Synthetic biology in cell-based cancer immunotherapy

Trends in Biotechnology

Volumn 33, Issue 8, 2015, Pages 449-461

  Chakravarti, Deboki ^a   Wong, Wilson W ^a  

^a Boston University   (United States)

Author keywords

Cancer; Chimeric antigen receptors; Genetic circuits; Immunotherapy; Synthetic biology

Indexed keywords

CELL ENGINEERING; CELLULAR MANUFACTURING; COST ENGINEERING; CYTOLOGY; DISEASES; T-CELLS; TUMORS;

ANTIGEN RECEPTORS; CANCER; CANCER IMMUNOTHERAPY; CELLULAR ENGINEERING; COST OF MANUFACTURING; GENETIC CIRCUITS; IMMUNOTHERAPY; SYNTHETIC RECEPTORS;

SYNTHETIC BIOLOGY;

RECEPTOR;

CANCER IMMUNOTHERAPY; CELL BASED CANCER IMMUNOTHERAPY; CELL ENGINEERING; GENETIC ENGINEERING; GENOME EDITING; HOST CELL; HUMAN; IMMUNOCOMPETENT CELL; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; T LYMPHOCYTE; TUMOR IMMUNITY; ANIMAL; BIOLOGICAL THERAPY; IMMUNOTHERAPY; MOUSE; NEOPLASMS; SYNTHETIC BIOLOGY;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; HUMANS; IMMUNOTHERAPY; MICE; NEOPLASMS; SYNTHETIC BIOLOGY;

EID: 84937522794     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2015.05.001     Document Type: Review

References (119)

