Blocking the PD-1/PD-L1 pathway in glioma: A potential new treatment strategy

Journal of Hematology and Oncology

Volumn 10, Issue 1, 2017, Pages

  Xue, Song ^a,b   Hu, Man ^b,c   Iyer, Veena ^d   Yu, Jinming ^b,c  

^a UNIVERSITY OF JINAN   (China)

^b SHANDONG CANCER HOSPITAL AND INSTITUTE   (China)

^c SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF TOLEDO MEDICAL CENTER   (United States)

Author keywords

Expression; Glioma; Immunosuppressive; PD 1; PD L1; Treatment

Indexed keywords

ANTINEOPLASTIC AGENT; ATEZOLIZUMAB; BEVACIZUMAB; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DURVALUMAB; GALUNISERTIB; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; NIVOLUMAB; PEMBROLIZUMAB; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PIDILIZUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 1 ANTIBODY; PROGRAMMED DEATH 1 RECEPTOR; PROGRAMMED DEATH 1 RECEPTOR ANTIBODY; TEMOZOLOMIDE; UNCLASSIFIED DRUG; PDCD1 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; CANCER GROWTH; CANCER IMMUNOTHERAPY; DRUG EFFICACY; DRUG INDUCED DISEASE; GLIOBLASTOMA; GLIOMA; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PONTINE GLIOMA; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; UPREGULATION; ANTAGONISTS AND INHIBITORS; IMMUNOTHERAPY; METABOLISM; PROCEDURES;

B7-H1 ANTIGEN; GLIOMA; HUMANS; IMMUNOTHERAPY; PROGRAMMED CELL DEATH 1 RECEPTOR; TUMOR ESCAPE;

EID: 85018649211     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-017-0455-6     Document Type: Review

References (67)

