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Review

Immune infiltration of tumor microenvironment following immunotherapy for glioblastoma multiforme

ORCID Icon, &
Pages 2575-2582 | Received 05 Oct 2016, Accepted 03 Mar 2017, Published online: 24 Oct 2017

References

  • Stupp R, Mason WP, Van Den Bent Martin J, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–96. doi:10.1056/NEJMoa043330. PMID:15758009
  • MacCarty WC. Factors which influence longevity in cancer. Ann Surg. 1922;76(1):9–12; PMID:17864672
  • Wade H. Of its relationship to cancer. J Pathol Bacteriol. 1908;12:384. doi:10.1002/path.1700120221
  • Hamlin IM. Possible host resistance in carcinoma of the breast: A histological study. Br J Cancer. 1968;22(3):383–401. doi:10.1038/bjc.1968.47. PMID:5681002
  • Husby G, Hoagland PM, Strickland RG, Williams RC, Jr. Tissue T and B cell infiltration of primary and metastatic cancer. J Clin Invest. 1976;57(6):1471–1482. doi:10.1172/JCI108417. PMID:180052
  • Bertrand I, Mannen H. Etude des reactions vasculaires dans les astrocytomes. Rev Neurol. 1960;102:3–19
  • Palma L, Di Lorenzo N, Guidetti B. Lymphocytic infiltrates in primary glioblastomas and recidivous gliomas: Incidence, fate, and relevance to prognosis in 228 operated cases. J Neurosurg. 1978;49(6):854–61. doi:10.3171/jns.1978.49.6.0854. PMID:731302
  • Goldmann J, Kwidzinski E, Brandt C, Mahlo J, Richter D, Bechmann I. T cells traffic from brain to cervical lymph nodes via the cribroid plate and the nasal mucosa. J Leukoc Biol. 2006;80(4):797–801. doi:10.1189/jlb.0306176. PMID:16885505
  • Polyzoidis S, Tuazon J, Brazil L, Beaney R, Al-Sarraj ST, Doey L, Logan J, Hurwitz V, Jarosz J, Bhangoo R, et al. Active dendritic cell immunotherapy for glioblastoma: Current status and challenges. Br J Neurosurg. 2015;29(2):197–205. doi:10.3109/02688697.2014.994473. PMID:25541743
  • Ochs K, Sahm F, Opitz CA, Lanz TV, Oezen I, Couraud PO, von Deimling A, Wick W, Platten M. Immature mesenchymal stem cell-like pericytes as mediators of immunosuppression in human malignant glioma. J Neuroimmunol. 2013;265(1):106–16. doi:10.1016/j.jneuroim.2013.09.011. PMID:24090655
  • Sims JS, Ung TH, Neira JA, Canoll P, Bruce JN. Biomarkers for glioma immunotherapy: The next generation. J Neurooncol. 2015;123(3):359–72
  • Smyth MJ, Godfrey DI, Trapani JA. A fresh look at tumor immunosurveillance and immunotherapy. Nat Immunol. 2001;2(4):293–99. doi:10.1038/86297. PMID:11276199
  • Sampson JH, Archer GE, Ashley DM, Fuchs HE, Hale LP, Dranoff G, Bigner DD. Subcutaneous vaccination with irradiated, cytokine-producing tumor cells stimulates CD8+ cell-mediated immunity against tumors located in the “immunologically privileged” central nervous system. Proc Natl Acad Sci U S A. 1996;93(19):10399–404. doi:10.1073/pnas.93.19.10399. PMID:8816812
  • Liau LM, Black KL, Prins RM, Sykes SN, DiPatre PL, Cloughesy TF, Becker DP, Bronstein JM. Treatment of intracranial gliomas with bone marrow-derived dendritic cells pulsed with tumor antigens. J Neurosurg. 1999;90(6):1115–24. doi:10.3171/jns.1999.90.6.1115. PMID:10350260
  • Broder H, Anderson A, Kremen TJ, Odesa SK, Liau LM. MART-1 adenovirus-transduced dendritic cell immunization in a murine model of metastatic central nervous system tumor. J Neurooncol. 2003;64(1-2):21–30. doi:10.1007/BF02700017. PMID:12952283
  • Siesjö P, Visse E, Sjögren HO. Cure of established, intracerebral rat gliomas induced by therapeutic immunizations with tumor cells and purified APC or adjuvant IFN-U03B3 treatment. Journal of Immunotherapy. 1996;19(5):334–45. doi:10.1097/00002371-199609000-00003. PMID:8941873
  • Hsu FJ, Benike C, Fagnoni F, Liles TM, Czerwinski D, Taidi B, Engleman EG, Levy R. Vaccination of patients with b–cell lymphoma using autologous antigen–pulsed dendritic cells. Nat Med. 1996;2(1):52–8. doi:10.1038/nm0196-52. PMID:8564842
  • Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, Dummer R, Burg G, Schadendorf D. Vaccination of melanoma patients with peptide-or tumorlysate-pulsed dendritic cells. Nat Med. 1998;4(3):328–32. doi:10.1038/nm0398-328. PMID:9500607
