Chimeric antigen receptor-T cell therapy for solid tumors require new clinical regimens

Expert Review of Anticancer Therapy

Volumn 17, Issue 12, 2017, Pages 1099-1106

  Xu, Jinjing ^a,b   Tian, Kang ^a   Zhang, Haixu ^a   Li, Liantao ^a   Liu, Hongyan ^a   Liu, Jingjie ^a   Zhang, Qing ^a   Zheng, Junnian ^a  

^a XUZHOU MEDICAL UNIVERSITY   (China)

^b Huai'an Maternal and Child Health Care Center   (China)

Author keywords

CAR T; Chemotherapy; clinical regimen; radical resection; solid tumor

Indexed keywords

ALT 803; ATEZOLIZUMAB; BMS 936559; CABOZANTINIB; CHECKPOINT KINASE INHIBITOR; CHIMERIC ANTIGEN RECEPTOR; CISPLATIN; DACARBAZINE; DOCETAXEL; DOXORUBICIN; FLUOROURACIL; GEMCITABINE; IPILIMUMAB; NIVOLUMAB; PEMBROLIZUMAB; PIDILIZUMAB; SORAFENIB; SUNITINIB; TEMOZOLOMIDE; TICILIMUMAB; ANTINEOPLASTIC AGENT; LYMPHOCYTE ANTIGEN RECEPTOR;

CANCER CHEMOTHERAPY; CANCER RECURRENCE; CANCER SURVIVAL; CELL THERAPY; CLINICAL EFFECTIVENESS; DRUG DELIVERY SYSTEM; DRUG EFFECT; HUMAN; METASTASIS; NONHUMAN; OVERALL SURVIVAL; RADICAL RESECTION; REVIEW; SOLID MALIGNANT NEOPLASM; T LYMPHOCYTE; TREATMENT RESPONSE; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; MULTIMODALITY CANCER THERAPY; NEOPLASM; PREVENTION AND CONTROL; PROCEDURES; TUMOR RECURRENCE;

ANIMALS; ANTINEOPLASTIC AGENTS; COMBINED MODALITY THERAPY; HUMANS; IMMUNOTHERAPY; NEOPLASM RECURRENCE, LOCAL; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 85038219456     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1080/14737140.2017.1395285     Document Type: Review

References (83)

