur R, Aghi MK, Berger MS, Butowski NA, Chang SM, Clarke JL, McDermott MW, Prados MD, Sloan AE, Bruce JN, Parsa AT. Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma:a phase Ⅱ, single-arm trial[J]. Neuro Oncol, 2014, 16:274-279.
[21] Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells[J]. Nat Rev Cancer, 2012, 12:265-277.
[22] Liau LM, Ashkan K, Tran DD, Campian JL, Trusheim JE, Cobbs CS, Heth JA, Salacz M, Taylor S, D'Andre SD, Iwamoto FM, Dropcho EJ, Moshel YA, Walter KA, Pillainayagam CP, Aiken R, Chaudhary R, Goldlust SA, Bota DA, Duic P, Grewal J, Elinzano H, Toms SA, Lillehei KO, Mikkelsen T, Walbert T, Abram SR, Brenner AJ, Brem S, Ewend MG, Khagi S, Portnow J, Kim LJ, Loudon WG, Thompson RC, Avigan DE, Fink KL, Geoffroy FJ, Lindhorst S, Lutzky J, Sloan AE, Schackert G, Krex D, Meisel HJ, Wu J, Davis RP, Duma C, Etame AB, Mathieu D, Kesari S, Piccioni D, Westphal M, Baskin DS, New PZ, Lacroix M, May SA, Pluard TJ, Tse V, Green RM, Villano JL, Pearlman M, Petrecca K, Schulder M, Taylor LP, Maida AE, Prins RM, Cloughesy TF, Mulholland P, Bosch ML. First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma[J]. J Transl Med, 2018, 16:142.
[23] Dafni U, Michielin O, Lluesma SM, Tsourti Z, Polydoropoulou V, Karlis D, Besser JM, Haanen J, Svane IM, Ohashi PS, Kammula US, Orcurto A, Zimmermann S, Trueb L, Klebanoff CA, Lotze MT, Kandalaft LE, Coukos G. Efficacy of adoptive therapy with tumor-infiltrating lymphocytes and recombinant interleukin-2 in advanced cutaneous melanoma:a systematic review and Meta-analysis[J]. Ann Oncol, 2019.[Epub print of ahead]
[24] Garfall AL, Maus MV, Hwang WT, Lacey SF, Mahnke YD, Melenhorst JJ, Zheng Z, Vogl DT, Cohen AD, Weiss BM, Dengel K, Kerr ND, Bagg A, Levine BL, June CH, Stadtmauer EA. Chimeric antigen receptor T cells against CD19 for multiple myeloma[J]. N Engl J Med, 2015, 373:1040-1047.
[25] Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia[J]. N Engl J Med, 2011, 365:725-733.
[26] O'Rourke DM, Nasrallah MP, Desai A, Melenhorst JJ, Mansfield K, Morrissette JJD, Martinez-Lage M, Brem S, Maloney E, Shen A, Isaacs R, Mohan S, Plesa G, Lacey SF, Navenot JM, Zheng Z, Levine BL, Okada H, June CH, Brogdon JL, Maus MV. A single dose of peripherally infused EGFRv Ⅲ-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma[J]. Sci Transl Med, 2017, 9.
[27] Neelapu SS, Tummala S, Kebriaei P, Wierda W, Gutierrez C, Locke FL, Komanduri KV, Lin Y, Jain N, Daver N, Westin J, Gulbis AM, Loghin ME, de Groot JF, Adkins S, Davis SE, Rezvani K, Hwu P, Shpall EJ. Chimeric antigen receptor T-cell therapy-assessment and management of toxicities[J]. Nat Rev Clin Oncol, 2018, 15:47-62.
[28] Brown CE, Starr R, Aguilar B, Shami AF, Martinez C, D'Apuzzo M, Barish ME, Forman SJ, Jensen MC. Stem-like tumor-initiating cells isolated from IL13Ralpha2 expressing gliomas are targeted and killed by IL13-zetakine-redirected T cells[J]. Clin Cancer Res, 2012, 18:2199-2209.
