Evasion of the Immune System by Glioblastoma Multiforme: An Obstacle to Achieving Effective Therapies

Kevin Johanes Kawengian, Septelia Inawati Wanandi

Abstract


Glioblastoma multiforme (GBM), a highly aggressive and malignant form of brain cancer, continues to pose a significant challenge in the field of oncology. Despite ongoing advancements in treatment strategies, the prognosis for GBM patients remains grim, with a 5-year survival rate hovering around 5%. The management of GBM involves multiple therapeutic approaches, including immunotherapy, but optimal treatment outcomes in terms of overcoming tumor recurrence and resistance have not been achieved. A key factor contributing to therapy resistance and the progression of GBM is the tumor's ability to evade the immune system, referred to as immune escape from cancer. This phenomenon reflects the tumor cells' efforts to adapt and survive the body's immune response. The release and expression of molecules like TGF-ß, IL-10, PD-L1, and NKG2DL by GBM cells impact the activation, recognition, and elimination of tumor cells by the immune system. Additionally, the involvement of cells such as MDSCs, Tregs, and TAMs plays a role in inhibiting the immune system's function, thereby promoting the development of GBM cells. A better comprehension of GBM's immune escape, supported by technological advances, will significantly aid in the future management of GBM patients' treatment.

Keywords: glioblastoma multiforme, GBM, cancer immunity, immune evasion, immune escape, immunotherapy


Full Text:

PDF

References


National Foundation For Cancer Research [Internet]; ©2023. What is GBM? [cited 2024 Jan 22]. Available from: https://www.nfcr.org/.

World Health Organization [Internet]; ©2024. Cancer [updated 2022 Feb 3; cited 2024 Jan 22]. Available from: https://www.who.int/.

Grech N, Dalli T, Mizzi S, Meilak L, Calleja N, Zrinzo A. Rising incidence of glioblastoma multiforme in a well-defined population. Cureus. 2020; 12(5): e8195, CrossRef.

Young RM, Jamshidi A, Davis G, Sherman JH. Current trends in the surgical management and treatment of adult glioblastoma. Ann Transl Med. 2015; 3(9): 121, CrossRef.

Daubon T, Hemadou A, Romero Garmendia I, Saleh M. Glioblastoma immune landscape and the potential of new immunotherapies. Front Immunol. 2020; 11: 585616, CrossRef.

Ramirez YP, Weatherbee JL, Wheelhouse RT, Ross AH. Glioblastoma multiforme therapy and mechanisms of resistance. Pharmaceuticals. 2013; 6(12): 1475-506, CrossRef.

Lee EQ, Wen PY. Corticosteroids for peritumoral edema: Time to overcome our addiction? Neuro Oncol. 2016; 18(9): 1191-2, CrossRef.

Sengupta S, Marrinan J, Frishman C, Sampath P. Impact of temozolomide on immune response during malignant glioma chemotherapy. Clin Dev Immunol. 2012; 2012: 831090, CrossRef.

Grossman SA, Ye X, Lesser G, Sloan A, Carraway H, Desideri S, et al. Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin Cancer Res. 2011; 17(16): 5473-80, CrossRef.

Hadjipanayis CG, Stummer W. 5-ALA and FDA approval for glioma surgery. J Neurooncol. 2019; 141(3): 479-86, CrossRef.

Sener U, Ruff MW, Campian JL. Immunotherapy in glioblastoma: Current approaches and future perspectives. Int J Mol Sci. 2022; 23(13): 7046, CrossRef.

Pearson JRD, Cuzzubbo S, McArthur S, Durrant LG, Adhikaree J, Tinsley CJ, et al. Immune escape in glioblastoma multiforme and the adaptation of immunotherapies for treatment. Front Immunol. 2020; 11: 582106, CrossRef.

Mitra R, Singh S, Khar A. Antitumour immune responses. Expert Rev Mol Med. 2003; 5(3): 1-19, CrossRef.

