The journey from discoveries in fundamental immunology to cancer immunotherapy

Cancer Cell

Volumn 27, Issue 4, 2015, Pages 439-449

  Miller, Jacques F A P ^a   Sadelain, Michel ^b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMP 224; ANTINEOPLASTIC AGENT; BMS 935559; CANCER VACCINE; CHIMERIC ANTIGEN RECEPTOR; CYCLOPHOSPHAMIDE; DURVALUMAB; MONOCLONAL ANTIBODY; MPDL 3280A; MSB 0010718C; NIVOLUMAB; PEMBROLIZUMAB; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PIDILIZUMAB; UNCLASSIFIED DRUG;

B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CELL ENGINEERING; CELLULAR IMMUNITY; HUMAN; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LEUKEMOGENESIS; MELANOMA; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMUS; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; MOUSE; NEOPLASMS; PHYSIOLOGY; RESEARCH; TRENDS;

ALLERGY AND IMMUNOLOGY; ANIMALS; B-LYMPHOCYTES; CANCER VACCINES; HUMANS; IMMUNOLOGIC SURVEILLANCE; IMMUNOTHERAPY; MICE; NEOPLASMS; RESEARCH; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84928056873     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.03.007     Document Type: Review

References (147)

1. Abu-Eid R., Samara R.N., Ozbun L., Abdalla M.Y., Berzofsky J.A., Friedman K.M., Mkrtichyan M., Khleif S.N. Selective inhibition of regulatory Tcells by targeting the PI3K-Akt pathway. Cancer Immunol Res 2014, 2:1080-1089.
2. Alexandrov L.B., Nik-Zainal S., Wedge D.C., Aparicio S.A., Behjati S., Biankin A.V., Bignell G.R., Bolli N., Borg A., Børresen-Dale A.L., et al. Signatures of mutational processes in human cancer. Nature 2013, 500:415-421. Australian Pancreatic Cancer Genome Initiative, ICGC Breast Cancer ConsortiumICGC Breast Cancer Consortium, ICGC MMML-Seq ConsortiumICGC MMML-Seq Consortium, ICGC PedBrainICGC PedBrain.
3. Asseman C., Mauze S., Leach M.W., Coffman R.L., Powrie F. An essential role for interleukin 10 in the function of regulatory Tcells that inhibit intestinal inflammation. J.Exp. Med. 1999, 190:995-1004.
4. August C.S., Berkel A.I., Levey R.H., Rosen F.S., Kay H.E. Establishment of immunological competence in a child with congenital thymic aplasia by a graft of fetal thymus. Lancet 1970, 1:1080-1083.
5. Berger M.F., Hodis E., Heffernan T.P., Deribe Y.L., Lawrence M.S., Protopopov A., Ivanova E., Watson I.R., Nickerson E., Ghosh P., et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 2012, 485:502-506.
6. Bevan M.J. In a radiation chimaera, host H-2 antigens determine immune responsiveness of donor cytotoxic cells. Nature 1977, 269:417-418.
7. Boon T., Van den Eynde B., Hirsch H., Moroni C., De Plaen E., van der Bruggen P., De Smet C., Lurquin C., Szikora J.P., De Backer O. Genes coding for tumor-specific rejection antigens. Cold Spring Harb. Symp. Quant. Biol. 1994, 59:617-622.
8. Bredenkamp N., Ulyanchenko S., O'Neill K.E., Manley N.R., Vaidya H.J., Blackburn C.C. An organized and functional thymus generated from FOXN1-reprogrammed fibroblasts. Nat. Cell Biol. 2014, 16:902-908.
9. Brentjens R.J., Latouche J.B., Santos E., Marti F., Gong M.C., Lyddane C., King P.D., Larson S., Weiss M., Rivière I., Sadelain M. Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat. Med. 2003, 9:279-286.