[29] Brown CE, Alizadeh D, Starr R, Weng L, Wagner JR, Naranjo A, Ostberg JR, Blanchard MS, Kilpatrick J, Simpson J, Kurien A, Priceman SJ, Wang X, Harshbarger TL, D'Apuzzo M, Ressler JA, Jensen MC, Barish ME, Chen M, Portnow J, Forman SJ, Badie B. Regression of glioblastoma after chimeric antigen receptor T-cell therapy[J]. N Engl J Med, 2016, 375:2561-2569.
[30] Phillips AC, Boghaert ER, Vaidya KS, Mitten MJ, Norvell S, Falls HD, DeVries PJ, Cheng D, Meulbroek JA, Buchanan FG, McKay LM, Goodwin NC, Reilly EB. ABT-414, an antibody-drug conjugate targeting a tumor-selective EGFR epitope[J]. Mol Cancer Ther, 2016, 15:661-669.
[31] Reardon DA, Lassman AB, van den Bent M, Kumthekar P, Merrell R, Scott AM, Fichtel L, Sulman EP, Gomez E, Fischer J, Lee HJ, Munasinghe W, Xiong H, Mandich H, Roberts-Rapp L, Ansell P, Holen KD, Gan HK. Efficacy and safety results of ABT-414 in combination with radiation and temozolomide in newly diagnosed glioblastoma[J]. Neuro Oncol, 2017, 19:965-975.
[32] Topalian SL, Taube JM, Anders RA, Pardoll DM. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy[J]. Nat Rev Cancer, 2016, 16:275-287.
[33] Reardon DA, Omuro A, Brandes AA, Rieger J, Wick A, Sepúlveda JM, Phuphanich S, Souza PD, Ahluwalia MS, Lim M, Vlahovic G, Sampson J. OS10.3 randomized phase 3 study evaluating the efficacy and safety of nivolumab vs bevacizumab in patients with recurrent glioblastoma:CheckMate 143[J]. Neuro Oncol, 2017, 19(Suppl_3):iii21.
[34] Morgan RA, Johnson LA, Davis JL, Zheng Z, Woolard KD, Reap EA, Feldman SA, Chinnasamy N, Kuan CT, Song H, Zhang W, Fine HA, Rosenberg SA. Recognition of glioma stem cells by genetically modified T cells targeting EGFRv Ⅲ and development of adoptive cell therapy for glioma[J]. Hum Gene Ther, 2012, 23:1043-1053.
[35] Narita Y, Arakawa Y, Yamasaki F, Nishikawa R, Aoki T, Kanamori M, Nagane M, Kumabe T, Hirose Y, Ichikawa T, Kobayashi H, Fujimaki T, Goto H, Takeshima H, Ueba T, Abe H, Tamiya T, Sonoda Y, Natsume A, Kakuma T, Sugita Y, Komatsu N, Yamada A, Sasada T, Matsueda S, Shichijo S, Itoh K, Terasaki M. A randomized, double-blind, phase Ⅲ trial of personalized peptide vaccination for recurrent glioblastoma[J]. Neuro Oncol, 2019, 21:348-359.
[36] Keskin DB, Anandappa AJ, Sun J, Tirosh I, Mathewson ND, Li S, Oliveira G, Giobbie-Hurder A, Felt K, Gjini E, Shukla SA, Hu Z, Li L, Le PM, Allesøe RL, Richman AR, Kowalczyk MS, Abdelrahman S, Geduldig JE, Charbonneau S, Pelton K, Iorgulescu JB, Elagina L, Zhang W, Olive O, McCluskey C, Olsen LR, Stevens J, Lane WJ, Salazar AM, Daley H, Wen PY, Chiocca EA, Harden M, Lennon NJ, Gabriel S, Getz G, Lander ES, Regev A, Ritz J, Neuberg D, Rodig SJ, Ligon KL, Suvà ML, Wucherpfennig KW, Hacohen N, Fritsch EF, Livak KJ, Ott PA, Wu CJ, Reardon DA. Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial[J]. Nature, 2019, 565:234-239.