1. DuPage M., et al. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 2012, 482:405-409.
2. Rabinovich G.A., et al. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 2007, 25:267-296.
3. Shiao S.L., et al. Immune microenvironments in solid tumors: new targets for therapy. Genes Dev. 2011, 25:2559-2572.
4. Bouchlaka M.N., et al. Immunotherapy following hematopoietic stem cell transplantation: potential for synergistic effects. Immunotherapy 2010, 2:399-418.
5. Wrzesinski C., et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. J. Immunother. 2010, 33:1-7.
6. Wrzesinski C., et al. Hematopoietic stem cells promote the expansion and function of adoptively transferred antitumor CD8 T cells. J. Clin. Invest. 2007, 117:492-501.
7. Platten M., et al. Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer Res. 2012, 72:5435-5440.
8. + T cells. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:1969-1974.
9. Melero I., et al. IL-12 gene therapy for cancer: in synergy with other immunotherapies. Trends Immunol. 2001, 22:113-115.
10. Del Vecchio M., et al. Interleukin-12: biological properties and clinical application. Clin. Cancer Res. 2007, 13:4677-4685.
11. Lee C.S., et al. Novel antibodies targeting immune regulatory checkpoints for cancer therapy. Br. J. Clin. Pharmacol. 2013, 76:233-247.
12. Spigel D.R., Socinski M.A. Rationale for chemotherapy, immunotherapy, and checkpoint blockade in SCLC: beyond traditional treatment approaches. J. Thorac. Oncol. 2013, 8:587-598.
13. Pardoll D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12:252-264.
14. Moser J.C., et al. The Mayo Clinic experience with the use of kinase inhibitors, ipilimumab, bevacizumab, and local therapies in the treatment of metastatic uveal melanoma. Melanoma Res. 2015, 25:59-63.
15. Philips G.K., Atkins M. Therapeutic uses of anti-PD-1 and anti-PD-L1 antibodies. Int. Immunol. 2015, 27:39-46.
16. Way J.C., et al. Integrating biological redesign: where synthetic biology came from and where it needs to go. Cell 2014, 157:151-161.
17. Auslander S., Fussenegger M. From gene switches to mammalian designer cells: present and future prospects. Trends Biotechnol. 2013, 31:155-168.
18. Bashor C.J., et al. Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu. Rev. Biophys. 2010, 39:515-537.
19. Fischbach M.A., et al. Cell-based therapeutics: the next pillar of medicine. Sci. Transl. Med. 2013, 5:179ps177.
20. Cox D.B., et al. Therapeutic genome editing: prospects and challenges. Nat. Med. 2015, 21:121-131.
21. O'Sullivan D., Pearce E.L. Targeting T cell metabolism for therapy. Trends Immunol. 2015, 36:71-80.
22. Lo Presti E., et al. Tumor-infiltrating gammadelta T Lymphocytes: pathogenic role, clinical significance, and differential programing in the tumor microenvironment. Front. Immunol. 2014, 5:607.
23. +-enriched versus unselected tumor-infiltrating lymphocytes for adoptive cell therapy for patients with melanoma. J. Clin. Oncol. 2013, 31:2152-2159.
24. Khammari A., et al. Adoptive TIL transfer in the adjuvant setting for melanoma: long-term patient survival. J. Immunol. Res. 2014, 2014:186212.
25. Duong C.P., et al. Cancer immunotherapy utilizing gene-modified T cells: from the bench to the clinic. Mol. Immunol. 2015, Published online January 13, 2015. 10.1016/j.molimm.2014.12.009.
26. Thaxton J.E., Li Z. To affinity and beyond: harnessing the T Cell receptor for cancer immunotherapy. Hum. Vaccines Immunother. 2014, 10:3313-3321.
27. Johnson L.A., et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009, 114:535-546.
28. Chmielewski M., et al. T cell activation by antibody-like immunoreceptors: increase in affinity of the single-chain fragment domain above threshold does not increase T cell activation against antigen-positive target cells but decreases selectivity. J. Immunol. 2004, 173:7647-7653.
29. Jena B., et al. Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. Blood 2010, 116:1035-1044.
30. Davila M.L., et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci. Transl. Med. 2014, 6:224ra225.
31. Brentjens R.J., et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 2011, 118:4817-4828.
32. Maude S.L., et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 2014, 371:1507-1517.
33. Lee D.W., et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet 2015, 385:517-528.
34. Wang Q.S., et al. Treatment of CD33-directed chimeric antigen receptor-modified T cells in one patient with relapsed and refractory acute myeloid leukemia. Mol. Ther. 2015, 23:184-191.
35. Ritchie D.S., et al. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol. Ther. 2013, 21:2122-2129.
36. Couzin-Frankel J. Cancer immunotherapy. Science 2013, 342:1432-1433.
37. Hinrichs C.S., Restifo N.P. Reassessing target antigens for adoptive T-cell therapy. Nat. Biotechnol. 2013, 31:999-1008.
38. Morgan R.A., et al. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol. Ther. 2010, 18:843-851.
39. Frigault M.J., et al. Identification of chimeric antigen receptors that mediate constitutive or inducible proliferation of T cells. Cancer Immunol. Res. 2015, 3:356-367.
