Immunotherapy for human glioma: innovative approaches and recent results

References

• Paul W. The Immune System. An Introduction. Third Edition. Raven Press, NY, USA (1993).
   Google Scholar
• Hsieh CS, Heimberger AB, Gold JS, O’Garra A, Murphy KM. Differential regulation of T-helper phenotype development by interleukins 4 and 10 in an α β T-cell-receptor transgenic system. Proc. Natl Acad. Sci. USA 89(13), 6065–6069 (1992).
   PubMed Web of Science ®Google Scholar
• Murphy JB, Sturm E. Conditions determining the transplantability of tissues in the brain. J. Exp. Med. 38, 183–197 (1923).
   PubMedGoogle Scholar
• Medawar PB. Immunity to homologous grafted skin. III. The fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. Br. J. Exp. Pathol. 29, 58–69 (1948).
   PubMed Web of Science ®Google Scholar
• Schackert HK, Itaya T, Schackert G, Fearon E, Vogelstein B, Frost P. Systemic immunity against a murine colon tumor (CT-26) produced by immunization with syngeneic cells expressing a transfected viral gene product. Int. J. Cancer 43(5), 823–827 (1989).
   PubMedGoogle Scholar
• Kida Y, Cravioto H, Hochwald GM, Hochgeschwender U, Ransohoff J. Immunity to transplantable nitrosourea-induced neurogenic tumors. II. Immunoprophylaxis of tumors of the brain. J. Neuropathol. Exp. Neurol. 42(2), 122–135 (1983).
   PubMedGoogle Scholar
• Mitchell MS. Relapse in the central nervous system in melanoma patients successfully treated with biomodulators. J. Clin. Oncol. 7(11), 1701–1709 (1989).
   PubMed Web of Science ®Google Scholar
• Yamada S, DePasquale M, Patlak CS, Cserr HF. Albumin outflow into deep cervical lymph from different regions of rabbit brain. Am. J. Physiol. 261(4 Pt 2), H1197–H1204 (1991).
   PubMed Web of Science ®Google Scholar
• Bradbury M, Westrop R. Factors influencing exit of substances from cerebrospinal fluid into deep cervical lymph of the rabbit. J. Physiol. 339, 519–534 (1983).
   PubMed Web of Science ®Google Scholar
• Cserr HF, DePasquale M, Harling-Berg CJ, Park JT, Knopf PM. Afferent and efferent arms of the humoral immune response to CSF- administered albumins in a rat model with normal blood-brain barrier permeability. J. Neuroimmunol. 41(2), 195–202 (1992).
   PubMed Web of Science ®Google Scholar
• Ni HT, Merica RR, Spellman SR, Wang JM, Low WC. Visualization of antigen-specific T-cell activation in vivo in response to intracerebral administration of a xenopeptide. Exp. Neurol. 164(2), 362–370 (2000).
   PubMed Web of Science ®Google Scholar
• Lampson LA, Hickey WF. Monoclonal antibody analysis of MHC expression in human brain biopsies: tissue ranging from ‘histologically normal’ to that showing different levels of glial tumor involvement. J. Immunol. 136(11), 4054–4062 (1986).
   PubMedGoogle Scholar
• Wong GH, Bartlett PF, Clark-Lewis I, Battye F, Schrader JW. Inducible expression of H-2 and Ia antigens on brain cells. Nature 310(5979), 688–691 (1984).
   PubMed Web of Science ®Google Scholar
• Massa PT, Ozato K, McFarlin DE. Cell type-specific regulation of major histocompatibility complex (MHC) class I gene expression in astrocytes, oligodendrocytes, and neurons. Glia 8(3), 201–207 (1993).
   PubMedGoogle Scholar
• Mattiace LA, Davies P, Dickson DW. Detection of HLA-DR on microglia in the human brain is a function of both clinical and technical factors. Am. J. Pathol. 136(5), 1101–1114 (1990).
   PubMed Web of Science ®Google Scholar
• McMenamin PG, Forrester JV. Dendritic Cells in the Central Nervous System and Eye and their Associated Supporting Tissues (Volume 1). Academic Press, NY, USA (1999).