[37] Hilf N, Kuttruff-Coqui S, Frenzel K, Bukur V, Stevanovic S, Gouttefangeas C, Platten M, Tabatabai G, Dutoit V, van der Burg SH, Thor Straten P, Martínez-Ricarte F, Ponsati B, Okada H, Lassen U, Admon A, Ottensmeier CH, Ulges A, Kreiter S, von Deimling A, Skardelly M, Migliorini D, Kroep JR, Idorn M, Rodon J, Piró J, Poulsen HS, Shraibman B, McCann K, Mendrzyk R, Löwer M, Stieglbauer M, Britten CM, Capper D, Welters MJP, Sahuquillo J, Kiesel K, Derhovanessian E, Rusch E, Bunse L, Song C, Heesch S, Wagner C, Kemmer-Brück A, Ludwig J, Castle JC, Schoor O, Tadmor AD, Green E, Fritsche J, Meyer M, Pawlowski N, Dorner S, Hoffgaard F, Rössler B, Maurer D, Weinschenk T, Reinhardt C, Huber C, Rammensee HG, Singh-Jasuja H, Sahin U, Dietrich PY, Wick W. Actively personalized vaccination trial for newly diagnosed glioblastoma[J]. Nature, 2019, 565:240-245.
[38] Lichty BD, Breitbach CJ, Stojdl DF, Bell JC. Going viral with cancer immunotherapy[J]. Nat Rev Cancer, 2014, 14:559-567.
[39] Martuza RL, Malick A, Markert JM, Ruffner KL, Coen DM. Experimental therapy of human glioma by means of a genetically engineered virus mutant[J]. Science, 1991, 252:854-856.
[40] Perez OD, Logg CR, Hiraoka K, Diago O, Burnett R, Inagaki A, Jolson D, Amundson K, Buckley T, Lohse D, Lin A, Burrascano C, Ibanez C, Kasahara N, Gruber HE, Jolly DJ. Design and selection of Toca 511 for clinical use:modified retroviral replicating vector with improved stability and gene expression[J]. Mol Ther, 2012, 20:1689-1698.
[41] Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A, Martin F, Apetoh L, Rébé C, Ghiringhelli F. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity[J]. Cancer Res, 2010, 70:3052-3061.
[42] Huber BE, Austin EA, Richards CA, Davis ST, Good SS. Metabolism of 5-fluorocytosine to 5-fluorouracil in human colorectal tumor cells transduced with the cytosine deaminase gene:significant antitumor effects when only a small percentage of tumor cells express cytosine deaminase[J]. Proc Nati Acad Sci USA, 1994, 91:8302-8306.
[43] Cloughesy TF, Landolfi J, Hogan DJ, Bloomfield S, Carter B, Chen CC, Elder JB, Kalkanis SN, Kesari S, Lai A, Lee IY, Liau LM, Mikkelsen T, Mikkelsen T, Nghiemphu PL, Piccioni D, Walbert T, Chu A, Das A, Diago OR, Gammon D, Gruber HE, Hanna M, Jolly DJ, Kasahara N, McCarthy D, Mitchell L, Ostertag D, Robbins JM, Rodriguez-Aguirre M, Vogelbaum MA. Phase 1 trial of vocimagene amiretrorepvec and 5-fluorocytosine for recurrent high-grade glioma[J]. Sci Transl Med, 2016, 8:341-375.
[44] Desjardins A, Gromeier M, Herndon JE 2nd, Beaubier N, Bolognesi DP, Friedman AH, Friedman HS, McSherry F, Muscat AM, Nair S, Peters KB, Randazzo D, Sampson JH, Vlahovic G, Harrison WT, McLendon RE, Ashley D, Bigner DD. Recurrent glioblastoma treated with recombinant poliovirus[J]. N Engl J Med, 2018, 379:150-161.
[45] Lawler SE, Speranza MC, Cho CF, Chiocca EA. Oncolytic viruses in cancer treatment:a review[J]. JAMA Oncol, 2017, 3:841-849.