1. Zhang Q, Li H, Yang J, et al. Strategies to improve the clinical performance of chimeric antigen receptor-modified T cells for cancer. Curr Gene Ther. 2013;13(1):65–70.
2. Wu Y, Jiang S, Ying T., From therapeutic antibodies to chimeric antigen receptors (CARs): making better CARs based on antigen-binding domain. Expert Opin Biol Ther. 2016;16(12):1469–1478.
3. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507–1517.
4. Locke FL, Neelapu SS, Bartlett NL, et al. Phase 1 results of ZUMA-1: a multicenter study of KTE-C19 anti-CD19 CAR T cell therapy in refractory aggressive lymphoma. Mol Therapy. 2017;25(1):285–295.
5. DLBCL Responds Well to Anti-CD19. CAR therapy. Cancer Discov. 2017;7(3):241–242.
6. Till BG, Jensen MC, Wang J, et al. CD20-specific adoptive immunotherapy for lymphoma using a chimeric antigen receptor with both CD28 and 4-1BB domains: pilot clinical trial results. Blood. 2012;119(17):3940–3950.
7. Haso W, Lee DW, Shah NN, et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood. 2013;121(7):1165–1174.
8. Lim WA, June CH., The principles of engineering immune cells to treat cancer. Cell. 2017;168(4):724–740.
9. Kershaw MH, Westwood JA, Parker LL, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res. 2006;12(20 Pt 1):6106–6115.
10. Park JR, Digiusto DL, Slovak M, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Therapy. 2007;15(4):825–833.
11. Morgan RA, Yang JC, Kitano M, et al. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Therapy. 2010;18(4):843–851.
12. Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118(23):6050–6056.
13. Pule MA, Savoldo B, Myers GD, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008;14(11):1264–1270.
14. Maus MV, Haas AR, Beatty GL, et al. T cells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol Res. 2013;1(1):26–31.
15. Ahmed N, Brawley VS, Hegde M, et al. Human epidermal growth factor receptor 2 (HER2) -specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol. 2015;33:1688–1696.
16. Lamers CH, Klaver Y, Gratama JW, et al. Treatment of metastatic renal cell carcinoma (mRCC) with CAIX CAR-engineered T-cells-a completed study overview. Biochem Soc Trans. 2016;44(3):951–959.
17. Brown CE, Badie B, Barish ME, et al. Bioactivity and safety of IL13Ralpha2-redirected chimeric antigen receptor CD8+ T cells in patients with recurrent glioblastoma. Clin Cancer Res. 2015;21(18):4062–4072.
18. Katz SC, Burga RA, McCormack E, et al. Phase I hepatic immunotherapy for metastases study of intra-arterial chimeric antigen receptor-modified T-cell therapy for CEA+ liver metastases. Clin Cancer Res. 2015;21(14):3149–3159.
19. 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.
20. Junghans RP, Ma Q, Rathore R, et al. Phase I trial of anti-PSMA designer CAR-T cells in prostate cancer: possible role for interacting interleukin 2-T cell pharmacodynamics as a determinant of clinical response. Prostate. 2016;76(14):1257–1270.
21. You F, Jiang L, Zhang B, et al. Phase 1 clinical trial demonstrated that MUC1 positive metastatic seminal vesicle cancer can be effectively eradicated by modified anti-MUC1 chimeric antigen receptor transduced T cells. Sci China Life Sci. 2016;59(4):386–397.
22. Feng KC, Guo YL, Liu Y, et al. Cocktail treatment with EGFR-specific and CD133-specific chimeric antigen receptor-modified T cells in a patient with advanced cholangiocarcinoma. J Hematol Oncol. 2017;10(1):4.
23. Hege KM, Bergsland EK, Fisher GA, et al. Safety, tumor trafficking and immunogenicity of chimeric antigen receptor (CAR)-T cells specific for TAG-72 in colorectal cancer. J Immunother Cancer. 2017;5:22.
24. Ahmed N, Brawley V, Hegde M, et al. HER2-specific chimeric antigen receptor-modified virus-specific T cells for progressive glioblastoma: a phase 1 dose-escalation trial. JAMA Oncology. 2017;3(8):1094–1101.
25. Feng K, Liu Y, Guo Y, et al. Phase I study of chimeric antigen receptor modified T cells in treating HER2-positive advanced biliary tract cancers and pancreatic cancers. Protein Cell. 2017.
26. Heczey A, Louis CU, Savoldo B, et al. CAR T cells administered in combination with lymphodepletion and PD-1 inhibition to patients with neuroblastoma. Mol Therapy. 2017;25(9):2214–2224.
27. Zhang C, Wang Z, Yang Z, et al. Phase I escalating-dose trial of CAR-T therapy targeting CEA+ metastatic colorectal cancers. Mol Therapy. 2017;25(5):1248–1258.
28. Thistlethwaite FC, Gilham DE, Guest RD, et al. The clinical efficacy of first-generation carcinoembryonic antigen (CEACAM5)-specific CAR T cells is limited by poor persistence and transient pre-conditioning-dependent respiratory toxicity. Cancer Immunology, Immunotherapy: CII. 2017;66:1425–1436.
29. Lamers CH, Willemsen R, Van Elzakker P, et al. Immune responses to transgene and retroviral vector in patients treated with ex vivo-engineered T cells. Blood. 2011;117(1):72–82.