   Google Scholar
• Williams K Jr, Ulvestad E, Cragg L, Blain M, Antel JP. Induction of primary T-cell responses by human glial cells. J. Neurosci. Res. 36(4), 382–390 (1993).
   PubMed Web of Science ®Google Scholar
• Williams K, Ulvestad E, Antel JP. B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur. J. Immunol. 24(12), 3031–3037 (1994).
   PubMedGoogle Scholar
• Serot J, Foliguet B, Bene M, Faure G. Ultrastructural and immunohistochemical evidence for dendritic-like cells within the human choroid plexus epithelium. Neuroreport 8(8), 1995–1998 (1997).
   PubMedGoogle Scholar
• Greter M, Heppner FL, Lemos MP et al. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nature Med. 11(3), 328–334 (2005).
   PubMed Web of Science ®Google Scholar
• McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nature Med. 11(3), 335–339 (2005).
   PubMed Web of Science ®Google Scholar
• Plautz GE, Mukai S, Cohen PA, Shu S. Cross-presentation of tumor antigens to effector T-cells is sufficient to mediate effective immunotherapy of established intracranial tumors. J. Immunol. 165(7), 3656–3662 (2000).
   PubMedGoogle Scholar
• Calzascia T, Di Berardino-Besson W, Wilmotte R et al. Cutting edge: cross-presentation as a mechanism for efficient recruitment of tumor-specific CTL to the brain. J. Immunol. 171(5), 2187–2191 (2003).
   PubMedGoogle Scholar
• Calzascia T, Masson F, Di Berardino-Besson W et al. Homing phenotypes of tumor-specific CD8 T-cells are predetermined at the tumor site by crosspresenting APCs. Immunity 22(2), 175–184 (2005).
   PubMed Web of Science ®Google Scholar
• Chaux P, Favre N, Martin M, Martin F. Tumor-infiltrating dendritic cells are defective in their antigen-presenting function and inducible B7 expression in rats. Int. J. Cancer 72(4), 619–624 (1997).
   PubMed Web of Science ®Google Scholar
• Ulvestad E, Williams K, Bjerkvig R, Tiekotter K, Antel J, Matre R. Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. J. Leukoc. Biol. 56(6), 732–740 (1994).
   PubMed Web of Science ®Google Scholar
• Thomas W. Brain macrophages: evaluation of microglia and their functions. Brain Res. Brain Res. Rev. 17(1), 61–74 (1992).
   PubMedGoogle Scholar
• Banati R, Graeber M. Surveillance, intervention and cytotoxicity: is there a protective role of microglia? Dev. Neurosci. 16(3,4), 114–127 (1994).
   PubMedGoogle Scholar
• Yao J, Harvath L, Gilbert D, Colton C. Chemotaxis by a CNS macrophage, the microglia. J. Neurosci. Res. 27(1), 36–42 (1990).
   PubMed Web of Science ®Google Scholar
• Pfeiffer S, Gooding R, Apperley J, Goldschmidt H, Samson D. Dendritic cells generated from the blood of patients with multiple myeloma are phenotypically and functionally identical to those similarly produced from healthy donors. Br. J. Haematol. 98(4), 973–982 (1997).
   PubMed Web of Science ®Google Scholar
• Radmayr C, Bock G, Hobisch A, GKlocker H, Bartsch G, Thurnher M. Dendritic antigen-presenting cells from the peripheral blood of renal-cell-carcinoma patients. Int. J. Cancer 63(5), 627–632 (1995).
   PubMedGoogle Scholar
• Archer GE, Bigner DD, Friedman AH, Heimberger AB, Sampson J. Induction of CD4 and CD8 T-cells to the tumor specific antigen EGFRvIII. 15th International Conference on Brain Tumor Research and Therapy. Society for Neuro-Oncology, Sorrento, Italy (2003).
   Google Scholar
• Hauser SL, Bhan AK, Gilles FH et al. Immunohistochemical staining of human brain with monoclonal antibodies that identify lymphocytes, monocytes, and the Ia antigen. J. Neuroimmunol. 5(2), 197–205 (1983).
