CD70, a novel target of CAR T-cell therapy for gliomas

Neuro-Oncology

Volumn 20, Issue 1, 2018, Pages 55-65

  Jin, Linchun ^a,b   Ge, Haitao ^b   Long, Yu ^a,b   Yang, Changlin ^a   Chang, Yifan Emily ^a,d   Mu, Luyan ^b   Sayour, Elias J ^a   De Leon, Gabriel ^a,e   Wang, Qiong J ^c,f   Yang, James C ^c   Kubilis, Paul S ^a   Bao, Hongbo ^b   Xia, Songsong ^b   Lu, Dunyue ^b   Kong, Yingjun ^b   Hu, Li ^b   Shang, Yujiao ^b   Jiang, Chencheng ^b   Nie, Jing ^b   Li, Shimin ^b   Gu, Yunhe ^b   Sun, Jiahang ^b   Mitchell, Duane A ^a   Lin, Zhiguo ^b   Huang, Jianping ^a   more..

^a UNIVERSITY OF FLORIDA   (United States)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f MEDIMMUNE   (United States)

Author keywords

CD70; chimeric antigen receptors (CARs); gliomas; immunosuppressive ligand; immunotherapy

Indexed keywords

CD70 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; ISOCITRATE DEHYDROGENASE; CD70 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL DEATH; CELL THERAPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN TISSUE; MOLECULAR IMAGING; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BRAIN TUMOR; GENETICS; IMMUNOLOGY; PATHOLOGY; PROCEDURES; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; BRAIN NEOPLASMS; CD27 LIGAND; CELL LINE, TUMOR; GLIOMA; HUMANS; IMMUNOTHERAPY, ADOPTIVE; ISOCITRATE DEHYDROGENASE; MICE; RECEPTORS, CHIMERIC ANTIGEN; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 85040928540     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nox116     Document Type: Article

References (36)

1. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009; 10(5):459-466.
2. Stupp R, Mason WP, van den Bent MJ, et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987-996.
3. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480(7378):480-489.
4. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer. 2008;8(4):299-308.
5. Morgan RA, Johnson LA, Davis JL, et al. Recognition of glioma stem cells by genetically modified T cells targeting EGFRvIII and development of adoptive cell therapy for glioma. Hum Gene Ther. 2012;23(10):1043-1053.
6. Bowman MR, Crimmins MA, Yetz-Aldape J, Kriz R, Kelleher K, Herrmann S. The cloning of CD70 and its identification as the ligand for CD27. J Immunol. 1994;152(4):1756-1761.
7. Hintzen RQ, Lens SM, Beckmann MP, Goodwin RG, Lynch D, van Lier RA. Characterization of the human CD27 ligand, a novel member of the TNF gene family. J Immunol. 1994;152(4):1762-1773.
8. Hintzen RQ, Lens SM, Lammers K, Kuiper H, Beckmann MP, van Lier RA. Engagement of CD27 with its ligand CD70 provides a second signal for T cell activation. J Immunol. 1995;154(6):2612-2623.
9. Nolte MA, van Olffen RW, van Gisbergen KP, van Lier RA. Timing and tuning of CD27-CD70 interactions: the impact of signal strength in setting the balance between adaptive responses and immunopathology. Immunol Rev. 2009;229(1):216-231.
10. Held-Feindt J, Mentlein R. CD70/CD27 ligand, a member of the TNF family, is expressed in human brain tumors. Int J Cancer. 2002;98(3):352-356.
11. Ryan MC, Kostner H, Gordon KA, et al. Targeting pancreatic and ovarian carcinomas using the auristatin-based anti-CD70 antibody-drug conjugate SGN-75. Br J Cancer. 2010;103(5):676-684.
12. Wischhusen J, Jung G, Radovanovic I, et al. Identification of CD70-mediated apoptosis of immune effector cells as a novel immune escape pathway of human glioblastoma. Cancer Res. 2002;62(9):2592-2599.
13. Adam PJ, Terrett JA, Steers G, et al. CD70 (TNFSF7) is expressed at high prevalence in renal cell carcinomas and is rapidly internalised on antibody binding. Br J Cancer. 2006;95(3):298-306.
14. Huang J, Kerstann KW, Ahmadzadeh M, et al. Modulation by IL-2 of CD70 and CD27 expression on CD8+ T cells: importance for the therapeutic effectiveness of cell transfer immunotherapy. J Immunol. 2006;176(12):7726-7735.
15. Keller AM, Xiao Y, Peperzak V, Naik SH, Borst J. Costimulatory ligand CD70 allows induction of CD8+ T-cell immunity by immature dendritic cells in a vaccination setting. Blood. 2009;113(21):5167-5175.
16. Chahlavi A, Rayman P, Richmond AL, et al. Glioblastomas induce T-lymphocyte death by two distinct pathways involving gangliosides and CD70. Cancer Res. 2005;65(12):5428-5438.
17. Diegmann J, Junker K, Loncarevic IF, Michel S, Schimmel B, von Eggeling F. Immune escape for renal cell carcinoma: CD70 mediates apoptosis in lymphocytes. Neoplasia. 2006;8(11):933-938.
18. Ruf M, Mittmann C, Nowicka AM, et al. pVHL/HIF-regulated CD70 expression is associated with infiltration of CD27+ lymphocytes and increased serum levels of soluble CD27 in clear cell renal cell carcinoma. Clin Cancer Res. 2015;21(4):889-898.
19. Wang QJ, Yu Z, Hanada K-i, et al. Pre-clinical evaluation of chimeric antigen receptors targeting CD70-expressing cancers. Clinical Cancer Research. 2016.
20. Johnson LA, Scholler J, Ohkuri T, et al. Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma. Science Translational Medicine. 2015; 7(275):275ra222-275ra222.
21. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol. 2005;175(10):7046-7052.
22. Che JW, Kraft AR, Selin LK, Welsh RM. Regulatory T cells resist virus infection-induced apoptosis. J Virol. 2015;89(4):2112-2120.
23. Verhaak RG, Hoadley KA, Purdom E, et al.; Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98-110.
24. Ge H, Mu L, Jin L, et al. Tumor associated CD70 expression is involved in promoting tumor migration and macrophage infiltration in GBM. Int J Cancer. 2017. doi:10. 1002/ijc. 30830
25. Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel). 2014;6(3):1670-1690.
26. Oelkrug C, Ramage JM. Enhancement of T cell recruitment and infiltration into tumours. Clin Exp Immunol. 2014;178(1):1-8.
27. Network TCGAR. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med. 2015; 372(26):2481-2498.
28. Silence K, Dreier T, Moshir M, et al. ARGX-110, a highly potent antibody targeting CD70, eliminates tumors via both enhanced ADCC and immune checkpoint blockade. Paper presented at: MAbs2014.
29. Shaffer DR, Savoldo B, Yi Z, et al. T cells redirected against CD70 for the immunotherapy of CD70-positive malignancies. Blood. 2011;117(16):4304-4314.
30. Engelhardt B. Molecular mechanisms involved in T cell migration across the blood-brain barrier. J Neural Transm (Vienna). 2006;113(4):477-485.
31. Miao H, Choi BD, Suryadevara CM, et al. EGFRvIII-specific chimeric antigen receptor T cells migrate to and kill tumor deposits infiltrating the brain parenchyma in an invasive xenograft model of glioblastoma. PLoS One. 2014;9(4):e94281.
32. Brown CE, Alizadeh D, Starr R, et al. Regression of glioblastoma after chimeric antigen receptor T-cell therapy. N Engl J Med. 2016;375(26): 2561-2569.
33. Huang J, Jochems C, Anderson AM, et al. Soluble CD27-pool in humans may contribute to T cell activation and tumor immunity. J Immunol. 2013;190(12):6250-6258.
34. Abolhassani H, Edwards ES, Ikinciogullari A, et al. Combined immunodeficiency and Epstein-Barr virus-induced B cell malignancy in humans with inherited CD70 deficiency. J Exp Med. 2017;214(1): 91-106.
35. Izawa K, Martin E, Soudais C, et al. Inherited CD70 deficiency in humans reveals a critical role for the CD70-CD27 pathway in immunity to Epstein-Barr virus infection. J Exp Med. 2017;214(1):73-89.
36. Huang J, Wang QJ, Yang S, et al. Irradiation enhances human T-cell function by upregulating CD70 expression on antigen-presenting cells in vitro. J Immunother. 2011;34(4):327-335.