[46] Felix J, Savvides SN. Mechanisms of immunomodulation by mammalian and viral decoy receptors:insights from structures[J]. Nat Rev Immunol, 2017, 17:112-129.
[47] McFadden G, Mohamed MR, Rahman MM, Bartee E. Cytokine determinants of viral tropism[J]. Nat Rev Immunol, 2009, 9:645-655.
[48] Prlic M, Williams MA, Bevan MJ. Requirements for CD8 T-cell priming, memory generation and maintenance[J]. Curr Opin Immunol, 2007, 19:315-319.
[49] Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS, Kim-Schulze S. Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage Ⅲc and Ⅳ melanoma[J]. Ann Surg Oncol, 2010, 17:718-730.
[50] Messina JL, Fenstermacher DA, Eschrich S, Qu X, Berglund AE, Lloyd MC, Schell MJ, Sondak VK, Weber JS, Mulé JJ. 12-Chemokine gene signature identifies lymph node-like structures in melanoma:potential for patient selection for immunotherapy[J]?Sci Rep, 2012, 2:765.
[51] Vestweber D. How leukocytes cross the vascular endothelium[J]. Nat Rev Immunol, 2015, 15:692-704.
[52] Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses:a new class of immunotherapy drugs[J]. Nat Rev Drug Discov, 2016, 15:660.
[53] Baril M, Es-Saad S, Chatel-Chaix L, Fink K, Pham T, Raymond VA, Audette K, Guenier AS, Duchaine J, Servant M, Bilodeau M, Cohen E, Grandvaux N, Lamarre D. Genome-wide RNAi screen reveals a new role of a WNT/CTNNB1 signaling pathway as negative regulator of virus-induced innate immune responses[J]. PLoS Pathog, 2013, 9:E1003416.
[54] Peng D, Kryczek I, Nagarsheth N, Zhao L, Wei S, Wang W, Sun Y, Zhao E, Vatan L, Szeliga W, Kotarski J, Tarkowski R, Dou Y, Cho K, Hensley-Alford S, Munkarah A, Liu R, Zou W. Epigenetic silencing of TH1-type chemokines shapes tumour immunity and immunotherapy[J]. Nature, 2015, 527:249-253.
[55] Mosser DM, Zhang X. Interleukin-10:new perspectives on an old cytokine[J]. Immunol Rev, 2008, 226:205-218.
[56] Munn DH, Mellor AL. Indoleamine 2, 3-dioxygenase and tumor-induced tolerance[J]. J Clin Invest, 2007, 117:1147-1154.
[57] Friberg M, Jennings R, Alsarraj M, Dessureault S, Cantor A, Extermann M, Mellor AL, Munn DH, Antonia SJ. Indoleamine 2, 3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection[J]. Int J Cancer, 2002, 101:151-155.
[58] Gabrilovich DI, Velders MP, Sotomayor EM, Kast WM. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+myeloid cells[J]. J Immunol, 2001, 166:5398-5406.
[59] Prestwich RJ, Errington F, Ilett EJ, Morgan RS, Scott KJ, Kottke T, Thompson J, Morrison EE, Harrington KJ, Pandha HS, Selby PJ, Vile RG, Melcher AA. Tumor infection by oncolytic reovirus primes adaptive antitumor immunity[J]. Clin Cancer Res, 2008, 14:7358-7366.
[60] Ilkow CS, Marguerie M, Batenchuk C, Mayer J, Ben Neriah D, Cousineau S, Falls T, Jennings VA, Boileau M, Bellamy D, Bastin D, de Souza CT, Alkayyal A, Zhang J, Le Boeuf F, Arulanandam R, Stubbert L, Sampath P, Thorne SH, Paramanthan P, Chatterjee A, Strieter RM, Burdick M, Addison CL, Stojdl DF, Atkins HL, Auer RC, Diallo JS, Lichty BD, Bell JC. Reciprocal cellular cross-talk within the tumor microenvironment promotes oncolytic virus activity[J]. Nat Med, 2015, 21:530-536.