   PubMedGoogle Scholar
• Hickey WF, Kimura H. Graft versus host disease elicits expression of class I and class II histocompatibility antigens and the presence of scattered T-lymphocytes in rat central nervous system. Proc. Natl Acad. Sci. USA 84(7), 2082–2086 (1987).
   PubMedGoogle Scholar
• Paterson PY, Day ED. Current perspectives of neuroimmunologic disease: multiple sclerosis and experimental allergic encephalomyelitis. [Review]. Clin. Immunol. Rev. 1(4), 581–697 (1981).
   PubMedGoogle Scholar
• Hickey WF, Hsu BL, Kimura H. T-lymphocyte entry into the central nervous system. J. Neurosci. Res. 28(2), 254–260 (1991).
   PubMed Web of Science ®Google Scholar
• Borrow P, Cornell JL, Ruppe MD, Mucke L. Immunization-induced inflammatory infiltration of the central nervous system in transgenic mice expressing a microbial antigen in astrocytes. J. Neuroimmunol. 61(2), 133–149 (1995).
   PubMedGoogle Scholar
• Brabb T, von Dassow P, Ordonez N, Schnabel B, Duke B, Goverman J. In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity. J. Exp. Med. 192(6), 871–880 (2000).
   PubMed Web of Science ®Google Scholar
• Krakowski ML, Owens T. Naive T-lymphocytes traffic to inflamed central nervous system, but require antigen recognition for activation. Eur. J. Immunol. 30, 1002–1009 (2000).
   Google Scholar
• Walker PR, Calzascia T, Schnuriger V et al. The brain parenchyma is permissive for full antitumor CTL effector function, even in the absence of CD4 T-cells. J. Immunol. 165(6), 3128–3135 (2000).
   PubMed Web of Science ®Google Scholar
• von Hanwehr RI, Hofman FM, Taylor CR, Apuzzo ML. Mononuclear lymphoid populations infiltrating the microenvironment of primary CNS tumors. Characterization of cell subsets with monoclonal antibodies. J. Neurosurg. 60(6), 1138–1147 (1984).
   PubMedGoogle Scholar
• 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. 49(6), 854–861 (1978).
   PubMedGoogle Scholar
• Brooks WH, Markesbery WR, Gupta GD, Roszman TL. Relationship of lymphocyte invasion and survival of brain tumor patients. Ann. Neurol. 4(3), 219–224 (1978).
   PubMed Web of Science ®Google Scholar
• Safdari H, Hochberg F, Richardson E. Prognostic value of round cell (lymphocyte) infiltration in malignant gliomas. Surg. Neurol. 23(3), 221–226 (1985).
   PubMedGoogle Scholar
• Heimberger AB, Crotty LE, Archer GE et al. Epidermal growth factor receptor VIII peptide vaccination is efficacious against established intracerebral tumors. Clin. Cancer Res. 9, 4247–4254 (2003).
   PubMed Web of Science ®Google Scholar
• Sampson JH, Archer GE, Ashley DM et al. 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. USA 93(19), 10399–10404 (1996).
   PubMed Web of Science ®Google Scholar
• Wheeler CJ, Black KL, Liu G et al. Thymic CD8+ T-cell production strongly influences tumor antigen recognition and age-dependent glioma mortality. J. Immunol. 171(9), 4927–4933 (2003).
   PubMed Web of Science ®Google Scholar
• Sampson JH, Crotty LE, Lee S et al. Unarmed, tumor-specific, monoclonal antibody effectively treats brain tumors. Proc. Natl. Acad. Sci. USA 97(13), 7503–7508 (2000).
   PubMed Web of Science ®Google Scholar
• Graf MR, Prins RM, Merchant RE. IL-6 secretion by a rat T9 glioma clone induces a neutrophil-dependent antitumor response with resultant cellular, antiglioma immunity. J. Immunol. 166(1), 121–129 (2001).
   PubMed Web of Science ®Google Scholar
• Sandberg-Wollheim M, Zweiman B, Levinson A, Lisak R. Humoral immune responses within the human central nervous system following systemic immunization. J. Neuroimmunol. 11(3), 205–214 (1986).