Li Y, Liu X, Zhang X, Pan W, Li N, Tang B. Immune cycle-based strategies for cancer immunotherapy. Adv Funct Mater. 2021; 31(50): 2107540, CrossRef.

Engelhardt B, Ransohoff RM. Capture, crawl, cross: The T cell code to breach the blood-brain barriers. Trends Immunol. 2012; 33(12): 579-89, CrossRef.

Pachter JS, de Vries HE, Fabry Z. The blood-brain barrier and its role in immune privilege in the central nervous system. J Neuropathol Exp Neurol. 2003; 62(6): 593-604, CrossRef.

Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010; 37(1): 13-25, CrossRef.

McArthur S, Loiola RA, Maggioli E, Errede M, Virgintino D, Solito E. The restorative role of annexin A1 at the blood-brain barrier. Fluids Barriers CNS. 2016; 13(1): 17, CrossRef.

Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. Angiogenesis in brain tumours. Nat Rev Neurosci. 2007; 8(8): 610-22, CrossRef.

Anderson JC, McFarland BC, Gladson CL. New molecular targets in angiogenic vessels of glioblastoma tumours. Expert Rev Mol Med. 2008; 10: e23, CrossRef.

Henderson JT, Piquette-Miller M. Blood-brain barrier: An impediment to neuropharmaceuticals. Clin Pharmacol Ther. 2015; 97(4): 308-13, CrossRef.

Chaudhury A, Howe PH. The tale of transforming growth factor-beta (TGFβ) signaling: A soigné enigma. IUBMB Life. 2009; 61(10): 929-39, CrossRef.

Sánchez-Capelo A. Dual role for TGF-β1 in apoptosis. Cytokine Growth Factor Rev. 2005; 16(1): 15-34, CrossRef.

Alexandrow MG, Moses HL. Transforming growth factor β1 inhibits mouse keratinocytes late in G1 independent of effects on gene transcription. Cancer Res. 1995; 55(17): 3928-32, CrossRef.

Dang CV. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol. 1999; 19(1): 1-11, CrossRef.

Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci U S A. 1995; 92(12): 5545-9, CrossRef.

Xu J, Lamouille S, Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 2009; 19(2): 156-72, CrossRef.

Wang X, Eichhorn PJA, Thiery JP. TGF-β, EMT, and resistance to anti-cancer treatment. Semin Cancer Biol. 2023; 97: 1-11, CrossRef.

Pratiwi SE, Wahyuningrum SN, Putri RP, Danarto, Heriyanto DS, Arfian N, et al. ZEB1 is negatively correlated with E-cadherin in prostatic anomaly tissue. Mol Cell Biomed Sci. 2022; 6(1): 28-34, CrossRef.

Tsubakihara Y, Ohata Y, Okita Y, Younis S, Eriksson J, Sellin ME, et al. TGFβ selects for pro-stemness over pro-invasive phenotypes during cancer cell epithelial-mesenchymal transition. Mol Oncol. 2022; 16(12): 2330-54, CrossRef.

Orzan F, De Bacco F, Crisafulli G, Pellegatta S, Mussolin B, Siravegna G, et al. Genetic evolution of glioblastoma stem-like cells from primary to recurrent tumor. Stem Cells. 2017; 35(11): 2218-28, CrossRef.

Sabat R, Grütz G, Warszawska K, Kirsch S, Witte E, Wolk K, et al. Biology of interleukin-10. Cytokine Growth Factor Rev. 2010; 21(5): 331-44,

Iyer SS, Cheng G. Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Crit Rev Immunol. 2012; 32(1): 23-63, CrossRef.

Conrad ML, Renz H, Blaser K. Immunological approaches for tolerance induction in allergy. Curr Top Microbiol Immunol. 2011; 352: 1-26, CrossRef.

Lohr J, Ratliff T, Huppertz A, Ge Y, Dictus C, Ahmadi R, et al. Effector T-cell infiltration positively impacts survival of glioblastoma patients and is impaired by tumor-derived TGF-β. Clin Cancer Res. 2011; 17(13): 4296-308, CrossRef.