[61] Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI, Michielin O, Olszanski AJ, Malvehy J, Cebon J, Fernandez E, Kirkwood JM, Gajewski TF, Chen L, Gorski KS, Anderson AA, Diede SJ, Lassman ME, Gansert J, Hodi FS, Long GV. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy[J]. Cell, 2017, 170:1109-1119.
[62] Puzanov I, Milhem MM, Minor D, Hamid O, Li A, Chen L, Chastain M, Gorski KS, Anderson A, Chou J, Kaufman HL, Andtbacka RH. Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage ⅢB-Ⅳ melanoma[J]. J Clin Oncol, 2016, 34:2619-2626.
[63] Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA, Rogers LJ, Gracia GJ, Jones SA, Mangiameli DP, Pelletier MM, Gea-Banacloche J, Robinson MR, Berman DM, Filie AC, Abati A, Rosenberg SA. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma[J]. J Clin Oncol, 2005, 23:2346-2357.
[64] Rosenberg SA, Restifo NP. Adoptive cell transfer as personalized immunotherapy for human cancer[J]. Science, 2015, 348:62-68.
[65] Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, Hershkovitz L, Levy D, Kubi A, Hovav E, Chermoshniuk N, Shalmon B, Hardan I, Catane R, Markel G, Apter S, Ben-Nun A, Kuchuk I, Shimoni A, Nagler A, Schachter J. Clinical responses in a phase Ⅱ study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients[J]. Clin Cancer Res, 2010, 16:2646-2655.
[66] Arulanandam R, Batenchuk C, Varette O, Zakaria C, Garcia V, Forbes NE, Davis C, Krishnan R, Karmacharya R, Cox J, Sinha A, Babawy A, Waite K, Weinstein E, Falls T, Chen A, Hamill J, De Silva N, Conrad DP, Atkins H, Garson K, Ilkow C, Kærn M, Vanderhyden B, Sonenberg N, Alain T, Le Boeuf F, Bell JC, Diallo JS. Microtubule disruption synergizes with oncolytic virotherapy by inhibiting interferon translation and potentiating bystander killing[J]. Nature Commun, 2015, 6:6410.
[67] Diallo JS, Le Boeuf F, Lai F, Cox J, Vaha-Koskela M, Abdelbary H, MacTavish H, Waite K, Falls T, Wang J, Brown R, Blanchard JE, Brown ED, Kirn DH, Hiscott J, Atkins H, Lichty BD, Bell JC. A high-throughput pharmacoviral approach identifies novel oncolytic virus sensitizers[J]. Mol Ther, 2010, 18:1123-1129.
[68] Gong J, Chehrazi-Raffle A, Reddi S, Salgia R. Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy:a comprehensive review of registration trials and future considerations[J]. J Immunother Cancer, 2018, 6:8.
[69] Bauer HC, Krizbai IA, Bauer H, Traweger A. "You Shall Not Pass":tight junctions of the blood brain barrier[J]. Front Neurosci, 2014, 8:392.
[70] Jackson CM, Lim M, Drake CG. Immunotherapy for brain cancer:recent progress and future promise[J]. Clin Cancer Res, 2014, 20:3651-3659.
[71] Reynold S. Nutrient transport systems in brain:40 years of progress[J]. J Neurochem, 2009, 111:315-320.
[72] Mesquita SD, Louveau A, Vaccari A, Smirnov I, Cornelison RC, Kingsmore KM, Contarino C, Onengut-Gumuscu S, Farber E, Raper D, Viar KE, Powell RD, Baker W, Dabhi N, Bai R, Cao R, Hu S, Rich SS, Munson JM, Lopes MB, Overall CC, Acton ST, Kipnis J. Functional aspects of meningeal lymphatics in ageing and Alzheimer's disease[J]. Nature, 2018, 560:185-191.
[73] Han S, Zhang C, Li Q, Dong J, Liu Y, Huang Y, Jiang T, Wu A. Tumour-infiltrating CD4(+) and CD8(+) lymphocytes as predictors of clinical outcome in glioma[J]. Br J Cancer, 2014, 110:2560-2568.