   PubMedGoogle Scholar
• Bernheimer H, Lassmann H, Suchanek G. Dynamics of IgG+, IgA+, and IgM+ plasma cells in the central nervous system of guinea-pigs with chronic relapsing experimental allergic encephalomyelitis. Neuropathol. Appl. Neurobiol. 14(2), 157–167 (1988).
   PubMedGoogle Scholar
• Dan M, Schlachta C, Guy J et al. Human antiglioma monoclonal antibodies from patients with astrocytic tumors. J. Neurosurg. 76(4), 660–669 (1992).
   PubMed Web of Science ®Google Scholar
• Levi-Strauss M, Mallat M. Primary cultures of murine astrocytes produce C3 and factor B, two components of the alternative pathway of complement activation. J. Immunol. 139(7), 2361–2366 (1987).
   PubMed Web of Science ®Google Scholar
• Roszman TL, Brooks WH, Elliott LH. Inhibition of lymphocyte responsiveness by a glial tumor cell- derived suppressive factor. J. Neurosurg. 67(6), 874–879 (1987).
   PubMed Web of Science ®Google Scholar
• Bodmer S, Strommer K, Frei K et al. Immunosuppression and transforming growth factor-β in glioblastoma. Preferential production of transforming growth factor-β 2. J. Immunol. 143(10), 3222–3229 (1989).
   PubMed Web of Science ®Google Scholar
• Elliott LH, Brooks WH, Roszman TL. Suppression of high affinity IL-2 receptors on mitogen activated lymphocytes by glioma-derived suppressor factor. J. Neurooncol. 14(1), 1–7 (1992).
   PubMedGoogle Scholar
• Hishii M, Nitta T, Ishida H et al. Human glioma-derived interleukin-10 inhibits antitumor immune responses in vitro. Neurosurgery 37(6), 1160–1167 (1995).
   PubMed Web of Science ®Google Scholar
• Alleva DG, Burger CJ, Elgert KD. Tumor-induced regulation of suppressor macrophage nitric oxide and TNF-α production. Role of tumor-derived IL-10, TGF-beta, and prostaglandin E2. J. Immunol. 153(4), 1674–1686 (1994).
   PubMed Web of Science ®Google Scholar
• Sawamura Y, Diserens AC, de Tribolet N. In vitro prostaglandin E2 production by glioblastoma cells and its effect on interleukin-2 activation of oncolytic lymphocytes. J. Neurooncol. 9(2), 125–130 (1990).
   PubMed Web of Science ®Google Scholar
• Samuels V, Barrett J, Bockman S, Pantazis C, Allen M. Immunocytochemical study of transforming growth factor expression in benign and malignant gliomas. Am. J. Pathol. 134(4), 894–902 (1989).
   PubMed Web of Science ®Google Scholar
• Kuppner M, Hamou M, Sawamura Y, Bodmer S, deTribolet N. Inhibition of lymphocyte function by glioblastoma-derived transforming growth factor-β2. J. Neurosurg. 71(2), 211–217 (1989).
   PubMed Web of Science ®Google Scholar
• Roszman T, Elliott L, Brooks W. Modulation of T-cell function by gliomas. Immunol. Today 12(10), 370–374 (1991).
   PubMedGoogle Scholar
• Zou JP, Morford LA, Chougnet C et al. Human glioma-induced immunosuppression involves soluble factor(s) that alters monocyte cytokine profile and surface markers. J. Immunol. 162(8), 4882–4892 (1999).
   PubMed Web of Science ®Google Scholar
• Fakhrai H, Dorigo O, Shawler DL et al. Eradication of established intracranial rat gliomas by transforming growth factor β antisense gene therapy. Proc. Natl Acad. Sci. USA 93(7), 2909–2914 (1996).
   PubMed Web of Science ®Google Scholar
• Liau LM, Fakhrai H, Black KL. Prolonged survival of rats with intracranial C6 gliomas by treatment with TGF-β antisense gene. Neurol. Res. 20(8), 742–747 (1998).