Platten M, Wick W, Weller M. Malignant glioma biology: Role for TGF-β in growth, motility, angiogenesis, and immune escape. Microsc Res Tech. 2001; 52(4): 401-10, CrossRef.

Huettner C, Paulus W, Roggendorf W. Messenger RNA expression of the immunosuppressive cytokine IL-10 in human gliomas. Am J Pathol. 1995; 146(2): 317-22, article.

Sonabend AM, Rolle CE, Lesniak MS. The role of regulatory T cells in malignant glioma. Anticancer Res. 2008; 28(2B): 1143-50, article.

Wagner S, Czub S, Greif M, Vince GH, Süss N, Kerkau S, et al. Microglial/macrophage expression of interleukin 10 in human glioblastomas. Int J Cancer. 1999; 82(1): 12-6, CrossRef.

Sánchez-Zauco N, Torres J, Gómez A, Camorlinga-Ponce M, Muñoz-Pérez L, Herrera-Goepfert R, et al. Circulating blood levels of IL-6, IFN-γ, and IL-10 as potential diagnostic biomarkers in gastric cancer: A controlled study. BMC Cancer. 2017; 17(1): 384, CrossRef.

Al Azhar MA, Nadliroh S, Prameswari K, Handoko, Tobing DL, Herawati C. Profile of PD-1 and PD-L1 mRNA expression in peripheral blood of nasopharyngeal carcinoma. Mol Cell Biomed Sci. 2020; 4(3): 121-7, CrossRef.

Han Y, Liu D, Li L. PD-1/PD-L1 pathway: Current researches in cancer. Am J Cancer Res. 2020; 10(3): 727-42, article.

Wu Q, Jiang L, Li SC, He QJ, Yang B, Cao J. Small molecule inhibitors targeting the PD-1/PD-L1 signaling pathway. Acta Pharmacol Sin. 2021; 42(1): 1-9, CrossRef.

Arneth B. Tumor microenvironment. Medicina. 2019; 56(1): 15, CrossRef.

Poggio M, Hu T, Pai CC, Chu B, Belair CD, Chang A, et al. Suppression of exosomal PD-L1 induces systemic anti-tumor immunity and memory. Cell. 2019; 177(2): 414-27.e13, CrossRef.

Berghoff AS, Kiesel B, Widhalm G, Rajky O, Ricken G, Wöhrer A, et al. Programmed death ligand 1 expression and tumor-infiltrating lymphocytes in glioblastoma. Neuro Oncol. 2015; 17(8): 1064-75, CrossRef.

Nduom EK, Wei J, Yaghi NK, Huang N, Kong LY, Gabrusiewicz K, et al. PD-L1 expression and prognostic impact in glioblastoma. Neuro Oncol. 2016; 18(2): 195-205, CrossRef.

Xue S, Song G, Yu J. The prognostic significance of PD-L1 expression in patients with glioma: A meta-analysis. Sci Rep. 2017; 7(1): 4231, CrossRef.

Hao C, Chen G, Zhao H, Li Y, Chen J, Zhang H, et al. PD-L1 expression in glioblastoma, the clinical and prognostic significance: A systematic literature review and meta-analysis. Front Oncol. 2020; 10: 1015, CrossRef.

Omuro A, Vlahovic G, Lim M, Sahebjam S, Baehring J, Cloughesy T, et al. Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: Results from exploratory phase I cohorts of CheckMate 143. Neuro Oncol. 2018; 20(5): 674-86, CrossRef.

Shi P, Xu J, Cui H. The recent research progress of NF-κB signaling on the proliferation, migration, invasion, immune escape and drug resistance of glioblastoma. Int J Mol Sci. 2023; 24(12): 10337, CrossRef.