40. Fedorov V.D., et al. PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci. Transl. Med. 2013, 5:215ra172.
41. Duong C.P., et al. Engineering T cell function using chimeric antigen receptors identified using a DNA library approach. PLoS ONE 2013, 8:e63037.
42. Hacohen N., et al. Getting personal with neoantigen-based therapeutic cancer vaccines. Cancer Immunol. Res. 2013, 1:11-15.
43. Rajasagi M., et al. Systematic identification of personal tumor-specific neoantigens in chronic lymphocytic leukemia. Blood 2014, 124:453-462.
44. van Rooij N., et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J. Clin. Oncol. 2013, 31:e439-e442.
45. Brown S.D., et al. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014, 24:743-750.
46. + T cells in human melanoma. Nat. Med. 2015, 21:81-85.
47. Robbins P.F., et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 2013, 19:747-752.
48. Kloss C.C., et al. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat. Biotechnol. 2013, 31:71-75.
49. Fedorov V.D., et al. Novel approaches to enhance the specificity and safety of engineered T cells. Cancer J. 2014, 20:160-165.
50. Narayanan P., et al. A composite MyD88/CD40 switch synergistically activates mouse and human dendritic cells for enhanced antitumor efficacy. J. Clin. Invest. 2011, 121:1524-1534.
51. Kudo K., et al. T lymphocytes expressing a CD16 signaling receptor exert antibody-dependent cancer cell killing. Cancer Res. 2014, 74:93-103.
52. Bellone M., Calcinotto A. Ways to enhance lymphocyte trafficking into tumors and fitness of tumor infiltrating lymphocytes. Front. Oncol. 2013, 3:231.
53. Huang H., et al. VEGF suppresses T-lymphocyte infiltration in the tumor microenvironment through inhibition of NF-kappaB-induced endothelial activation. FASEB J. 2015, 29:227-238.
54. Adusumilli P.S., et al. Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity. Sci. Transl. Med. 2014, 6:261ra151.
55. Stephan S.B., et al. Biopolymer implants enhance the efficacy of adoptive T-cell therapy. Nat. Biotechnol. 2015, 33:97-101.
56. Kershaw M.H., et al. Redirecting migration of T cells to chemokine secreted from tumors by genetic modification with CXCR2. Hum. Gene Ther. 2002, 13:1971-1980.
57. Peng W., et al. Transduction of tumor-specific T cells with CXCR2 chemokine receptor improves migration to tumor and antitumor immune responses. Clin. Cancer Res. 2010, 16:5458-5468.
58. Conklin B.R., et al. Engineering GPCR signaling pathways with RASSLs. Nat. Methods 2008, 5:673-678.
59. Park J.S., et al. Synthetic control of mammalian-cell motility by engineering chemotaxis to an orthogonal bioinert chemical signal. Proc. Natl. Acad. Sci. U.S.A. 2008, 111:5896-5901.
60. Tey S.K. Adoptive T-cell therapy: adverse events and safety switches. Clin. Transl. Immunol. 2014, 3:e17.
61. Jones B.S., et al. Improving the safety of cell therapy products by suicide gene transfer. Front. Pharmacol. 2014, 5:254.
62. Bonini C., et al. HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science 2014, 276:1719-1724.
63. Marin V., et al. Comparison of different suicide-gene strategies for the safety improvement of genetically manipulated T cells. Hum. Gene Ther. Methods 2012, 23:376-386.
64. Straathof K.C., et al. An inducible caspase 9 safety switch for T-cell therapy. Blood 2005, 105:4247-4254.
65. Budde L.E., et al. Combining a CD20 chimeric antigen receptor and an inducible caspase 9 suicide switch to improve the efficacy and safety of T cell adoptive immunotherapy for lymphoma. PLoS ONE 2005, 8:e82742.
66. Di Stasi A., et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 2005, 365:1673-1683.
67. Zhou X., et al. Long-term outcome after haploidentical stem cell transplant and infusion of T cells expressing the inducible caspase 9 safety transgene. Blood 2014, 123:3895-3905.
68. Arbibe L., et al. An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat. Immunol. 2014, 8:47-56.
69. Yao T., et al. Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, yopH. J. Exp. Med. 1999, 190:1343-1350.
70. Wei P., et al. Bacterial virulence proteins as tools to rewire kinase pathways in yeast and immune cells. Nature 2012, 488:384-388.
71. Chen Y.Y., et al. Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8531-8536.
72. Chmielewski M., et al. IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res. 2010, 71:5697-5706.
73. Atkinson H., Chalmers R. Delivering the goods: viral and non-viral gene therapy systems and the inherent limits on cargo DNA and internal sequences. Genetica 2010, 138:485-498.
74. + T cells. J. Clin. Invest. 2005, 115:1616-1626.
75. Chang C.H., et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 2013, 153:1239-1251.
76. Rathmell J.C., et al. Activated Akt promotes increased resting T cell size, CD28-independent T cell growth, and development of autoimmunity and lymphoma. Eur. J. Immunol. 2003, 33:2223-2232.
77. Jacobs S.R., et al. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 2008, 180:4476-4486.
78. + T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 2008, 118:294-305.