10. Brentjens R.J., Davila M.L., Riviere I., Park J., Wang X., Cowell L.G., Bartido S., Stefanski J., Taylor C., Olszewska M., et al. CD19-targeted Tcells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013, 5:77ra38.
11. Brocker T. Chimeric Fv-zeta or Fv-epsilon receptors are not sufficient to induce activation or cytokine production in peripheral Tcells. Blood 2000, 96:1999-2001.
12. Brocker T., Peter A., Traunecker A., Karjalainen K. New simplified molecular design for functional Tcell receptor. Eur. J. Immunol. 1993, 23:1435-1439.
13. Bunnell B.A., Muul L.M., Donahue R.E., Blaese R.M., Morgan R.A. High-efficiency retroviral-mediated gene transfer into human and nonhuman primate peripheral blood lymphocytes. Proc. Natl. Acad. Sci. USA 1995, 92:7739-7743.
14. Burnet F.M. The thymus gland. Sci. Am. 1962, 207:50-57.
15. Burnet F.M. Immunological surveillance in neoplasia. Transplant. Rev. 1971, 7:3-25.
16. Cantor H., Boyse E.A. Functional subclasses of T-lymphocytes bearing different Ly antigens. I. The generation of functionally distinct T-cell subclasses is a differentiative process independent of antigen. J.Exp. Med. 1975, 141:1376-1389.
17. Chen Y.T., Scanlan M.J., Sahin U., Türeci O., Gure A.O., Tsang S., Williamson B., Stockert E., Pfreundschuh M., Old L.J. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl. Acad. Sci. USA 1997, 94:1914-1918.
18. Chinnasamy D., Yu Z., Kerkar S.P., Zhang L., Morgan R.A., Restifo N.P., Rosenberg S.A. Local delivery of interleukin-12 using Tcells targeting VEGF receptor-2 eradicates multiple vascularized tumors in mice. Clin. Cancer Res. 2012, 18:1672-1683.
19. Chmielewski M., Abken H. CAR Tcells transform to trucks: chimeric antigen receptor-redirected Tcells engineered to deliver inducible IL-12 modulate the tumour stroma to combat cancer. Cancer Immunol. Immunother. 2012, 61:1269-1277.
20. Claman H.N., Chaperon E.A., Triplett R.F. Thymus-marrow cell combinations. Synergism in antibody production. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine 1966, 122:1167-1171.
21. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., Sehy D., Blumberg R.S., Vignali D.A.A. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007, 450:566-569.
22. Coulie P.G., Van den Eynde B.J., van der Bruggen P., Boon T. Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat. Rev. Cancer 2014, 14:135-146.
23. Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunotherapy. Science 2013, 342:1432-1433.
24. Croft M. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity?. Nat. Rev. Immunol. 2003, 3:609-620.
25. Cross A.M., Leuchars E., Miller J.F. Studies on the recovery of the immune response in irradiated mice thymectomized in adult life. J.Exp. Med. 1964, 119:837-850.
26. Curiel T.J. Tregs and rethinking cancer immunotherapy. J.Clin. Invest. 2007, 117:1167-1174.
27. Curran M.A., Montalvo W., Yagita H., Allison J.P. PD-1 and CTLA-4 combination blockade expands infiltrating Tcells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl. Acad. Sci. USA 2010, 107:4275-4280.
28. Davila M.L., Riviere I., Wang X., Bartido S., Park J., Curran K., Chung S.S., Stefanski J., Borquez-Ojeda O., Olszewska M., et al. Efficacy and toxicity management of 19-28z CAR Tcell therapy in B cell acute lymphoblastic leukemia. Sci. Transl. Med. 2014, 6:24ra25.
29. Delgoffe G.M., Woo S.-R., Turnis M.E., Gravano D.M., Guy C., Overacre A.E., Bettini M.L., Vogel P., Finkelstein D., Bonnevier J., et al. Stability and function of regulatory Tcells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 2013, 501:252-256.