Qiu XY, Hu DX, Chen WQ, Chen RQ, Qian SR, Li CY, et al. PD-L1 confers glioblastoma multiforme malignancy via Ras binding and Ras/Erk/EMT activation. Biochim Biophys Acta Mol Basis Dis. 2018; 1864(5 Pt A): 1754-69, CrossRef.

Zingoni A, Molfetta R, Fionda C, Soriani A, Paolini R, Cippitelli M, et al. NKG2D and its ligands: "One for all, all for one". Front Immunol. 2018; 9: 476, CrossRef.

Siemaszko J, Marzec-Przyszlak A, Bogunia-Kubik K. NKG2D natural killer cell receptor-A short description and potential clinical applications. Cells. 2021; 10(6): 1420, CrossRef.

Liu H, Wang S, Xin J, Wang J, Yao C, Zhang Z. Role of NKG2D and its ligands in cancer immunotherapy. Am J Cancer Res. 2019; 9(10): 2064-78, article.

Duan S, Guo W, Xu Z, He Y, Liang C, Mo Y, et al. Natural killer group 2D receptor and its ligands in cancer immune escape. Mol Cancer. 2019; 18(1): 29, CrossRef.

Zingoni A, Vulpis E, Cecere F, Amendola MG, Fuerst D, Saribekyan T, et al. MICA-129 dimorphism and soluble mica are associated with the progression of multiple myeloma. Front Immunol. 2018; 9: 926, CrossRef.

Zhang Y, Hu R, Xi B, Nie D, Xu H, Liu A. Mechanisms of senescence-related NKG2D ligands release and immune escape induced by chemotherapy in neuroblastoma cells. Front Cell Dev Biol. 2022; 10: 829404, CrossRef.

Weiss T, Schneider H, Silginer M, Steinle A, Pruschy M, Polić B, et al. NKG2D-dependent antitumor effects of chemotherapy and radiotherapy against glioblastoma. Clin Cancer Res. 2018; 24(4): 882-95, CrossRef.

Zhong J, Yang X, Chen J, He K, Gao X, Wu X, et al. Circular EZH2-encoded EZH2-92aa mediates immune evasion in glioblastoma via inhibition of surface NKG2D ligands. Nat Commun. 2022; 13(1): 4795, CrossRef.

Codo P, Weller M, Meister G, Szabo E, Steinle A, Wolter M, et al. MicroRNA-mediated down-regulation of NKG2D ligands contributes to glioma immune escape. Oncotarget. 2014; 5(17): 7651-62, CrossRef.

Eisele G, Wischhusen J, Mittelbronn M, Meyermann R, Waldhauer I, Steinle A, et al. TGF-β and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain. 2006; 129(Pt 9): 2416-25, CrossRef.

Huang T, Wan X, Alvarez AA, James CD, Song X, Yang Y, et al. MIR93 (microRNA -93) regulates tumorigenicity and therapy response of glioblastoma by targeting autophagy. Autophagy. 2019; 15(6): 1100-11, CrossRef.

Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009; 9(3): 162-74, CrossRef.

Rodríguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: Mechanisms and therapeutic perspectives. Immunol Rev. 2008; 222: 180-91, CrossRef.

Nagaraj S, Gabrilovich DI. Myeloid-derived suppressor cells. Adv Exp Med Biol. 2007; 601: 213-23, CrossRef.

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(6): 2148-57, CrossRef.

Ostrand-Rosenberg S. Myeloid-derived suppressor cells: More mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother. 2010; 59(10): 1593-600, CrossRef.

Li ZL, Ye SB, OuYang LY, Zhang H, Chen YS, He J, et al. COX-2 promotes metastasis in nasopharyngeal carcinoma by mediating interactions between cancer cells and myeloid-derived suppressor cells. Oncoimmunology. 2015; 4(11): e1044712, CrossRef.

Kamran N, Kadiyala P, Saxena M, Candolfi M, Li Y, Moreno-Ayala MA, et al. Immunosuppressive myeloid cells' blockade in the glioma microenvironment enhances the efficacy of immune-stimulatory gene therapy. Mol Ther. 2017; 25(1): 232-48, CrossRef.