   PubMed Web of Science ®Google Scholar
• Fakhrai H, Gramatikova S, Safaei R. Downregulation of transforming growth factor B as therapeutic approach for brain tumors. In: Brain Tumor Immunotherapy. Liau LM, Becker DP, Cloughesy TF, Bigner DD (Eds). Humana Press Inc., Totowa, NJ, USA, 289–305 (2001).
   Google Scholar
• Prins RM, Incardona F, Lau R et al. Characterization of defective CD4-CD8 T-cells in murine tumors generated independent of antigen specificity. J. Immunol. 172(3), 1602–1611 (2004).
   PubMedGoogle Scholar
• Prins RM, Scott GP, Merchant RE, Graf MR. Irradiated tumor cell vaccine for treatment of an established glioma. II. Expansion of myeloid suppressor cells that promote tumor progression. Cancer Immunol. Immunother. 51(4), 190–199 (2002).
   PubMed Web of Science ®Google Scholar
• Barshes NR, Goodpastor SE, Goss JA. Pharmacologic immunosuppression. Front. Biosci. 9, 411–420 (2004).
   PubMed Web of Science ®Google Scholar
• Su YB, Sohn S, Krown SE et al. Selective CD4+ lymphopenia in melanoma patients treated with temozolomide: A toxicity with therapeutic implications. J. Clin. Oncol. 22(4), 610–616 (2004).
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason WP, van den Bent MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352(10), 987–996 (2005).
   PubMed Web of Science ®Google Scholar
• Bloom HJ, Peckham MJ, Richardson AE, Alexander PA, Payne PM. Glioblastoma multiforme: a controlled trial to assess the value of specific active immunotherapy in patients treated by radical surgery and radiotherapy. Br. J. Cancer 27(3), 253–267 (1973).
   PubMed Web of Science ®Google Scholar
• Trouillas P. Immunology and immunotherapy of cerebral tumors. Current status. Rev. Neurol. (Paris) 128(1), 23–38 (1973).
   PubMed Web of Science ®Google Scholar
• Wikstrand CJ, Bigner DD. Hyperimmunization of non-human primates with BCG-CW and cultured human glioma-derived cells. J. Neuroimmunol. 1(3), 249–260 (1981).
   PubMedGoogle Scholar
• Shapiro JR, Yung WK, Shapiro WR. Isolation, karyotype, and clonal growth of heterogeneous subpopulations of human malignant gliomas. Cancer Res. 41(6), 2349–2359 (1981).
   PubMedGoogle Scholar
• Fogel M, Gorelik E, Segal S, Feldman M. Differences in cell surface antigens of tumor metastases and those of the local tumor. J. Natl Cancer Inst. 62(3), 585–588 (1979).
   PubMedGoogle Scholar
• Bigner DD, Schold C, Bigner SH, Bullard DE, Wikstrand C. How heterogeneous are gliomas? Cancer Treat. Rep. 65(Suppl. 2), 45–49 (1981).
   PubMedGoogle Scholar
• Bigner DD, Bigner SH, Ponten J et al. Heterogeneity of genotypic and phenotypic characteristics of fifteen permanent cell lines derived from human gliomas. J. Neuropathol. Exp. Neurol. 40(3), 201–229 (1981).
   PubMed Web of Science ®Google Scholar
• Bigner SH, Batra SK, Rasheed A. Mechanisms of altered growth control. Cytogenetics, oncogenes and suppressor genes. In: Russell and Rubinstein’s Pathology of Tumors of the Nervous System. (Volume 6). Bigner DD, McLendon RE, Bruner JM (Eds). Oxford University Press, NY, USA 47 (1998).
   Google Scholar
• Kleihues P, Burger PC, Plate KH, Ohgaki H, Cavenee WK. Astrocytic tumors. In: Pathology and Genetics: Tumors of the Nervous System. (Volume 1). Kleihues P, Cavenee WJ (Eds). International Agency for Research on Cancer, Lyon, France (1997).
   Google Scholar
• Kurpad SN, Zhao XG, Wikstrand CJ, Batra SK, McLendon RE, Bigner DD. Tumor antigens in astrocytic gliomas. Glia 15(3), 244–256 (1995).