30. Dembić Z., Haas W., Weiss S., McCubrey J., Kiefer H., von Boehmer H., Steinmetz M. Transfer of specificity by murine alpha and beta T-cell receptor genes. Nature 1986, 320:232-238.
31. Dranoff G., Jaffee E., Lazenby A., Golumbek P., Levitsky H., Brose K., Jackson V., Hamada H., Pardoll D., Mulligan R.C. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA 1993, 90:3539-3543.
32. Duong C.P., Westwood J.A., Berry L.J., Darcy P.K., Kershaw M.H. Enhancing the specificity of T-cell cultures for adoptive immunotherapy of cancer. Immunotherapy 2011, 3:33-48.
33. Ehrlich P., Himmelweit F. The Collected Papers of Paul Ehrlich 1957, Pergamon Press, Oxford.
34. Eshhar Z., Waks T., Gross G., Schindler D.G. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc. Natl. Acad. Sci. USA 1993, 90:720-724.
35. Eshhar Z., Bach N., Fitzer-Attas C.J., Gross G., Lustgarten J., Waks T., Schindler D.G. The T-body approach: potential for cancer immunotherapy. Springer Semin. Immunopathol. 1996, 18:199-209.
36. European Society for Medical Oncology (2014). Immune checkpoint inhibitors provide antitumour activity across malignant diseases. http://www.esmo.org/Conferences/Past-Conferences/ESMO-2014-Congress.
37. Fedorov V.D., Themeli M., Sadelain M. PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci. Transl. Med. 2013, 5:ra172.
38. Finney H.M., Lawson A.D., Bebbington C.R., Weir A.N. Chimeric receptors providing both primary and costimulatory signaling in Tcells from a single gene product. J.Immunol. 1998, 161:2791-2797.
39. Fischer A., Hacein-Bey-Abina S., Cavazzana-Calvo M. Gene therapy of primary Tcell immunodeficiencies. Gene 2013, 525:170-173.
40. Gallardo H.F., Tan C., Ory D., Sadelain M. Recombinant retroviruses pseudotyped with the vesicular stomatitis virus G glycoprotein mediate both stable gene transfer and pseudotransduction in human peripheral blood lymphocytes. Blood 1997, 90:952-957.
41. Gattinoni L., Powell D.J., Rosenberg S.A., Restifo N.P. Adoptive immunotherapy for cancer: building on success. Nat. Rev. Immunol. 2006, 6:383-393.
42. Ghiringhelli F., Menard C., Puig P.E., Ladoire S., Roux S., Martin F., Solary E., Le Cesne A., Zitvogel L., Chauffert B. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory Tcells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol. Immunother. 2007, 56:641-648.
43. Godfrey D.I., MacDonald R., Kronenberg M., Smyth M.J., van Kaer L. NKT cells: what's in a name?. Nat. Rev. Immunol. 2004, 4:231-237.
44. Gold D.P., Puck J.M., Pettey C.L., Cho M., Coligan J., Woody J.N., Terhorst C. Isolation of cDNA clones encoding the 20K non-glycosylated polypeptide chain of the human T-cell receptor/T3 complex. Nature 1986, 321:431-434.
45. Gong M.C., Latouche J.B., Krause A., Heston W.D., Bander N.H., Sadelain M. Cancer patient Tcells genetically targeted to prostate-specific membrane antigen specifically lyse prostate cancer cells and release cytokines in response to prostate-specific membrane antigen. Neoplasia 1999, 1:123-127.
46. Good R.A. Discussion after Miller, J.F.A.P. Immunological Tolerance: A Reassessment of Mechanisms of the Immune Response 1969, 136. Academic Press, New York. M. Landy, W. Braun (Eds.).
47. Gowans J.L. Discussion after Miller, J.F.A.P. Immunological Tolerance: A Reassessment of Mechanisms of the Immune Response 1969, 164-169. Academic Press, New York. M. Landy, W. Braun (Eds.).