Chen Z, Hambardzumyan D. Immune microenvironment in glioblastoma subtypes. Front Immunol. 2018; 9: 1004, CrossRef.

Schlecker E, Stojanovic A, Eisen C, Quack C, Falk CS, Umansky V, et al. Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth. J Immunol. 2012; 189(12): 5602-11, CrossRef.

Maloy KJ, Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol. 2001; 2(9): 816-22, CrossRef.

Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, Itoh M, et al. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: Their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev. 2001; 182: 18-32, CrossRef.

Scheipers P, Reiser H. Role of the CTLA-4 receptor in T cell activation and immunity. Physiologic function of the CTLA-4 receptor. Immunol Res. 1998; 18(2): 103-15, CrossRef.

Pae HO, Oh GS, Choi BM, Chae SC, Chung HT. Differential expressions of heme oxygenase-1 gene in CD25- and CD25+ subsets of human CD4+ T cells. Biochem Biophys Res Commun. 2003; 306(3): 701-5, CrossRef.

Thornton AM, Shevach EM. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med. 1998; 188(2): 287-96, CrossRef.

Câmara NO, Sebille F, Lechler RI. Human CD4+CD25+ regulatory cells have marked and sustained effects on CD8+ T cell activation. Eur J Immunol. 2003; 33(12): 3473-83, CrossRef.

Cantini G, Pisati F, Mastropietro A, Frattini V, Iwakura Y, Finocchiaro G, 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(12): 1739-50, CrossRef.

El Andaloussi A, Lesniak MS. An increase in CD4+CD25+FOXP3+ regulatory T cells in tumor-infiltrating lymphocytes of human glioblastoma multiforme. Neuro Oncol. 2006; 8(3): 234-43, CrossRef.

Caponegro MD, Miyauchi JT, Tsirka SE. Contributions of immune cell populations in the maintenance, progression, and therapeutic modalities of glioma. AIMS Allergy Immunol. 2018; 2(1): 24-44, CrossRef.

Jacobs JF, Idema AJ, Bol KF, Grotenhuis JA, de Vries IJ, Wesseling P, et al. Prognostic significance and mechanism of Treg infiltration in human brain tumors. J Neuroimmunol. 2010; 225(1-2): 195-9, CrossRef.

Ben-Shoshan J, Maysel-Auslender S, Mor A, Keren G, George J. Hypoxia controls CD4+CD25+ regulatory T-cell homeostasis via hypoxia-inducible factor-1alpha. Eur J Immunol. 2008; 38(9): 2412-8, CrossRef.

Wang J, Yao L, Zhao S, Zhang X, Yin J, Zhang Y, et al. Granulocyte-colony stimulating factor promotes proliferation, migration and invasion in glioma cells. Cancer Biol Ther. 2012; 13(6): 389-400, CrossRef.

Zhang J, Sarkar S, Cua R, Zhou Y, Hader W, Yong VW. A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis. Carcinogenesis. 2012; 33(2): 312-9, CrossRef.

Le Mercier M, Fortin S, Mathieu V, Kiss R, Lefranc F. Galectins and gliomas. Brain Pathol. 2010; 20(1): 17-27, CrossRef.

Ridley A, Cavanagh JB. Lymphocytic infiltration in gliomas: Evidence of possible host resistance. Brain. 1971; 94(1): 117-24, CrossRef.

Hitchcock ER, Morris CS. Mononuclear cell infiltration in central portions of human astrocytomas. J Neurosurg. 1988; 68(3): 432-7, CrossRef.

Zhou W, Bao S. Reciprocal supportive interplay between glioblastoma and tumor-associated macrophages. Cancers. 2014; 6(2): 723-40, CrossRef.

Deininger MH, Seid K, Engel S, Meyermann R, Schluesener HJ. Allograft inflammatory factor-1 defines a distinct subset of infiltrating macrophages/microglial cells in rat and human gliomas. Acta Neuropathol. 2000; 100(6): 673-80, CrossRef.

