Remote control of therapeutic T cells through a small moleculeâ€"gated chimeric receptor

Science

Volumn 350, Issue 6258, 2015, Pages

  Wu, Chia Yung ^a,b   Roybal, Kole T ^a,b   Puchner, Elias M ^a,c   Onuffer, James ^a,b   Lim, Wendell A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Minnesota   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTIFICIAL RECEPTOR; CHIMERIC ANTIGEN RECEPTOR; ANTIGEN; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MOLECULAR LIBRARY;

ANTIGEN; BIOENGINEERING; CELLS AND CELL COMPONENTS; DOSE-RESPONSE RELATIONSHIP; PROTEIN; TOXICITY; TUMOR;

ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CELL ENGINEERING; CELL THERAPY; CONTROLLED STUDY; CYTOARCHITECTURE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; INTRACELLULAR SIGNALING; LYMPHOCYTE FUNCTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REGULATORY MECHANISM; T LYMPHOCYTE; ADVERSE EFFECTS; AGONISTS; ANIMAL; BIOLOGICAL THERAPY; DRUG EFFECTS; DRUG SCREENING; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MOLECULAR LIBRARY; MOUSE; NEOPLASMS; PHARMACOLOGY; PROCEDURES; TRANSPLANTATION;

ANIMALS; ANTIGENS; CELL ENGINEERING; CELL- AND TISSUE-BASED THERAPY; GENETIC ENGINEERING; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MICE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; SMALL MOLECULE LIBRARIES; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84945217637     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aab4077     Document Type: Article

References (57)