79. Pearce E.L., et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009, 460:103-107.
80. + T cell memory development. Immunity 2012, 36:68-78.
81. Landskron J., et al. Activated regulatory and memory T-cells accumulate in malignant ascites from ovarian carcinoma patients. Cancer Immunol. Immunother. 2015, 64:337-347.
82. Ostrand-Rosenberg S., et al. The programmed death-1 immune-suppressive pathway: barrier to antitumor immunity. J. Immunol. 2014, 193:3835-3841.
83. Zhou P., et al. In vivo discovery of immunotherapy targets in the tumour microenvironment. Nature 2014, 506:52-57.
84. Cong L., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
85. Konermann S., et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 2015, 517:583-588.
86. Malina A., et al. Adapting CRISPR/Cas9 for functional genomics screens. Methods Enzymol. 2014, 546:193-213.
87. Torikai H., et al. A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. Blood 2012, 119:5697-5705.
88. Reyes L.M., et al. Creating class I MHC-null pigs using guide RNA and the Cas9 endonuclease. J. Immunol. 2014, 193:5751-5757.
89. Nakazawa Y., et al. Optimization of the PiggyBac transposon system for the sustained genetic modification of human T lymphocytes. J. Immunother. 2009, 32:826-836.
90. Wu S.C., et al. piggyBac is a flexible and highly active transposon as compared to sleeping beauty, Tol2, and Mos1 in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15008-15013.
91. Singh H., et al. Manufacture of clinical-grade CD19-specific T cells stably expressing chimeric antigen receptor using Sleeping Beauty system and artificial antigen presenting cells. PLoS ONE 2013, 8:e64138.
92. Themeli M., et al. Generation of tumor-targeted human T lymphocytes from induced pluripotent stem cells for cancer therapy. Nat. Biotechnol. 2013, 31:928-933.
93. Klingemann H. Are natural killer cells superior CAR drivers?. Oncoimmunology 2014, 3:e28147.
94. Kruschinski A., et al. Engineering antigen-specific primary human NK cells against HER-2 positive carcinomas. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17481-17486.
95. Freeman A.I., et al. Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol. Ther. 2006, 13:221-228.
96. Russell S.J., et al. Remission of disseminated cancer after systemic oncolytic virotherapy. Mayo Clin. Proc. 2014, 89:926-933.
97. Xie Z., et al. Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science 2011, 333:1307-1311.
98. Davila M.L., et al. CD19 CAR-targeted T cells induce long-term remission and B Cell Aplasia in an immunocompetent mouse model of B cell acute lymphoblastic leukemia. PLoS ONE 2013, 8:e61338.
99. Brentjens R.J., et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013, 5:177ra138.
100. + T cells can mediate antileukemic activity and persist in post-transplant patients. Sci. Transl. Med. 2013, 5:174ra127.
101. Kochenderfer J.N., et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 2012, 119:2709-2720.
102. Kochenderfer J.N., et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood 2010, 116:4099-4102.
103. Badhiwala J., et al. Clinical trials in cellular immunotherapy for brain/CNS tumors. Expert Rev. Neurother. 2013, 13:405-424.
104. Morgan R.A., 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, 23:1043-1053.
105. Kershaw M.H., et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin. Cancer Res. 2006, 12:6106-6115.
106. Crompton J.G., et al. Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics. Cancer Res. 2015, 75:296-305.
107. Lloyd A., et al. Beyond the antigen receptor: editing the genome of T-cells for cancer adoptive cellular therapies. Front. Immunol. 2013, 4:221.
108. Freeman G.J., et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 2000, 192:1027-1034.
109. Pattanayak V., et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 2013, 31:839-843.
110. Pattanayak V., et al. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat. Methods 2011, 8:765-770.
111. Fine E.J., et al. An online bioinformatics tool predicts zinc finger and TALE nuclease off-target cleavage. Nucleic Acids Res. 2014, 42:e42.
112. Montague T.G., et al. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 2014, 42:W401-W407.
113. Silva G., et al. Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr. gene Ther. 2011, 11:11-27.
114. Zaslavskiy M., et al. Efficient design of meganucleases using a machine learning approach. BMC Bioinformat. 2014, 15:191.
115. Joung J.K., Sander J.D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell. Biol 2013, 14:49-55.
116. Urnov F.D., et al. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 2010, 11:636-646.
117. Sander J.D., Joung J.K. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 2014, 32:347-355.
118. Wilkie S., et al. Dual targeting of ErbB2 and MUC1 in breast cancer using chimeric antigen receptors engineered to provide complementary signaling. J. Clin. Immunol. 2012, 32:1059-1070.
119. Lanitis E., et al. Chimeric antigen receptor T cells with dissociated signaling domains exhibit focused antitumor activity with reduced potential for toxicity in vivo. Cancer Immunol. Res. 2013, 1:43-53.