1. Goodenberger ML, Jenkins RB. Genetics of adult glioma. Cancer Genet. 2012;205(12):613-21.
2. Han F, Hu R, Yang H, Liu J, Sui J, Xiang X, Wang F, Chu L, Song S. PTEN gene mutations correlate to poor prognosis in glioma patients: a meta-analysis. Onco Targets Ther. 2016;9:3485-92.
3. Gousias K, Markou M, Arzoglou V, Voulgaris S, Vartholomatos G, Kostoula A, Voulgari P, Polyzoidis K, Kyritsis AP. Frequent abnormalities of the immune system in gliomas and correlation with the WHO grading system of malignancy. J Neuroimmunol. 2010;226(1-2):136-42.
4. Sanmamed MF, Chen L. Inducible expression of B7-H1 (PD-L1) and its selective role in tumor site immune modulation. Cancer J. 2014;20(4):256-61.
5. Köhnke T, Krupka C, Tischer J, Knösel T, Subklewe M. Increase of PD-L1 expressing B-precursor ALL cells in a patient resistant to the CD19/CD3-bispecific T cell engager antibody blinatumomab. J Hematol Oncol. 2015;8(1):111.
6. Wei F, Zhong S, Ma Z, Kong H, Medvec A, Ahmed R, Freeman GJ, Krogsgaard M, Riley JL. Strength of PD-1 signaling differentially affects T-cell effector functions. Proc Natl Acad Sci USA. 2013;110(27):2480-9.
7. Weber JS, Kudchadkar RR, Yu B, Gallenstein D, Horak CE, Inzunza HD, Zhao X, Martinez AJ, Wang W, Gibney G. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol. 2013;31(34):4311-8.
8. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013;369(2):134-44.
9. Rizvi NA, Shepherd FA, Antonia SJ, Brahmer JR, Chow LQ, Goldman J, Juergens RA, Borghaei H, Ready NE, Gerber DE. First-line nivolumab (anti-PD-1; BMS-936558, ONO-4538) monotherapy in advanced NSCLC: safety, efficacy, and correlation of outcomes with PD-L1 status. Int J Radiat Oncol. 2014;90(5):s31.
10. Tsai KK, Daud AI. Nivolumab plus ipilimumab in the treatment of advanced melanoma. J Hematol Oncol. 2015;8(1):123.
11. Wintterle S, Schreiner B, Mitsdoerffer M, Schneider D, Chen L, Meyermann R, Weller M, Wiendl H. Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis. Cancer Res. 2003;63(21):7462-7.
12. Wilmotte R, Burkhardt K, Kindler V, Belkouch MC, Dussex G, Nd T, Walker PR, Dietrich PY. B7-homolog 1 expression by human glioma: a new mechanism of immune evasion. Neuroreport. 2005;16(16):1081-5.
13. Garber ST, Hashimoto Y, Weathers SP, Xiu J, Gatalica Z, Verhaak RGW, Zhou S, Fuller GN, Khasraw M, Groot JD. Immune checkpoint blockade as a potential therapeutic target: surveying CNS malignancies. Neuro Oncol. 2016;18(10):1357-66.
14. Berghoff AS, Kiesel B, Widhalm G, Rajky O, Ricken G, Wöhrer A, Dieckmann K, Filipits M, Brandstetter A, Weller M. Programmed death ligand 1 expression and tumor-infiltrating lymphocytes in glioblastoma. Neuro Oncol. 2014;17(8):1064-75.
15. Yao Y, Tao R, Wang X, Wang Y, Mao Y, Zhou LF. B7-H1 is correlated with malignancy-grade gliomas but is not expressed exclusively on tumor stem-like cells. Neuro Oncol. 2009;11(6):757-66.
16. Baral A, Ye HX, Jiang PC, Yao Y, Mao Y. B7-H3 and B7-H1 expression in cerebral spinal fluid and tumor tissue correlates with the malignancy grade of glioma patients. Oncol Lett. 2014;8(3):1195-201.
17. Zeng J, Zhang XK, Chen HD, Zhong ZH, Wu QL, Lin SX. Expression of programmed cell death-ligand 1 and its correlation with clinical outcomes in gliomas. Oncotarget. 2016;7(8):8944-55.
18. Liu Y, Carlsson R, Ambjørn M, Hasan M, Badn W, Darabi A, Siesjö P, Issazadeh-navikas S. PD-L1 expression by neurons nearby tumors indicates better prognosis in glioblastoma patients. J Neurosci. 2013;33(35):14231-45.
19. Nduom EK, Wei J, Yaghi NK, Huang N, Kong LY, Gabrusiewicz K, Ling X, Zhou S, Ivan C, Chen JQ, et al. PD-L1 expression and prognostic impact in glioblastoma. Neuro Oncol. 2016;18(2):195-205.
20. Yan G, Sheng Q, Jiang L, Fei Y, Samuels DC, Yu S. Large scale comparison of gene expression levels by microarrays and RNAseq using TCGA data. PloS one. 2013;8(8):1-10.
21. Chen KH, Yuan CT, Tseng LH, Shun CT, Yeh KH. Case report: mismatch repair proficiency and microsatellite stability in gastric cancer may not predict programmed death-1 blockade resistance. J Hematol Oncol. 2016;9(1):29.
22. Mccaughan GJ, Fulham MJ, Mahar A, Soper J, Hong AM, Stalley PD, Tattersall MH, Bhadri VA. Programmed cell death-1 blockade in recurrent disseminated Ewing sarcoma. J Hematol Oncol. 2016;9(1):48.
23. Bloch O, Crane CA, Kaur R, Safaee M, Rutkowski MJ, Parsa AT. Gliomas promote immunosuppression through induction of B7-H1 expression in tumor-associated macrophages. Clin Cancer Res. 2013;19(12):3165-75.