48. Gowans J.L., McGregor D.D., Cowen D.M. Initiation of immune responses by small lymphocytes. Nature 1962, 196:651-655.
49. Gross L. Pathogenic properties, and "vertical" transmission of the mouse leukemia agent. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine 1951, 78:342-348.
50. Grupp S.A., Kalos M., Barrett D., Aplenc R., Porter D.L., Rheingold S.R., Teachey D.T., Chew A., Hauck B., Wright J.F., et al. Chimeric antigen receptor-modified Tcells for acute lymphoid leukemia. N.Engl. J. Med. 2013, 368:1509-1518.
51. Gubin M.M., Zhang X., Schuster H., Caron E., Ward J.P., Noguchi T., Ivanova Y., Hundal J., Arthur C.D., Krebber W.-J., et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 2014, 515:577-581.
52. Harding F.A., McArthur J.G., Gross J.A., Raulet D.H., Allison J.P. CD28-mediated signalling co-stimulates murine Tcells and prevents induction of anergy in T-cell clones. Nature 1992, 356:607-609.
53. Hedrick S.M., Cohen D.I., Nielsen E.A., Davis M.M. Isolation of cDNA clones encoding Tcell-specific membrane-associated proteins. Nature 1984, 308:149-153.
54. Heslop H.E., Ng C.Y., Li C., Smith C.A., Loftin S.K., Krance R.A., Brenner M.K., Rooney C.M. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat. Med. 1996, 2:551-555.
55. Ho W.Y., Blattman J.N., Dossett M.L., Yee C., Greenberg P.D. Adoptive immunotherapy: engineering Tcell responses as biologic weapons for tumor mass destruction. Cancer Cell 2003, 3:431-437.
56. Hombach A., Wieczarkowiecz A., Marquardt T., Heuser C., Usai L., Pohl C., Seliger B., Abken H. Tumor-specific Tcell activation by recombinant immunoreceptors: CD3 zeta signaling and CD28 costimulation are simultaneously required for efficient IL-2 secretion and can be integrated into one combined CD28/CD3 zeta signaling receptor molecule. J.Immunol. 2001, 167:6123-6131.
57. Hoyos V., Savoldo B., Quintarelli C., Mahendravada A., Zhang M., Vera J., Heslop H.E., Rooney C.M., Brenner M.K., Dotti G. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 2010, 24:1160-1170.
58. Huang P., Westmoreland S.V., Jain R.K., Fukumura D. Spontaneous nonthymic tumors in SCID mice. Comp. Med. 2011, 61:227-234.
59. Hudson L., Sprent J., Miller J.F., Playfair J.H.L. B cell-derived immunoglobulin on activated mouse T lymphocytes. Nature 1974, 251:60-62.
60. Imai C., Mihara K., Andreansky M., Nicholson I.C., Pui C.H., Geiger T.L., Campana D. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004, 18:676-684.
61. Irving B.A., Weiss A. The cytoplasmic domain of the Tcell receptor zeta chain is sufficient to couple to receptor-associated signal transduction pathways. Cell 1991, 64:891-901.
62. Iwai Y., Ishida M., Tanaka Y., Okazaki T., Honjo T., Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. USA 2002, 99:12293-12297.
63. Jensen M.C., Riddell S.R. Designing chimeric antigen receptors to effectively and safely target tumors. Curr. Opin. Immunol. 2015, 33C:9-15.
64. Josefowicz S.Z., Lu L.-F., Rudensky A.Y. Regulatory Tcells: mechanisms of differentiation and function. Annu. Rev. Immunol. 2012, 30:531-564.
65. Kappler J.W., Roehm N., Marrack P. T cell tolerance by clonal elimination in the thymus. Cell 1987, 49:273-280.
66. Keir M.E., Butte M.J., Freeman G.J., Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008, 26:677-704.
67. H nucleotide sequences in Tcells. J.Exp. Med. 1982, 156:1848-1853.
68. Kim J.V., Latouche J.B., Rivière I., Sadelain M. The ABCs of artificial antigen presentation. Nat. Biotechnol. 2004, 22:403-410.