1. J. A. Bluestone, H. Bour-Jordan, Current and future immunomodulation strategies to restore tolerance in autoimmune diseases. Cold Spring Harb. Perspect. Biol. 4, a007542 (2012). doi: 10.1101/cshperspect.a007542
2. M. Sadelain, R. Brentjens, I. Riviére, The basic principles of chimeric antigen receptor design. Cancer Discov. 3, 388-398 (2013). doi: 10.1158/2159-8290.CD-12-0548; pmid: 23550147
3. M. Kalos, C. H. June, Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 39, 49-60 (2013). doi: 10.1016/j.immuni.2013.07.002; pmid: 23890063
4. J. N. Kochenderfer, S. A. Rosenberg, Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat. Rev. Clin. Oncol. 10, 267-276 (2013). doi: 10.1038/nrclinonc.2013.46
5. N. Gupta et al., Neural stem cell engraftment and myelination in the human brain. Sci. Transl. Med. 4, 155ra137 (2012). pmid: 23052294
6. P. Lu et al., Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 150, 1264-1273 (2012). doi: 10.1016/j.cell.2012.08.020; pmid: 22980985
7. M. A. Fischbach, J. A. Bluestone, W. A. Lim, Cell-based therapeutics: The next pillar of medicine. Sci. Transl. Med. 5, 179ps7 (2013). doi: 10.1126/scitranslmed.3005568; pmid: 23552369
8. C. Mason, D. A. Brindley, E. J. Culme-Seymour, N. L. Davie, Cell therapy industry: Billion dollar global business with unlimited potential. Regen. Med. 6, 265-272 (2011). doi: 10.2217/rme.11.28; pmid: 21548728
9. H. Ye, D. Aubel, M. Fussenegger, Synthetic mammalian gene circuits for biomedical applications. Curr. Opin. Chem. Biol. 17, 910-917 (2013). doi: 10.1016/j.cbpa.2013.10.006; pmid: 24466575
10. M. R. Roberts et al., Targeting of human immunodeficiency virus-infected cells by CD8+ T lymphocytes armed with universal T-cell receptors. Blood 84, 2878-2889 (1994). pmid: 7949163
11. M. Kalos et al., T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3, 95ra73 (2011). pmid: 21832238
12. J. N. Kochenderfer 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 119, 2709-2720 (2012). pmid: 22160384
13. S. A. Grupp et al., Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 368, 1509-1518 (2013). doi: 10.1056/NEJMoa1215134; pmid: 23527958
14. M. L. Davila et al., Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci. Transl. Med. 6, 224ra25 (2014). doi: 10.1126/scitranslmed.3008226; pmid: 24553386
15. M. V. Maus, S. A. Grupp, D. L. Porter, C. H. June, Antibodymodified T cells: CARs take the front seat for hematologic malignancies. Blood 123, 2625-2635 (2014). doi: 10.1182/blood-2013-11-492231
16. R. A. Morgan 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. 18, 843-851 (2010). doi: 10.1038/mt.2010.24; pmid: 20179677
17. F. Ciceri et al., Infusion of suicide-gene-engineered donor lymphocytes after family haploidentical haemopoietic stem-cell transplantation for leukaemia (the TK007 trial): A nonrandomised phase I-II study. Lancet Oncol. 10, 489-500 (2009). doi: 10.1016/S1470-2045(09)70074-9; pmid: 19345145
18. T. Sato et al., Engineered human tmpk/AZT as a novel enzyme/prodrug axis for suicide gene therapy. Mol. Ther. 15, 962-970 (2007). doi: 10.1038/mt.sj.6300122; pmid: 17375075
19. V. D. Fedorov, M. Themeli, M. Sadelain, PD-1-and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert offtarget immunotherapy responses. Sci. Transl. Med. 5, 215ra172 (2013). doi: 10.1126/scitranslmed.3006597; pmid: 24337479
20. J. D. Byrne et al., Local iontophoretic administration of cytotoxic therapies to solid tumors. Sci. Transl. Med. 7, 273ra14 (2015). doi: 10.1126/scitranslmed.3009951; pmid: 25653220
21. W. Lim, B. Mayer, T. Pawson, Cell Signaling (Garland Science, New York, 2014
22. A. Weiss, D. R. Littman, Signal transduction by lymphocyte antigen receptors. Cell 76, 263-274 (1994). doi: 10.1016/0092-8674(94)90334-4; pmid: 8293463
23. I. A. Graef, L. J. Holsinger, S. Diver, S. L. Schreiber, G. R. Crabtree, Proximity and orientation underlie signaling by the non-receptor tyrosine kinase ZAP70. EMBO J. 16, 5618-5628 (1997). doi: 10.1093/emboj/16.18.5618; pmid: 9312021
24. A. Di Stasi et al., Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365, 1673-1683 (2011). doi: 10.1056/NEJMoa1106152; pmid: 22047558
25. J. H. Bayle et al., Rapamycin analogs with differential binding specificity permit orthogonal control of protein activity. Chem. Biol. 13, 99-107 (2006). doi: 10.1016/j. chembiol.2005.10.017; pmid: 16426976
26. S. D. Liberles, S. T. Diver, D. J. Austin, S. L. Schreiber, Inducible gene expression and protein translocation using nontoxic ligands identified by a mammalian three-hybrid screen. Proc. Natl. Acad. Sci. U.S.A. 94, 7825-7830 (1997). doi: 10.1073/pnas.94.15.7825; pmid: 9223271
27. J. Choi, J. Chen, S. L. Schreiber, J. Clardy, Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 273, 239-242 (1996). doi: 10.1126/science.273.5272.239; pmid: 8662507
28. J. Lin, A. Weiss, The tyrosine phosphatase CD148 is excluded from the immunologic synapse and down-regulates prolonged T cell signaling. J. Cell Biol. 162, 673-682 (2003). doi: 10.1083/jcb.200303040; pmid: 12913111
29. J. Wu et al., An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285, 730-732 (1999). doi: 10.1126/science.285.5428.730; pmid: 10426994