24. Rodrigues JC, Gonzalez GC, Zhang L, Ibrahim G, Kelly JJ, Gustafson MP, Lin Y, Dietz AB, Forsyth PA, Yong VW, et al. Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties. Neuro Oncol. 2010;12(4):351-65.
25. Avril T, Saikali S, Vauleon E, Jary A, Hamlat A, De Tayrac M, Mosser J, Quillien V. Distinct effects of human glioblastoma immunoregulatory molecules programmed cell death ligand-1 (PDL-1) and indoleamine 2,3-dioxygenase (IDO) on tumour-specific T cell functions. Jf Neuroimmunol. 2010;225(1-2):22-33.
26. Lee SJ, Jang BC, Lee SW, Yang YI, Suh SI, Park YM, Oh S, Shin JG, Yao S, Chen L. Interferon regulatory factor-1 is prerequisite to the constitutive expression and IFN-γ-induced upregulation of B7-H1 (CD274). FEBS Lett. 2006;580(3):755-62.
27. Gowrishankar K, Gunatilake D, Gallagher SJ, Tiffen J, Rizos H, Hersey P. Inducible but not constitutive expression of PD-L1 in human melanoma cells is dependent on activation of NF-κB. PloS one. 2015;10(4):e0123410.
28. Chen J, Feng Y, Lu L, Wang H, Dai L, Li Y, Zhang P. Interferon-γ-induced PD-L1 surface expression on human oral squamous carcinoma via PKD2 signal pathway. Immunobiology. 2012;217(4):385-93.
29. Noman MZ, Desantis G, Janji B, Hasmim M, Karray S, Dessen P, Bronte V, Chouaib S. PD-L1 is a novel direct target of HIF-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med. 2014;211(5):781-90.
30. Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, Herbst RS, Gettinger SN, Chen L, Rimm DL. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest. 2014;94(1):107-16.
31. Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, Cachola KE, Murray JC, Tihan T, Jensen MC, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med. 2007;13(1):84-8.
32. Crane C, Panner A, Pieper RO, Arbiser J, Parsa AT. Honokiol-mediated inhibition of PI3K/mTOR pathway: a potential strategy to overcome immunoresistance in glioma, breast, and prostate carcinoma without impacting T cell function. J Immunother. 2009;32(6):585-92.
33. Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, Wang HY, Wysocka M, Cheng M, Ruggeri BA, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci USA. 2008;105(52):20852-7.
34. Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, Mikse OR, Cherniack AD, Beauchamp EM, Pugh TJ. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov. 2013;3(12):1355-63.
35. Lastwika KJ, Rd WW, Li QK, Norris J, Xu H, Ghazarian SR, Kitagawa H, Kawabata S, Taube JM, Yao S. Control of PD-L1 expression by oncogenic activation of the AKT/mTOR pathway in non-small cell lung cancer. Cancer Res. 2015;76(2):227.
36. Mittendorf EA, Philips AV, Mericbernstam F, Na Q, Yun W, Harrington S, Su X, Ying W, Gonzalezangulo AM, Akcakanat A. PD-L1 expression in triple-negative breast cancer. Cancer Immunol Res. 2014;2(4):361-70.
37. Ota K, Azuma K, Iwama E, Harada T, Matsumoto K, Takamori S, Kage M, Hoshino T, Nakanishi Y, Okamoto I. Induction of PD-L1 expression by the EML4-ALK oncoprotein and downstream signaling pathways in non-small cell lung cancer. Clin Cancer Res. 2015;21(17):4014-21.
38. Chen N, Fang W, Zhan J, Hong S, Tang Y, Kang S, Zhang Y, He X, Zhou T, Qin T. Upregulation of PD-L1 by EGFR activation mediates the immune escape in EGFR-driven NSCLC: implication for optional immune targeted therapy for NSCLC patients with EGFR mutation. J Thorac Oncol. 2015;10(6):910-23.
39. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-33.
40. Wang X, Li J, Dong K, Lin F, Long M, Ouyang Y, Wei J, Chen X, Weng Y, He T. Tumor suppressor miR-34a targets PD-L1 and functions as a potential immunotherapeutic target in acute myeloid leukemia. Cell Signal. 2015;27(3):443-52.
41. Chen L, Gibbons DL, Goswami S, Cortez MA, Ahn YH, Byers LA, Zhang X, Yi X, Dwyer D, Lin W. Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression. Nat Commun. 2014;5:5241.
42. Han SJ, Ahn BJ, Waldron JS, Yang I, Fang S, Crane CA, Pieper RO, Parsa AT. Gamma interferon-mediated superinduction of B7-H1 in PTEN-deficient glioblastoma: a paradoxical mechanism of immune evasion. Neuroreport. 2009;20(18):1597-602.
43. Ivashko IN, Kolesar JM. Pembrolizumab and nivolumab: PD-1 inhibitors for advanced melanoma. Am J Health Syst Pharm. 2016;73(4):193-201.
44. Gettinger S, Rizvi NA, Chow LQ, Borghaei H, Brahmer J, Ready N, Gerber DE, Shepherd FA, Antonia S, Goldman JW. Nivolumab monotherapy for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 2016;34(25):2980-7.