Leenstra S, Das PK, Troost D, de Boer OJ, Bosch DA. Human malignant astrocytes express macrophage phenotype. J Neuroimmunol. 1995; 56(1): 17-25, CrossRef.

Nagarsheth N, Wicha MS, Zou W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat Rev Immunol. 2017; 17(9): 559-72, CrossRef.

Gao H, Zhang IY, Zhang L, Song Y, Liu S, Ren H, et al. S100B suppression alters polarization of infiltrating myeloid-derived cells in gliomas and inhibits tumor growth. Cancer Lett. 2018; 439: 91-100, CrossRef.

Yin J, Kim SS, Choi E, Oh YT, Lin W, Kim TH, et al. ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages. Nat Commun. 2020; 11(1): 2978, CrossRef.

Huang BR, Liu YS, Lai SW, Lin HJ, Shen CK, Yang LY, et al. CAIX Regulates GBM Motility and TAM adhesion and polarization through EGFR/STAT3 under hypoxic conditions. Int J Mol Sci. 2020; 21(16): 5838, CrossRef.

Jiang Y, Zhan H. Communication between EMT and PD-L1 signaling: New insights into tumor immune evasion. Cancer Lett. 2020; 468: 72-81, CrossRef.

Liu X, Liu Y, Qi Y, Huang Y, Hu F, Dong F, et al. Signal pathways involved in the interaction between tumor-associated macrophages/TAMs and glioblastoma cells. Front Oncol. 2022; 12: 822085, CrossRef.

Carvalho JADV, Barbosa CCL, Feher O, Maldaun MVC, Camargo VP, Moraes FY, et al. Systemic dissemination of glioblastoma: Literature review. Rev Assoc Med Bras. 2019; 65(3): 460-8, CrossRef.

Pardridge WM. CSF, blood-brain barrier, and brain drug delivery. Expert Opin Drug Deliv. 2016; 13(7): 963-75, CrossRef.

Rizk ML, Zou L, Savic RM, Dooley KE. Importance of drug pharmacokinetics at the site of action. Clin Transl Sci. 2017; 10(3): 133-42, CrossRef.

Rapoport SI. Effect of concentrated solutions on blood-brain barrier. Am J Physiol. 1970; 219(1): 270-4, CrossRef.

Raymond JJ, Robertson DM, Dinsdale HB. Pharmacological modification of bradykinin induced breakdown of the blood-brain barrier. Can J Neurol Sci. 1986; 13(3): 214-20, CrossRef.

Hynynen K, McDannold N, Sheikov NA, Jolesz FA, Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage. 2005; 24(1): 12-20, CrossRef.

Kung Y, Huang HY, Liao WH, Huang AP, Hsiao MY, Wu CH, et al. A single high-intensity shock wave pulse with microbubbles opens the blood-brain barrier in rats. Front Bioeng Biotechnol. 2020; 8: 402, CrossRef.

Meng J, Agrahari V, Youm I. Advances in targeted drug delivery approaches for the central nervous system tumors: The inspiration of nanobiotechnology. J Neuroimmune Pharmacol. 2017; 12(1): 84-98, CrossRef.

Zhang B, Wang H, Liao Z, Wang Y, Hu Y, Yang J, et al. EGFP-EGF1-conjugated nanoparticles for targeting both neovascular and glioma cells in therapy of brain glioma. Biomaterials. 2014; 35(13): 4133-45, CrossRef.

Yu YJ, Atwal JK, Zhang Y, Tong RK, Wildsmith KR, Tan C, et al. Therapeutic bispecific antibodies cross the blood-brain barrier in nonhuman primates. Sci Transl Med. 2014; 6(261): 261ra154, CrossRef.

Galstyan A, Markman JL, Shatalova ES, Chiechi A, Korman AJ, Patil R, et al. Blood-brain barrier permeable nano immunoconjugates induce local immune responses for glioma therapy. Nat Commun. 2019; 10(1): 3850, CrossRef.