69. Kisielow P., Hirst J.A., Shiku H., Beverley P.C.L., Hoffman M.K., Boyse E.A., Oettgen H.F. Ly antigens as markers for functionally distinct subpopulations of thymus-derived lymphocytes of the mouse. Nature 1975, 253:219-220.
70. Kloss C.C., Condomines M., Cartellieri M., Bachmann M., Sadelain M. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered Tcells. Nat. Biotechnol. 2013, 31:71-75.
71. Kochenderfer J.N., Rosenberg S.A. Treating B-cell cancer withTcells expressing anti-CD19 chimeric antigen receptors. Nat. Rev. Clin. Oncol. 2013, 10:267-276.
72. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 1975, 256:495-497.
73. Krause A., Guo H.F., Latouche J.B., Tan C., Cheung N.K., Sadelain M. Antigen-dependent CD28 signaling selectively enhances survival and proliferation in genetically modified activated human primary T lymphocytes. J.Exp. Med. 1998, 188:619-626.
74. Krummel M.F., Allison J.P. Pillars article: CD28 and CTLA-4 have opposing effects on the response of Tcells to stimulation. The journal of experimental medicine. 1995. 182: 459-465. J.Immunol. 2011, 187:3459-3465.
75. Lafferty K.J., Cunningham A.J. A new analysis of allogeneic interactions. Aust. J. Exp. Biol. Med. Sci. 1975, 53:27-42.
76. Leach D.R., Krummel M.F., Allison J.P. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996, 271:1734-1736.
77. Lee D.W., Kochenderfer J.N., Stetler-Stevenson M., Cui Y.K., Delbrook C., Feldman S.A., Fry T.J., Orentas R., Sabatino M., Shah N.N., et al. Tcells 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.
78. Letourneur F., Klausner R.D. T-cell and basophil activation through the cytoplasmic tail of T-cell-receptor zeta family proteins. Proc. Natl. Acad. Sci. USA 1991, 88:8905-8909.
79. Maher J., Brentjens R.J., Gunset G., Rivière I., Sadelain M. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta /CD28 receptor. Nat. Biotechnol. 2002, 20:70-75.
80. Makino Y., Kanno R., Ito T., Higashino K., Taniguchi M. Predominant expression of invariant V α 14+ TCR α chain in NK1.1+ Tcell populations. Int. Immunol. 1995, 7:1157-1161.
81. Marchalonis J.J., Cone R.E., Atwell J.L. Isolation and partial characterization of lymphocyte surface immunoglobulins. J.Exp. Med. 1972, 135:956-971.
82. Markley J.C., Sadelain M. IL-7 and IL-21 are superior to IL-2 and IL-15 in promoting human Tcell-mediated rejection of systemic lymphoma in immunodeficient mice. Blood 2010, 115:3508-3519.
83. Maude S.L., Frey N., Shaw P.A., Aplenc R., Barrett D.M., Bunin N.J., Chew A., Gonzalez V.E., Zheng Z., Lacey S.F., et al. Chimeric antigen receptor Tcells for sustained remissions in leukemia. N.Engl. J. Med. 2014, 371:1507-1517.
84. Mavilio F., Ferrari G., Rossini S., Nobili N., Bonini C., Casorati G., Traversari C., Bordignon C. Peripheral blood lymphocytes as target cells of retroviral vector-mediated gene transfer. Blood 1994, 83:1988-1997.
85. McIntire K.R., Sell S., Miller J.F. Pathogenesis of the post-neonatal thymectomy wasting syndrome. Nature 1964, 204:151-155.
86. Miller J.F. Role of the thymus in murine leukaemia. Nature 1959, 183:1069.
87. Miller J.F. Fate of subcutaneous thymus grafts in thymectomized mice inoculated with leukaemic filtrate. Nature 1959, 184(23):1809-1810.