   PubMed Web of Science ®Google Scholar
• Nitta T, Sato K, Yagita H, Okumura K, Ishii S. Preliminary trial of specific targeting therapy against malignant glioma. Lancet 335(8686), 368–371 (1990).
   PubMed Web of Science ®Google Scholar
• Plautz GE, Miller DW, Barnett GH et al. T-cell adoptive immunotherapy of newly diagnosed gliomas. Clin. Cancer Res. 6(6), 2209–2218 (2000).
   PubMed Web of Science ®Google Scholar
• Hayes RL, Koslow M, Hiesiger EM et al. Improved long-term survival after intracavitary interleukin-2 and lymphokine-activated killer cells for adults with recurrent malignant glioma. Cancer 76(5), 840–852 (1995).
   PubMed Web of Science ®Google Scholar
• Kikuchi T, Akasaki Y, Irie M, Homma S, Abe T, Ohno T. Results of Phase I clinical trial of vaccination of glioma patients with fusions of dendritic and glioma cells. Cancer Immunol. Immunother. 50(7), 337–344 (2001).
   PubMed Web of Science ®Google Scholar
• Kikuchi T, Akasaki Y, Abe T et al. Vaccination of glioma patients with fusions of dendritic and glioma cells and recombinant human interleukin-12. J. Immunother. 27(6), 452–459 (2004).
   PubMed Web of Science ®Google Scholar
• Yu J, Wheeler C, Zeltzer P et al. Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res. 61(3), 842–847 (2001).
   PubMed Web of Science ®Google Scholar
• Yu J, Liu G, Ying H, Yong W, Black K, Wheeler CJ. Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res. 64(14), 4973–4979 (2004).
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Hlatky R, Suki D et al. Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin. Cancer Res. 11(4), 1462–1466 (2005).
   PubMed Web of Science ®Google Scholar
• Cobbs C, Harkins L, Samanta M et al. Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res. 62(12), 3347–3350 (2002).
   PubMed Web of Science ®Google Scholar
• Yamanaka R, Abe T, Yajima N et al. Vaccination of recurrent glioma patients with tumor lysate-pulsed dendritic cells elicits immune responses: Results of a clinical Phase I/II trial. Br. J. Cancer 89(7), 1172–1179 (2003).
   PubMed Web of Science ®Google Scholar
• Wheeler CJ, Das A, Liu G, Yu J, Black K. Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination. Clin. Cancer Res. 10(16), 5316–5326 (2004).
   PubMed Web of Science ®Google Scholar
• Cokgor I, Akabani G, Kuan CT et al. Phase I trial results of iodine-131-labeled antitenascin monoclonal antibody 81C6 treatment of patients with newly diagnosed malignant gliomas. J. Clin. Oncol. 18(22), 3862–3872 (2000).
   PubMed Web of Science ®Google Scholar
• Reardon DA, Akabani G, Coleman RE et al. Phase II trial of murine (131)I-labeled antitenascin monoclonal antibody 81C6 administered into surgically created resection cavities of patients with newly diagnosed malignant gliomas. J. Clin. Oncol. 20(5), 1389–1397 (2002).
   PubMed Web of Science ®Google Scholar
• Stragliotto G, Vega F, Stasiecki P, Gropp P, Poisson M, Delattre J. Multiple infusions of anti-epidermal growth factor receptor (EGFR) monoclonal antibody (EMD 55,900) in patients with recurrent malignant gliomas. Eur. J. Cancer 32A(4), 636–640 (1996).
   PubMed Web of Science ®Google Scholar
• Salazar AM, Levy HB, Ondra S et al. Long-term treatment of malignant gliomas with intramuscularly administered polyinosinic-polycytidylic acid stabillized with polylysine and carboxymethylcellulose: an open pilot study. Neurosurgery 38(6), 1096–1194 (1996).
   PubMed Web of Science ®Google Scholar
• Lozupone F, Rivoltini L, Luciani F et al. Adoptive transfer of an antiMART-1(27–35)-specific CD8+ T-cell clone leads to immunoselection of human melanoma antigen-loss variants in SCID mice. Eur. J. Immunol. 33(2), 556–566 (2003).