Bogdahn U, Hau P, Stockhammer G, Venkataramana NK, Mahapatra AK, Suri A, et al. Targeted therapy for high-grade glioma with the TGF-β2 inhibitor trabedersen: Results of a randomized and controlled phase IIb study. Neuro Oncol. 2011; 13(1): 132-42, CrossRef.

Soares KC, Rucki AA, Kim V, Foley K, Solt S, Wolfgang CL, et al. TGF-β blockade depletes T regulatory cells from metastatic pancreatic tumors in a vaccine dependent manner. Oncotarget. 2015; 6(40): 43005-15, CrossRef.

Wolchok JD, Chiarion-Sileni V, Gonzalez R, Rutkowski P, Grob JJ, Cowey CL, et al. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2017; 377(14): 1345-56, CrossRef.

Herbst RS, Baas P, Kim DW, Felip E, Pérez-Gracia JL, Han JY, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): A randomised controlled trial. Lancet. 2016; 387(10027): 1540-1550, CrossRef.

Horn L, Mansfield AS, Szczęsna A, Havel L, Krzakowski M, Hochmair MJ, et al. First-line atezolizumab plus chemotherapy in extensive-stage small-cell lung cancer. N Engl J Med. 2018; 379(23): 2220-9, CrossRef.

Yang T, Kong Z, Ma W. PD-1/PD-L1 immune checkpoint inhibitors in glioblastoma: Clinical studies, challenges and potential. Hum Vaccin Immunother. 2021; 17(2): 546-53, CrossRef.

Berghoff AS, Preusser M. Does neoadjuvant anti-PD1 therapy improve glioblastoma outcome? Nat Rev Neurol. 2019; 15(6): 314-5, CrossRef.

Schalper KA, Rodriguez-Ruiz ME, Diez-Valle R, López-Janeiro A, Porciuncula A, Idoate MA, et al. Neoadjuvant nivolumab modifies the tumor immune microenvironment in resectable glioblastoma. Nat Med. 2019; 25(3): 470-6, CrossRef.

Dai B, Qi N, Li J, Zhang G. Temozolomide combined with PD-1 Antibody therapy for mouse orthotopic glioma model. Biochem Biophys Res Commun. 2018; 501(4): 871-6, CrossRef.

Zeng J, See AP, Phallen J, Jackson CM, Belcaid Z, Ruzevick J, et al. Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas. Int J Radiat Oncol Biol Phys. 2013; 86(2): 343-9, CrossRef.

Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, et al. Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol. 2010; 28(31): 4722-9, CrossRef.

Migliorini D, Dutoit V, Allard M, Grandjean Hallez N, Marinari E, Widmer V, et al. Phase I/II trial testing safety and immunogenicity of the multipeptide IMA950/poly-ICLC vaccine in newly diagnosed adult malignant astrocytoma patients. Neuro Oncol. 2019; 21(7): 923-33, CrossRef.

Migliorini D, Dietrich PY, Stupp R, Linette GP, Posey AD Jr, June CH. CAR T-cell therapies in glioblastoma: A first look. Clin Cancer Res. 2018; 24(3): 535-40, CrossRef.

Suryadevara CM, Desai R, Abel ML, Riccione KA, Batich KA, Shen SH, et al. Temozolomide lymphodepletion enhances CAR abundance and correlates with antitumor efficacy against established glioblastoma. Oncoimmunology. 2018; 7(6): e1434464, CrossRef.

Weiss T, Weller M, Guckenberger M, Sentman CL, Roth P. NKG2D-based CAR T cells and radiotherapy exert synergistic efficacy in glioblastoma. Cancer Res. 2018; 78(4): 1031-43, CrossRef.




DOI: https://doi.org/10.21705/mcbs.v8i2.434

Copyright (c) 2024 Cell and BioPharmaceutical Institute

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Indexed by:

               

                      


Cell and BioPharmaceutical Institute