88. Miller J.F. Recovery of leukaemogenic agent from nonleukaemic tissues of thymectomized mice. Nature 1960, 187:703.
89. Miller J.F. Etiology and pathogenesis of mouse leukemia. Advances in Cancer Research 1961, 291-368. Academic Press, New York. A. Haddow, S. Weinhouse (Eds.).
90. Miller J.F. Immunological function of the thymus. Lancet 1961, 2:748-749.
91. Miller J.F. Effect of neonatal thymectomy on the immunological responsiveness of the mouse. Proc. R. Soc. Lond. B Biol. Sci. 1962, 156:415-428.
92. Miller J.F. Immunological significance of the thymus of the adult mouse. Nature 1962, 195:1318-1319.
93. Miller J.F. The thymus in relation to neoplasia. Modern Trends in Pathology 1967, Volume 2:140-175. Butterworths, London.
94. Miller J.F. The golden anniversary of the thymus. Nat. Rev. Immunol. 2011, 11:489-495.
95. Miller J.F., Mitchell G.F. The thymus and the precursors of antigen-reactive cells. Nature 1967, 216:659-663.
96. Miller J.F., Mitchell G.F. Cell to cell interaction in the immune response. I. Hemolysin-forming cells in neonatally thymectomized mice reconstituted with thymus or thoracic duct lymphocytes. J.Exp. Med. 1968, 128:801-820.
97. Miller J.F., Mitchell G.F. Thymus and antigen-reactive cells. Transplant. Rev. 1969, 1:3-42.
98. Miller J.F., Sprent J. Thymus-derived cells in mouse thoracic duct lymph. Nat. New Biol. 1971, 230:267-270.
99. Miller J.F., Grant G.A., Roe F.J. Effect of thymectomy on the induction of skin tumours by 3,4-benzopyrene. Nature 1963, 199:920-922.
100. Miller J.F., Law L.W., Ting R.C. Influence of thymectomy on tumor induction by polyoma virus in C57BL mice. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine 1964, 116:323-327.
101. Miller J.F., De Burgh P.M., Grant G.A. Thymus and the production of antibody-plaque-forming cells. Nature 1965, 208:1332-1334.
102. Miller J.F., Mitchell G.F., Weiss N.S. Cellular basis of the immunological defects in thymectomized mice. Nature 1967, 214:992-997.
103. Mitchell G.F., Miller J.F. Cell to cell interaction in the immune response. II. The source of hemolysin-forming cells in irradiated mice given bone marrow and thymus or thoracic duct lymphocytes. J.Exp. Med. 1968, 128:821-837.
104. Nishimura T., Kaneko S., Kawana-Tachikawa A., Tajima Y., Goto H., Zhu D., Nakayama-Hosoya K., Iriguchi S., Uemura Y., Shimizu T., et al. Generation of rejuvenated antigen-specific Tcells by reprogramming to pluripotency and redifferentiation. Cell Stem Cell 2013, 12:114-126.
105. Oettgen H.C., Terhorst C., Cantley L.C., Rosoff P.M. Stimulation of the T3-T cell receptor complex induces a membrane-potential-sensitive calcium influx. Cell 1985, 40:583-590.
106. Okazaki T., Honjo T. PD-1 and PD-1 ligands: from discovery to clinical application. Int. Immunol. 2007, 19:813-824.
107. Ostrand-Rosenberg S. Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol. Immunother. 2010, 59:1593-1600.
108. Papadopoulos E.B., Ladanyi M., Emanuel D., Mackinnon S., Boulad F., Carabasi M.H., Castro-Malaspina H., Childs B.H., Gillio A.P., Small T.N., et al. Infusions of donor leukocytes to treat Epstein-Barr virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N.Engl. J. Med. 1994, 330:1185-1191.