   PubMed Web of Science ®Google Scholar
• Sanchez-Perez L, Kottke T, Diaz RM et al. Potent selection of antigen loss variants of B16 melanoma following inflammatory killing of melanocytes in vivo. Cancer Res. 65(5), 2009–2017 (2005).
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Yang JC, Robbins PF et al. Cell transfer therapy for cancer: lessons from sequential treatments of a patient with metastatic melanoma. J. Immunother. 26(5), 385–393 (2003).
   PubMed Web of Science ®Google Scholar
• Restifo NP, Marincola FM, Kawakami Y, Taubenberger J, Yannelli JR, Rosenberg SA. Loss of functional beta 2-microglobulin in metastatic melanomas from five patients receiving immunotherapy. J. Natl Cancer Inst. 88(2), 100–108 (1996).
   PubMed Web of Science ®Google Scholar
• Wintterle S, Schreiner B, Mitsdoerffer M et al. Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis. Cancer Res. 63(21), 7462–7467 (2003).
   PubMed Web of Science ®Google Scholar
• Wiendl H, Mitsdoerffer M, Hofmeister V et al. A functional role of HLA-G expression in human gliomas: an alternative strategy of immune escape. J. Immunol. 168(9), 4772–4780 (2002).
   PubMed Web of Science ®Google Scholar
• Akasaki Y, Liu G, Chung NH, Ehtesham M, Black KL, Yu JS. Induction of a CD4+ T regulatory Type 1 response by cyclooxygenase-2-overexpressing glioma. J. Immunol. 173(7), 4352–4359 (2004).
   PubMed Web of Science ®Google Scholar
• Kuppner MC, Hamou MF, de Tribolet N. Immunohistological and functional analyses of lymphoid infiltrates in human glioblastomas. Cancer Res. 48(23), 6926–6932 (1988).
   PubMed Web of Science ®Google Scholar
• Naganuma H, Sasaki A, Satoh E et al. Transforming growth factor-beta inhibits interferon-gamma secretion by lymphokine-activated killer cells stimulated with tumor cells. Neurol. Med. Chir. 36(11), 789–795 (1996).
   PubMedGoogle Scholar
• Ashkenazi E, Deutsch M, Tirosh R, Weinreb A, Tsukerman A, Brodie C. A selective impairment of the IL-2 system in lymphocytes of patients with glioblastomas: increased level of soluble IL-2R and reduced protein tyrosine phosphorylation. Neuroimmunomodulation 4(1), 49–56 (1997).
   PubMed Web of Science ®Google Scholar
• Roussel E, Gingras MC, Grimm EA, Bruner JM, Moser RP. Predominance of a Type 2 intratumoural immune response in fresh tumour-infiltrating lymphocytes from human gliomas. Clin. Exp. Immunol. 105(2), 344–352 (1996).
   PubMedGoogle Scholar
• Yu JS, Lee PK, Ehtesham M, Samoto K, Black KL, Wheeler CJ. Intratumoral T-cell subset ratios and Fas ligand expression on brain tumor endothelium. J. Neurooncol. 64(1–2), 55–61 (2003).
   PubMed Web of Science ®Google Scholar
• Morford LA, Dix AR, Brooks WH, Roszman TL. Apoptotic elimination of peripheral T-lymphocytes in patients with primary intracranial tumors. J. Neurosurg. 91(6), 935–946 (1999).
   PubMed Web of Science ®Google Scholar
• Kuppner MC, Sawamura Y, Hamou MF, de Tribolet N. Influence of PGE2- and cAMP-modulating agents on human glioblastoma cell killing by interleukin-2-activated lymphocytes. J. Neurosurg. 72(4), 619–625 (1990).
   PubMed Web of Science ®Google Scholar
• Takano T, Lin JH, Arcuino G, Gao Q, Yang J, Nedergaard M. Glutamate release promotes growth of malignant gliomas. Nature Med. 7(9), 1010–1015 (2001).
   PubMed Web of Science ®Google Scholar