45. Huang BY, Zhan YP, Zong WJ, Yu CJ, Li JF, Qu YM, Han S. The PD-1/B7-H1 pathway modulates the natural killer cells versus mouse glioma stem cells. PloS one. 2015;10(8):e0134715.
46. Zhai L, Lauing KL, Chang AL, Dey M, Qian J, Cheng Y, Lesniak MS, Wainwright DA. The role of IDO in brain tumor immunotherapy. J Neurooncol. 2015;123(3):395-403.
47. Wainwright DA, Chang AL, Dey M, Balyasnikova IV, Kim CK, Tobias A, Cheng Y, Kim JW, Qiao J, Zhang L, et al. Durable therapeutic efficacy utilizing combinatorial blockade against IDO, CTLA-4, and PD-L1 in mice with brain tumors. Clinical Cancer Res. 2014;20(20):5290-301.
48. Teng F, Kong L, Meng X, Yang J, Yu J. Radiotherapy combined with immune checkpoint blockade immunotherapy: achievements and challenges. Cancer Lett. 2015;365(1):23-9.
49. Zeng J, See AP, Phallen J, Jackson CM, Belcaid Z, Ruzevick J, Durham N, Meyer C, Harris TJ, Albesiano E, 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.
50. Schnorfeil FM. T cells are functionally not impaired in AML: increased PD-1 expression is only seen at time of relapse and correlates with a shift towards the memory T cell compartment. J Hematol Oncol. 2015;8(1):93.
51. Cohen MH, Shen YL, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme. Oncologist. 2009;14(11):1131-8.
52. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):699-708.
53. Hughes PE, Caenepeel S, Wu LC. Targeted therapy and checkpoint immunotherapy combinations for the treatment of cancer. Trends Immunol. 2016;37(7):462-76.
54. Amin A, Plimack ER, Infante JR, Ernstoff M, Rini BI, Mcdermott DF, Knox J, Pal SK, Voss M, Sharma P. Nivolumab (N) (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib (S) or pazopanib (P) in patients (PTS) with metastatic renal cell carcinoma (mRCC). Ann Oncol. 2014;25 suppl 4:iv362-3.
55. Yasuda S, Sho M, Yamato I, Yoshiji H, Wakatsuki K, Nishiwada S, Yagita H, Nakajima Y. Simultaneous blockade of programmed death 1 and vascular endothelial growth factor receptor 2 (VEGFR2) induces synergistic anti-tumour effect in vivo. Clin Exp Immunol. 2013;172(3):500-6.
56. Queirolo P, Spagnolo F, Ascierto PA, Simeone E, Marchetti P, Scoppola A, Vecchio MD, Guardo LD, Maio M, Giacomo AMD. Efficacy and safety of ipilimumab in patients with advanced melanoma and brain metastases. J Neurooncol. 2014;118(1):109-16.
57. Margolin K, Ernstoff MS, Hamid O, Lawrence D, Mcdermott D, Puzanov I, Wolchok JD, Clark JI, Sznol M, Logan TF. Iconography: ipilimumab in patients with melanoma and brain metastases: an open-label, phase 2 trial. Lancet Oncol. 2012;13(5):459-65.
58. Di GA, Ascierto PA, Pilla L, Santinami M, Ferrucci PF, Giannarelli D, Marasco A, Rivoltini L, Simeone E, Nicoletti SV. Ipilimumab and fotemustine in patients with advanced melanoma (NIBIT-M1): an open-label, single-arm phase 2 trial. Lancet Oncol. 2012;13(9):879-86.
59. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci USA. 2010;107(9):4275-80.
60. Goldberg SB, Gettinger SN, Mahajan A, Chiang AC, Herbst RS, Sznol M, Tsiouris AJ, Cohen J, Vortmeyer A, Jilaveanu L. Pembrolizumab for patients with melanoma or non-small-cell lung cancer and untreated brain metastases: early analysis of a non-randomised, open-label, phase 2 trial. Lancet Oncol. 2016;17(7):976-83.
61. Atkins MB, Kudchadkar RR, Sznol M, Mcdermott DF, Lotem M, Schachter J, Wolchok JD, Urba WJ, Kuzel T, Schuchter LM. Phase 2, multicenter, safety and efficacy study of pidilizumab in patients with metastatic melanoma. J Clinical Oncol 2014; 32 suppl 5: abstract 9001.
62. Segal NH, Antonia SJ, Brahmer JR, Maio M, Blakehaskins A, Li X, Vasselli J, Ibrahim RA, Lutzky J, Khleif S. Preliminary data from a multi-arm expansion study of MEDI4736, an anti-PD-L1 antibody. J Clinical Oncol 2014; 32 suppl 5: abstract 3002.
63. Ma W, Gilligan BM, Yuan J, Li T. Current status and perspectives in translational biomarker research for PD-1/PD-L1 immune checkpoint blockade therapy. J Hematol Oncol. 2016;9(1):1.
64. Philips GK, Atkins M. Therapeutic uses of anti-PD-1 and anti-PD-L1 antibodies. Int Immunol. 2014;27(1):39-46.
65. Wang J, Yuan R, Song W, Sun J, Liu D, Li Z. PD-1, PD-L1 (B7-H1) and tumor-site immune modulation therapy: the historical perspective. J Hematol Oncol. 2017;10(1):34.
66. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252-64.
67. Reardon DA, Okada H. Re-defining response and treatment effects for neuro-oncology immunotherapy clinical trials. J Neurooncol. 2015;123(3):339-46.