30. Di S, Li Z. Treatment of solid tumors with chimeric antigen receptor-engineered T cells: current status and future prospects. Sci China Life Sci. 2016;59(4):360–369.
31. Zuccolotto G, Fracasso G, Merlo A, et al. PSMA-specific CAR-engineered T cells eradicate disseminated prostate cancer in preclinical models. PloS One. 2014;9(10):e109427.
32. Zhang Q, Wang H, Li H, et al. Chimeric antigen receptor-modified T cells inhibit the growth and metastases of established tissue factor-positive tumors in NOG mice. Oncotarget. 2017;8(6):9488–9499.
33. Jaspers JE, Brentjens RJ. Development of CAR T cells designed to improve antitumor efficacy and safety. Pharmacol Ther. 2017;178:83–91.
34. Munn DH, Sharma MD, Johnson TS, et al. IDO, PTEN-expressing tregs and control of antigen-presentation in the murine tumor microenvironment. Cancer Immunology, Immunotherapy: CII. 2017;66:1049–1058.
35. Goswami KK, Ghosh T, Ghosh S, et al. Tumor promoting role of anti-tumor macrophages in tumor microenvironment. Cell Immunol. 2017;316:1–10.
36. Scarfo I, Maus MV. Current approaches to increase CAR T cell potency in solid tumors: targeting the tumor microenvironment. J Immunother Cancer. 2017;5:28.
37. Tacar O, Sriamornsak P, Dass CR. Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol. 2013;65(2):157–170.
38. Casares N, Pequignot MO, Tesniere A, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med. 2005;202(12):1691–1701.
39. Hu J, Zhu S, Xia X, et al. CD8+T cell-specific induction of NKG2D receptor by doxorubicin plus interleukin-12 and its contribution to CD8+T cell accumulation in tumors. Mol Cancer. 2014;13:34.
40. Alizadeh D, Trad M, Hanke NT, et al. Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer. Cancer Res. 2014;74(1):104–118.
41. Ramakrishnan R, Assudani D, Nagaraj S, et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest. 2010;120(4):1111–1124.
42. Hsu FT, Chen TC, Chuang HY, et al. Enhancement of adoptive T cell transfer with single low dose pretreatment of doxorubicin or paclitaxel in mice. Oncotarget. 2015;6(42):44134–44150.
43. Roskoski R, Jr. Sunitinib: a VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem Biophys Res Commun. 2007;356(2):323–328.
44. Ozao-Choy J, Ma G, Kao J, et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009;69(6):2514–2522.
45. Ko JS, Zea AH, Rini BI, et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res. 2009;15(6):2148–2157.
46. Finke JH, Rini B, Ireland J, et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin Cancer Res. 2008;14(20):6674–6682.
47. Yu N, Fu S, Xu Z, et al. Synergistic antitumor responses by combined GITR activation and sunitinib in metastatic renal cell carcinoma. Int J Cancer. 2016;138(2):451–462.
48. Huo M, Zhao Y, Satterlee AB, et al. Tumor-targeted delivery of sunitinib base enhances vaccine therapy for advanced melanoma by remodeling the tumor microenvironment. J Control Release. 2017;245:81–94.
49. Draghiciu O, Nijman HW, Hoogeboom BN, et al. Sunitinib depletes myeloid-derived suppressor cells and synergizes with a cancer vaccine to enhance antigen-specific immune responses and tumor eradication. Oncoimmunology. 2015;4(3):e989764.
50. Bose A, Taylor JL, Alber S, et al. Sunitinib facilitates the activation and recruitment of therapeutic anti-tumor immunity in concert with specific vaccination. Int J Cancer. 2011;129(9):2158–2170.
51. van Hooren L, Georganaki M, Huang H, et al. Sunitinib enhances the antitumor responses of agonistic CD40-antibody by reducing MDSCs and synergistically improving endothelial activation and T-cell recruitment. Oncotarget. 2016;7(31):50277–50289.
52. Gaither KA, Little AA, McBride AA, et al. The immunomodulatory, antitumor and antimetastatic responses of melanoma-bearing normal and alcoholic mice to sunitinib and ALT-803: a combinatorial treatment approach. Cancer Immunology, Immunotherapy: CII. 2016;65(9):1123–1134.
53. Bhatia S, Heath E, Puzanov I, et al. Phase II study of recombinant IL-21 (rIL-21) plus sorafenib as second- or third-line therapy for metastatic renal cell cancer (mRCC): final results. J Clinical Oncology. 2009;27(15_suppl):3023.
54. Matsushita H, Enomoto Y, Kume H, et al. A pilot study of autologous tumor lysate-loaded dendritic cell vaccination combined with sunitinib for metastatic renal cell carcinoma. J Immunother Cancer. 2014;2:30.
55. Patel PH, Chaganti RS, Motzer RJ. Targeted therapy for metastatic renal cell carcinoma. Br J Cancer. 2006;94(5):614–619.
56. Fabian MA, Biggs WH, 3rd, Treiber DK, et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol. 2005;23(3):329–336.
57. Busse A, Asemissen AM, Nonnenmacher A, et al. Immunomodulatory effects of sorafenib on peripheral immune effector cells in metastatic renal cell carcinoma. Eur J Cancer. 2011;47(5):690–696.