[74] Zeng J, See AP, Phallen J, Jackson CM, Belcaid Z, Ruzevick J, Durham N, Meyer C, Harris TJ, Albesiano E, Pradilla G, Ford E, Wong J, Hammers HJ, Mathios D, Tyler B, Brem H, Tran PT, Pardoll D, Drake CG, Lim M. Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas[J]. Int J Radiat Oncol Biol Phys, 2013, 86:343-349.
[75] Mitchell DA, Batich KA, Gunn MD, Huang MN, Sanchez-Perez L, Nair SK, Congdon KL, Reap EA, Archer GE, Desjardins A, Friedman AH, Friedman HS, Herndon JE 2nd, Coan A, McLendon RE, Reardon DA, Vredenburgh JJ, Bigner DD, Sampson JH. Tetanus toxoid and CCL improve dendritic cell vaccines in mice and glioblastoma patients[J]. Nature, 2015, 519:366-369.
[76] Weiss T, Weller M, Guckenberger M, Sentman CL, Roth P. NKG2D-based CAR-T cells and radiotherapy exert synergistic efficacy in glioblastoma[J]. Cancer Res, 2018, 78:1031-1043.
[77] Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, Alexe G, Lawrence M, O'Kelly M, Tamayo P, Weir BA, Gabriel S, Winckler W, Gupta S, Jakkula L, Feiler HS, Hodgson JG, James CD, Sarkaria JN, Brennan C, Kahn A, Spellman PT, Wilson RK, Speed TP, Gray JW, Meyerson M, Getz G, Perou CM, Hayes DN; Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1[J]. Cancer Cell, 2010, 17:98-110.
[78] Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers[J]. Nature, 2012, 489:519-525.
[79] Grossman SA, Ye X, Lesser G, Sloan A, Carraway H, Desideri S, Piantadosi S; NABTT CNS Consortium. Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide[J]. Clin Cancer Res, 2011, 17:5473-5480.
[80] Mathios D, Kim JE, Mangraviti A, Phallen J, Park CK, Jackson CM, Garzon-Muvdi T, Kim E, Theodros D, Polanczyk M, Martin AM, Suk I, Ye X, Tyler B, Bettegowda C, Brem H, Pardoll DM, Lim M. Anti-PD-1 antitumor immunity is enhanced by local and abrogated by systemic chemotherapy in GBM[J]. Sci Transl Med, 2016, 8:370ar180.
[81] Maxwell R, Luksik AS, Garzon-Muvdi T, Hung AL, Kim ES, Wu A, Xia Y, Belcaid Z, Gorelick N, Choi J, Theodros D, Jackson CM, Mathios D, Ye X, Tran PT, Redmond KJ, Brem H, Pardoll DM, Kleinberg LR, Lim M. Contrasting impact of corticosteroids on anti-PD-1 immunotherapy efficacy for tumor histologies located within or outside the central nervous system[J]. Oncoimmunology, 2018, 7:E1500108.
[82] Giles AJ, Hutchinson MKND, Sonnemann HM, Jung J, Fecci PE, Ratnam NM, Zhang W, Song H, Bailey R, Davis D, Reid CM, Park DM, Gilbert MR. Dexamethasone-induced immunosuppression:mechanisms and implications for immunotherapy[J]. J Immunother, 2018, 6:51.
[83] Woroniecka K, Chongsathidkiet P, Rhodin KE, Kemeny H, Dechant C, Farber SH, Elsamadicy AA, Cui X, Koyama S, Jackson C, Hansen LJ, Johanns TM, Sanchez-Perez L,Chandramohan V, Yu YA, Bigner DD, Giles A, Healy P, Dranoff G, Weinhold KJ, Dunn GP, Fecci PE. T-cell exhaustion signatures vary with tumor type and are severe in glioblastoma[J]. Clin Cancer Res, 2018, 24:4175-4186.

Please choose a citation manager

Content to export