  • Tjoa B, Simmons S, Bowes V, Ragde H, Rogers M, Elgamal A, Kenny GM, Cobb OE, Ireton RC, Troychak MJ, et al. Evaluation of phase I/II clinical trials in prostate cancer with dendritic cells and PSMA peptides. Prostate. 1998;36(1):39–44. doi:10.1002/(SICI)1097-0045(19980615)36:1%3c39::AID-PROS6%3e3.0.CO;2-6. PMID:9650914
  • Kugler A, Stuhler G, Walden P, Zöller G, Zobywalski A, Brossart P, Trefzer U, Ullrich S, Müller CA, Becker V, Gross AJ, Hemmerlein B, Kanz L, Muller GA, Ringert R-H. Regression of human metastatic renal cell carcinoma after vaccination with tumor cell–dendritic cell hybrids. Nat Med. 2000;6(3):332–36. doi:10.1038/73193. PMID:10700237
  • Sabado RL, Bhardwaj N. Dendritic cell immunotherapy. Ann N Y Acad Sci. 2013;1284(1):31–45. doi:10.1111/nyas.12125. PMID:23651191
  • Liau LM, Prins RM, Kiertscher SM, Odesa SK, Kremen TJ, Giovannone AJ, Lin JW, Chute DJ, Mischel PS, Cloughesy TF, Roth MD. Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res. 2005;11(15):5515–25. doi:10.1158/1078-0432.CCR-05-0464. PMID:16061868
  • Yamanaka R, Homma J, Yajima N, Tsuchiya N, Sano M, Kobayashi T, Yoshida S, Abe T, Narita M, Takahashi M, Tanaka R. Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: Results of a clinical phase I/II trial. Clin Cancer Res. 2005;11(11):4160–67. doi:10.1158/1078-0432.CCR-05-0120. PMID:15930352
  • Chang C, Huang Y, Yang D, Kikuta K, Wei KJ, Kubota T, Yang WK. A phase I/II clinical trial investigating the adverse and therapeutic effects of a postoperative autologous dendritic cell tumor vaccine in patients with malignant glioma. J Clin Neurosci. 2011;18(8):1048–54. doi:10.1016/j.jocn.2010.11.034. PMID:21715171
  • Yu JS, Liu G, Ying H, Yong WH, Black KL, Wheeler CJ. Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res. 2004;64(14):4973–79. doi:10.1158/0008-5472.CAN-03-3505. PMID:15256471
  • Prins RM, Soto H, Konkankit V, Odesa SK, Eskin A, Yong WH, Nelson SF, Liau LM. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res. 2011;17(6):1603–15. doi:10.1158/1078-0432.CCR-10-2563. PMID:21135147
  • Walker DG, Laherty R, Tomlinson FH, Chuah T, Schmidt C. Results of a phase I dendritic cell vaccine trial for malignant astrocytoma: Potential interaction with adjuvant chemotherapy. J Clin Neurosci. 2008;15(2):114–21. doi:10.1016/j.jocn.2007.08.007. PMID:18083572
  • Steiner HH, Bonsanto MM, Beckhove P, Brysch M, Geletneky K, Ahmadi R, Schuele-Freyer R, Kremer P, Ranaie G, Matejic D, et al. Antitumor vaccination of patients with glioblastoma multiforme: A pilot study to assess feasibility, safety, and clinical benefit. J Clin Oncol. 2004;22(21):4272–81. doi:10.1200/JCO.2004.09.038. PMID:15452186
  • Liau LM, Jensen ER, Kremen TJ, Odesa SK, Sykes SN, Soung MC, Miller JF, Bronstein JM. Tumor immunity within the central nervous system stimulated by recombinant listeria monocytogenes vaccination. Cancer Res. 2002;62(8):2287–93; PMID:11956085
  • Yamanaka R, Homma J, Yajima N, Tsutiya N, Takahashi M, Tanaka R. Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: Results of a clinical phase I/II trial. Cancer Res. 2004;64(7 Supplement):283–283
  • Clark WH, Jr, Elder DE, Guerry D, 4th, Braitman LE, Trock BJ, Schultz D, Synnestvedt M, Halpern AC. Model predicting survival in stage I melanoma based on tumor progression. J Natl Cancer Inst. 1989;81(24):1893–904. doi:10.1093/jnci/81.24.1893. PMID:2593166
  • Clemente CG, Mihm MC, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer. 1996;77(7):1303–10. doi:10.1002/(SICI)1097-0142(19960401)77:7%3c1303::AID-CNCR12%3e3.0.CO;2-5. PMID:8608507
  • Mihm MC, Jr, Clemente CG, Cascinelli N. Tumor infiltrating lymphocytes in lymph node melanoma metastases: A histopathologic prognostic indicator and an expression of local immune response. Lab Invest. 1996;74(1):43–7; PMID:8569196
  • Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004;10(9):942–949. doi:10.1038/nm1093. PMID:15322536
  • Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, Rubin SC, Coukos G. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003;348(3):203–13. doi:10.1056/NEJMoa020177. PMID:12529460
  • Naito Y, Saito K, Shiiba K, Ohuchi A, Saigenji K, Nagura H, Ohtani H. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res. 1998;58(16):3491–94; PMID:9721846
  • Walker DG, Chuah T, Rist MJ, Pender MP. T-cell apoptosis in human glioblastoma multiforme: Implications for immunotherapy. J Neuroimmunol. 2006;175(1):59–68. doi:10.1016/j.jneuroim.2006.03.006. PMID:16631933
  • Yang I, Tihan T, Han SJ, Wrensch MR, Wiencke J, Sughrue ME, Parsa AT. CD8 T-cell infiltrate in newly diagnosed glioblastoma is associated with long-term survival. J Clin Neurosci. 2010;17(11):1381–5. doi:10.1016/j.jocn.2010.03.031. PMID:20727764
  • Boker DK, Kalff R, Gullotta F, Weekes-Seifert S, Mohrer U. Mononuclear infiltrates in human intracranial tumors as a prognostic factor. influence of preoperative steroid treatment. I. glioblastoma. Clin Neuropathol. 1984;3(4):143–7; PMID:6478676
  • Brooks W, Markesbery W, Gupta G, Roszman T. Relationship of lymphocyte invasion and survival of brain tumor patients. Ann Neurol. 1978;4(3):219–24. doi:10.1002/ana.410040305. PMID:718133
  • Safdari H, Hochberg FH, Richardson EP. Prognostic value of round cell (lymphocyte) infiltration in malignant gliomas. Surg Neurol. 1985;23(3):221–26. doi:10.1016/0090-3019(85)90086-2. PMID:2983448
  • Rossi M, Jones N, Candy E, Nicoll JA, Compton JS, Hughes JT, Esiri MM, Moss TH, Cruz-Sanchez FF, Coakham HB. The mononuclear cell infiltrate compared with survival in high-grade astrocytomas. Acta Neuropathol. 1989;78(2):189–93. doi:10.1007/BF00688208. PMID:2750489
  • Schiffer D, Cavicchioli D, Giordana MT, Palmucci L, Piazza A. Analysis of some factors effecting survival in malignant gliomas. Tumori. 1979;65(1):119–25; PMID:220763
  • Authier A, Farrand KJ, Broadley KW, Ancelet LR, Hunn MK, Stone S, McConnell MJ, Hermans IF. Enhanced immunosuppression by therapy‐exposed glioblastoma multiforme tumor cells. Int J Cancer. 2015;136(11):2566–78. doi:10.1002/ijc.29309. PMID:25363661
  • Yu JS, Wheeler CJ, Zeltzer PM, Ying H, Finger DN, Lee PK, Yong WH, Incardona F, Thompson RC, Riedinger MS, et al. Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res. 2001;61(3):842–7; PMID:11221866
  • Yang Y, Lu J, Liu H, Jin G, Bai R, Li X, Wang D, Zhao J, Huang Y, Liu K, et al. Dendritic cells loading autologous tumor lysate promote tumor angiogenesis. Tumor Biol. 2016;37(12):15687–95
  • Hsu M, Sedighim S, Wang T, Antonios JP, Everson RG, Tucker AM, Du L, Emerson R, Yusko E, Sanders C, et al. TCR sequencing can identify and track glioma-infiltrating T cells after DC vaccination. Cancer Immunol Res. 2016;4(5):412–8.
  • Everson RG, Jin RM, Wang X, Safaee M, Scharnweber R, Lisiero DN, Soto H, Liau LM, Prins RM. Cytokine responsiveness of CD8 T cells is a reproducible biomarker for the clinical efficacy of dendritic cell vaccination in glioblastoma patients. J Immunother Cancer. 2014;2(1):1. doi:10.1186/2051-1426-2-10. PMID:24829758
  • Kamran N, Calinescu A, Candolfi M, Chandran M, Mineharu Y, Asad AS, Koschmann C, Nunez FJ, Lowenstein PR, Castro MG. Recent advances and future of immunotherapy for glioblastoma. Expert Opin Biol Ther. 2016;16(10):1245–64. doi:10.1080/14712598.2016.1212012. PMID:27411023
  • Libard S, Popova SN, Amini R, Kärjä V, Pietiläinen T, Hämäläinen KM, Sundström C, Hesselager G, Bergqvist M, Ekman S, et al. Human cytomegalovirus tegument protein pp65 is detected in all intra-and extra-axial brain tumours independent of the tumour type or grade. PloS one. 2014;9(9):e108861. doi:10.1371/journal.pone.0108861. PMID:25268364
  • Shamran HA, Kadhim HS, Hussain AR, Kareem A, Taub DD, Price RL, Nagarkatti M, Nagarkatti PS, Singh UP. Detection of human cytomegalovirus in different histopathological types of glioma in iraqi patients. BioMed Res Int. 2015;2015:642652

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