30. B. A. Irving, A. C. Chan, A. Weiss, Functional characterization of a signal transducing motif present in the T cell antigen receptor zeta chain. J. Exp. Med. 177, 1093-1103 (1993). doi: 10.1084/jem.177.4.1093; pmid: 8459204
31. C. S. Guy et al., Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat. Immunol. 14, 262-270 (2013). pmid: 23377202
32. M. C. Milone et al., Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17, 1453-1464 (2009). doi: 10.1038/mt.2009.83; pmid: 19384291
33. T. Miyamoto et al., Rapid and orthogonal logic gating with a gibberellin-induced dimerization system. Nat. Chem. Biol. 8, 465-470 (2012). doi: 10.1038/nchembio.922; pmid: 22446836
34. K. Murase, Y. Hirano, T. P. Sun, T. Hakoshima, Gibberellininduced DELLA recognition by the gibberellin receptor GID1. Nature 456, 459-463 (2008). doi: 10.1038/nature07519; pmid: 19037309
35. S. Manley et al., High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155-157 (2008). doi: 10.1038/nmeth.1176; pmid: 18193054
36. E. M. Puchner, J. M. Walter, R. Kasper, B. Huang, W. A. Lim, Counting molecules in single organelles with superresolution microscopy allows tracking of the endosome maturation trajectory. Proc. Natl. Acad. Sci. U.S.A. 110, 16015-16020 (2013). doi: 10.1073/pnas.1309676110; pmid: 24043832
37. E. Betzig et al., Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645 (2006). doi: 10.1126/science.1127344; pmid: 16902090
38. A. D. Douglass, R. D. Vale, Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121, 937-950 (2005). doi: 10.1016/j.cell.2005.04.009; pmid: 15960980
39. P. E. Simms, T. M. Ellis, Utility of flow cytometric detection of CD69 expression as a rapid method for determining poly-and oligoclonal lymphocyte activation. Clin. Diagn. Lab. Immunol. 3, 301-304 (1996). pmid: 8705673
40. O. Boyman, J. Sprent, The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12, 180-190 (2012). pmid: 22343569
41. H. Ikeda, L. J. Old, R. D. Schreiber, The roles of IFNg in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 13, 95-109 (2002). doi: 10.1016/S1359-6101(01)00038-7; pmid: 11900986
42. J. B. Huppa, M. Gleimer, C. Sumen, M. M. Davis, Continuous T cell receptor signaling required for synapse maintenance and full effector potential. Nat. Immunol. 4, 749-755 (2003). doi: 10.1038/ni951; pmid: 12858171
43. M. A. Purbhoo, D. J. Irvine, J. B. Huppa, M. M. Davis, T cell killing does not require the formation of a stable mature immunological synapse. Nat. Immunol. 5, 524-530 (2004). doi: 10.1038/ni1058; pmid: 15048111
44. A. Ray, B. Dittel, J. Visual. Exp. www.jove.com/video/1488/isolation-of-mouse-peritoneal-cavity-cells (2010). doi: 10.3791/1488
45. H. Ye, Y. C. Park, M. Kreishman, E. Kieff, H. Wu, The structural basis for the recognition of diverse receptor sequences by TRAF2. Mol. Cell 4, 321-330 (1999). doi: 10.1016/S1097-2765 (00)80334-2; pmid: 10518213
46. I. K. Jang, Z. H. Lee, Y. J. Kim, S. H. Kim, B. S. Kwon, Human 4-1BB (CD137) signals are mediated by TRAF2 and activate nuclear factor-kB. Biochem. Biophys. Res. Commun. 242, 613-620 (1998). doi: 10.1006/bbrc.1997.8016; pmid: 9464265
47. Y. Y. Chen, M. C. Jensen, C. D. Smolke, Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. Proc. Natl. Acad. Sci. U.S.A. 107, 8531-8536 (2010). doi: 10.1073/pnas.1001721107; pmid: 20421500
48. J. S. Park et al., Synthetic control of mammalian-cell motility by engineering chemotaxis to an orthogonal bioinert chemical signal. Proc. Natl. Acad. Sci. U.S.A. 111, 5896-5901 (2014). doi: 10.1073/pnas.1402087111; pmid: 24711398
49. A. Bishop et al., Unnatural ligands for engineered proteins: New tools for chemical genetics. Annu. Rev. Biophys. Biomol. Struct. 29, 577-606 (2000). doi: 10.1146/annurev.biophys.29.1.577; pmid: 10940260
50. L. A. Banaszynski, T. J. Wandless, Conditional control of protein function. Chem. Biol. 13, 11-21 (2006). doi: 10.1016/j.chembiol.2005.10.010; pmid: 16426967
51. W. Bacchus, M. Fussenegger, The use of light for engineered control and reprogramming of cellular functions. Curr. Opin. Biotechnol. 23, 695-702 (2012). doi: 10.1016/j.copbio.2011.12.004; pmid: 22204821
52. J. E. Toettcher, D. Gong, W. A. Lim, O. D. Weiner, Light-based feedback for controlling intracellular signaling dynamics. Nat. Methods 8, 837-839 (2011). doi: 10.1038/nmeth.1700; pmid: 21909100
53. A. Levskaya, O. D. Weiner, W. A. Lim, C. A. Voigt, Spatiotemporal control of cell signalling using a lightswitchable protein interaction. Nature 461, 997-1001 (2009). doi: 10.1038/nature08446; pmid: 19749742
54. M. J. Kennedy et al., Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 7, 973-975 (2010). doi: 10.1038/nmeth.1524; pmid: 21037589
55. Y. I. Wu et al., A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104-108 (2009). doi: 10.1038/nature08241; pmid: 19693014
56. K. E. Prehoda, J. A. Scott, R. D. Mullins, W. A. Lim, Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801-806 (2000). doi: 10.1126/science.290.5492.801; pmid: 11052943
57. J. E. Dueber, B. J. Yeh, R. P. Bhattacharyya, W. A. Lim, Rewiring cell signaling: The logic and plasticity of eukaryotic protein circuitry. Curr. Opin. Struct. Biol. 14, 690-699 (2004). doi: 10.1016/j.sbi.2004.10.004; pmid: 15582393