109. Pardoll D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12:252-264.
110. Pegram H.J., Lee J.C., Hayman E.G., Imperato G.H., Tedder T.F., Sadelain M., Brentjens R.J. Tumor-targeted Tcells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood 2012, 119:4133-4141.
111. Penn I., Starzl T.E. Immunosuppression and cancer. Transplant. Proc. 1973, 5:943-947.
112. + Tcells. J.Exp. Med. 1996, 183:2669-2674.
113. Prosser M.E., Brown C.E., Shami A.F., Forman S.J., Jensen M.C. Tumor PD-L1 co-stimulates primary human CD8(+) cytotoxic Tcells modified to express a PD1:CD28 chimeric receptor. Mol. Immunol. 2012, 51:263-272.
114. Qureshi O.S., Zheng Y., Nakamura K., Attridge K., Manzotti C., Schmidt E.M., Baker J., Jeffery L.E., Kaur S., Briggs Z., et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2011, 332:600-603.
115. Ramos C.A., Savoldo B., Dotti G. CD19-CAR trials. Cancer J. 2014, 20:112-118.
116. Robbins P.F., Morgan R.A., Feldman S.A., Yang J.C., Sherry R.M., Dudley M.E., Wunderlich J.R., Nahvi A.V., Helman L.J., Mackall C.L., et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J.Clin. Oncol. 2011, 29:917-924.
117. Romeo C., Seed B. Cellular immunity to HIV activated by CD4 fused to Tcell or Fc receptor polypeptides. Cell 1991, 64:1037-1046.
118. Rosenberg S.A., Spiess P., Lafreniere R. A new approach to theadoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 1986, 233:1318-1321.
119. Rygaard J. Thymus and Self: Immunobiology of the Mouse Mutant Nude 1973, F.A.D.L., København.
120. Rygaard J., Povlsen C.O. The nude mouse vs. the hypothesis of immunological surveillance. Transplant. Rev. 1976, 28:43-61.
121. Sadelain M., Rivière I., Brentjens R. Targeting tumours with genetically enhanced T lymphocytes. Nat. Rev. Cancer 2003, 3:35-45.
122. Sadelain M., Brentjens R., Rivière I. The promise and potential pitfalls of chimeric antigen receptors. Curr. Opin. Immunol. 2009, 21:215-223.
123. Sadelain M., Brentjens R., Rivière I. The basic principles of chimeric antigen receptor design. Cancer Discov 2013, 3:388-398.
124. Sakaguchi S., Powrie F. Emerging challenges in regulatory Tcell function and biology. Science 2007, 317:627-629.
125. Sakaguchi S., Fukuma K., Kuribayashi K., Masuda T. Organ-specific autoimmune diseases induced in mice by elimination of Tcell subset. I. Evidence for the active participation of Tcells in natural self-tolerance; deficit of a Tcell subset as a possible cause of autoimmune disease. J.Exp. Med. 1985, 161:72-87.
126. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565-1570.
127. Schubert D., Bode C., Kenefeck R., Hou T.Z., Wing J.B., Kennedy A., Bulashevska A., Petersen B.S., Schäffer A.A., Grüning B.A., et al. Autosomal dominant immune dysregulation syndrome in humans with CTLA4 mutations. Nat. Med. 2014, 20:1410-1416.
128. Seliger B. Molecular mechanisms of MHC class I abnormalities andAPM components in human tumors. Cancer Immunol. Immunother. 2008, 57:1719-1726.
129. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., Schreiber R.D. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001, 410:1107-1111.
130. Simpson T.R., Li F., Montalvo-Ortiz W., Sepulveda M.A., Bergerhoff K., Arce F., Roddie C., Henry J.Y., Yagita H., Wolchok J.D., et al. Fc-dependent depletion of tumor-infiltrating regulatory Tcells co-defines theefficacy of anti-CTLA-4 therapy against melanoma. J.Exp. Med. 2013, 210:1695-1710.