58. Cabrera R, Ararat M, Xu Y, et al. Immune modulation of effector CD4+ and regulatory T cell function by sorafenib in patients with hepatocellular carcinoma. Cancer Immunology, Immunotherapy: CII. 2013;62(4):737–746.
59. Chen ML, Yan BS, Lu WC, et al. Sorafenib relieves cell-intrinsic and cell-extrinsic inhibitions of effector T cells in tumor microenvironment to augment antitumor immunity. Int J Cancer. 2014;134(2):319–331.
60. Chuang HY, Chang YF, Liu RS, et al. Serial low doses of sorafenib enhance therapeutic efficacy of adoptive T cell therapy in a murine model by improving tumor microenvironment. PloS One. 2014;9(10):e109992.
61. Suzuki E, Kapoor V, Jassar AS, et al. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res. 2005;11(18):6713–6721.
62. Takahara A, Koido S, Ito M, et al. Gemcitabine enhances Wilms’ tumor gene WT1 expression and sensitizes human pancreatic cancer cells with WT1-specific T-cell-mediated antitumor immune response. Cancer Immunology, Immunotherapy: CII. 2011;60(9):1289–1297.
63. Homma Y, Taniguchi K, Nakazawa M, et al. Changes in the immune cell population and cell proliferation in peripheral blood after gemcitabine-based chemotherapy for pancreatic cancer. Clin Transl Oncol. 2014;16(3):330–335.
64. Zhang Q, Zhang Y, Li K, et al. A novel strategy to improve the therapeutic efficacy of gemcitabine for non-small cell lung cancer by the tumor-penetrating peptide iRGD. PloS One. 2015;10(6):e0129865.
65. Bunt SK, Mohr AM, Bailey JM, et al. Rosiglitazone and gemcitabine in combination reduces immune suppression and modulates T cell populations in pancreatic cancer. Cancer Immunology, Immunotherapy: CII. 2013;62(2):225–236.
66. Vincent J, Mignot G, Chalmin F, et al. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 2010;70(8):3052–3061.
67. Kodumudi KN, Woan K, Gilvary DL, et al. A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin Cancer Res. 2010;16(18):4583–4594.
68. Kwilas AR, Ardiani A, Donahue RN, et al. Dual effects of a targeted small-molecule inhibitor (cabozantinib) on immune-mediated killing of tumor cells and immune tumor microenvironment permissiveness when combined with a cancer vaccine. J Transl Med. 2014;12:294.
69. Patnaik A, Swanson KD, Csizmadia E, et al. Cabozantinib eradicates advanced murine prostate cancer by activating antitumor innate immunity. Cancer Discov. 2017;7:750–765.
70. Hong M, Puaux AL, Huang C, et al. Chemotherapy induces intratumoral expression of chemokines in cutaneous melanoma, favoring T-cell infiltration and tumor control. Cancer Res. 2011;71(22):6997–7009.
71. Ruella M, Kalos M. Adoptive immunotherapy for cancer. Immunol Rev. 2014;257(1):14–38.
72. Chen N, Morello A, Tano Z, et al. CAR T-cell intrinsic PD-1 checkpoint blockade: a two-in-one approach for solid tumor immunotherapy. Oncoimmunology. 2017;6(2):e1273302.
73. Hegde UP, Mukherji B. Current status of chimeric antigen receptor engineered T cell-based and immune checkpoint blockade-based cancer immunotherapies. Cancer Immunol Immunother: CII. 2017;66:1113–1121.
74. John LB, Devaud C, Duong CPM, et al. Anti-PD-1 antibody therapy potently enhances the eradication of established tumors by gene-modified T cells. Clin Cancer Res. 2013;19(20):5636–5646.
75. Liu XJ, Ranganathan R, Jiang SG, et al. A chimeric switch-receptor targeting PD1 augments the efficacy of second-generation CAR T cells in advanced solid tumors. Cancer Res. 2016;76(6):1578–1590.
76. Serganova I, Moroz E, Cohen I, et al. Enhancement of PSMA-directed CAR adoptive immunotherapy by PD-1/PD-L1 blockade. Mol Ther Oncolytics. 2017;4:41–54.
77. Schneider D, Xiong Y, Wu D, et al. A tandem CD19/CD20 CAR lentiviral vector drives on-target and off-target antigen modulation in leukemia cell lines. J Immunother Cancer. 2017;5:42.
78. Zah E, Lin MY, Silva-Benedict A, et al. T cells expressing CD19/CD20 bispecific chimeric antigen receptors prevent antigen escape by malignant B cells. Cancer Immunol Res. 2016;4(6):498–508.
79. Hegde M, Corder A, Chow KK, et al. Combinational targeting offsets antigen escape and enhances effector functions of adoptively transferred T cells in glioblastoma. Mol Therapy. 2013;21(11):2087–2101.
80. Anurathapan U, Chan RC, Hindi HF, et al. Kinetics of tumor destruction by chimeric antigen receptor-modified T cells. Mol Therapy. 2014;22(3):623–633.
81. Grada Z, Hegde M, Byrd T, et al. TanCAR: a novel bispecific chimeric antigen receptor for cancer immunotherapy. Mol Ther Nucleic Acids. 2013;2:e105.
82. Dasgupta A, Lim AR, Ghajar CM. Circulating and disseminated tumor cells: harbingers or initiators of metastasis? Mol Oncol. 2017;11(1):40–61.
83. Ellsworth DL, Blackburn HL, Shriver CD, et al. Single-cell sequencing and tumorigenesis: improved understanding of tumor evolution and metastasis. Clin Transl Med. 2017;6(1):15.