131. Smith K.A. The interleukin 2 receptor. Annu. Rev. Cell Biol. 1989, 5:397-425.
132. Snyder A., Makarov V., Merghoub T., Yuan J., Zaretsky J.M., Desrichard A., Walsh L.A., Postow M.A., Wong P., Ho T.S., et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N.Engl. J. Med. 2014, 371:2189-2199.
133. Steinman R.M., Cohn Z.A. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J.Exp. Med. 1973, 137:1142-1162.
134. Stephan M.T., Ponomarev V., Brentjens R.J., Chang A.H., Dobrenkov K.V., Heller G., Sadelain M. T cell-encoded CD80 and 4-1BBL induce auto- and transcostimulation, resulting in potent tumor rejection. Nat. Med. 2007, 13:1440-1449.
135. Stone J.D., Kranz D.M. Role of Tcell receptor affinity in the efficacy and specificity of adoptive Tcell therapies. Front. Immunol. 2013, 4:244.
136. Sugiyama D., Nishikawa H., Maeda Y., Nishioka M., Tanemura A., Katayama I., Ezoe S., Kanakura Y., Sato E., Fukumori Y., et al. Anti-CCR4 mAb selectively depletes effector-type FoxP3+CD4+ regulatory Tcells, evoking antitumor immune responses in humans. Proc. Natl. Acad. Sci. USA 2013, 110:17945-17950.
137. Themeli M., Kloss C.C., Ciriello G., Fedorov V.D., Perna F., Gonen M., Sadelain M. Generation of tumor-targeted human T lymphocytes frominduced pluripotent stem cells for cancer therapy. Nat. Biotechnol. 2013, 31:928-933.
138. Themeli M., Riviere I., Sadelain M. New cell sources for Tcell engineering and adoptive immunotherapy. Cell Stem Cell 2015, Published online April 2, 2015. 10.1016/j.stem.2015.03.011.
139. Townsend A.R.M., Rothbard J., Gotch F.M., Bahadur G., Wraith D., McMichael A.J. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 1986, 44:959-968.
140. Vizcardo R., Masuda K., Yamada D., Ikawa T., Shimizu K., Fujii S., Koseki H., Kawamoto H. Regeneration of human tumor antigen-specific Tcells from iPSCs derived from mature CD8(+) Tcells. Cell Stem Cell 2013, 12:31-36.
141. Warner N.L., Szenberg A., Burnet F.M. The immunological role of different lymphoid organs in the chicken. I. Dissociation of immunological responsiveness. Aust. J. Exp. Biol. Med. Sci. 1962, 40:373-387.
142. Watanabe N., Nakajima H. Coinhibitory molecules in autoimmune diseases. Clin. Dev. Immunol. 2012, 2012:269756.
143. Wilkie S., van Schalkwyk M.C., Hobbs S., Davies D.M., van der Stegen S.J., Pereira A.C., Burbridge S.E., Box C., Eccles S.A., Maher J. 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.
144. Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T., Miyara M., Fehervari Z., Nomura T., Sakaguchi S. CTLA-4 control over Foxp3+ regulatory Tcell function. Science 2008, 322:271-275.
145. Yoshikai Y., Anatoniou D., Clark S.P., Yanagi Y., Sangster R., Van den Elsen P., Terhorst C., Mak T.W. Sequence and expression of transcripts of the human T-cell receptor β-chain genes. Nature 1984, 312:521-524.
146. Zhao Y., Parkhurst M.R., Zheng Z., Cohen C.J., Riley J.P., Gattinoni L., Restifo N.P., Rosenberg S.A., Morgan R.A. Extrathymic generation of tumor-specific Tcells from genetically engineered human hematopoietic stem cells via Notch signaling. Cancer Res. 2007, 67:2425-2429.
147. Zinkernagel R.M., Doherty P.C. Immunological surveillance against altered self components by sensitised T lymphocytes in lymphocytic choriomeningitis. Nature 1974, 251:547-548.