Role of memory T cell subsets for adoptive immunotherapy

Seminars in Immunology

Volumn 28, Issue 1, 2016, Pages 28-34

  Busch, Dirk H ^a,d   Fräßle, Simon P ^a   Sommermeyer, Daniel ^b,c   Buchholz, Veit R ^a   Riddell, Stanley R ^a,b,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b USA   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d DZIF National Centre for Infection Research   (Germany)

Author keywords

Adoptive T cell therapy; Clinical cell processing and purification; Memory stem cells; T cell engineering; T cell subsets

Indexed keywords

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; DNA MODIFICATION; GENETIC ENGINEERING; HUMAN; MEMORY T LYMPHOCYTE; ONTOGENY; REVIEW; T LYMPHOCYTE SUBPOPULATION; ADULT STEM CELL; ANIMAL; CELL DIFFERENTIATION; CELL SEPARATION; CELL SURVIVAL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFECTION; NEOPLASM; PHYSIOLOGY; PROCEDURES; T LYMPHOCYTE; TRANSPLANTATION;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CELL SURVIVAL; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOTHERAPY, ADOPTIVE; INFECTION; NEOPLASMS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 84960172060     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2016.02.001     Document Type: Review

References (76)

1. Maus M.V., Fraietta J.A., Levine B.L., Kalos M., Zhao Y., June C.H. Adoptive immunotherapy for cancer or viruses. Annu. Rev. Immunol. 2014, 32:189-225.
2. Jenkins M.K., Chu H.H., McLachlan J.B., Moon J.J. On the composition of the preimmune repertoire of T cells specific for Peptide-major histocompatibility complex ligands. Annu. Rev. Immunol. 2010, 28:275-294.
3. Williams M.A., Bevan M.J. Effector and memory CTL differentiation. Annu. Rev. Immunol. 2007, 25:171-192.
4. De Rosa S.C., Herzenberg L.A., Herzenberg L.A., Roederer M. 11-color, 13-parameter flow cytometry: identification of human naive T cells by phenotype, function, and T-cell receptor diversity. Nat. Med. 2001, 7:245-248.
5. Newell E.W., Sigal N., Bendall S.C., Nolan G.P., Davis M.M. Cytometry by time-of-flight shows combinatorial cytokine expression and virus-specific cell niches within a continuum of CD8+ T cell phenotypes. Immunity 2012, 36:142-152.
6. Arsenio J., Kakaradov B., Metz P.J., Kim S.H., Yeo G.W., Chang J.T. Early specification of CD8(+) T lymphocyte fates during adaptive immunity revealed by single-cell gene-expression analyses. Nat. Immunol. 2014, 15:365-372.
7. Seder R.A., Darrah P.A., Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 2008, 8:247-258.
8. Appay V., Douek D.C., Price D.A. CD8+ T cell efficacy in vaccination and disease. Nat. Med. 2008, 14:623-628.
9. Jensen M.C., Riddell S.R. Design and implementation of adoptive therapy with chimeric antigen receptor-modified T cells. Immunol. Rev. 2014, 257:127-144.
10. Sallusto F., Lenig D., Förster R., Lipp M., Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999, 401:708-712.
11. Masopust D., Vezys V., Marzo A.L., Lefrançois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001, 291:2413-2417.
12. Gebhardt T., Wakim L.M., Eidsmo L., Reading P.C., Heath W.R., Carbone F.R. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 2009, 10:524-530.
13. Gebhardt T., Whitney P.G., Zaid A., Mackay L.K., Brooks A.G., Heath W.R., et al. Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 2011, 477:216-219.
14. Farber D.L., Yudanin N.A., Restifo N.P. Human memory T cells: generation, compartmentalization and homeostasis. Nat. Rev. Immunol. 2014, 14:24-35.
15. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136:2348-2357.
16. Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations (*). Annu. Rev. Immunol. 2010, 28:445-489.
17. Gasteiger G., Rudensky A.Y. Interactions between innate and adaptive lymphocytes. Nat. Publ. Gr. 2014, 14:631-639.
18. O'Shea J.J., Paul W.E. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 2010, 327:1098-1102.
19. Kaech S.M., Cui W. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Publ. Gr. 2012, 12:749-761.
20. Böttcher J.P., Beyer M., Meissner F., Abdullah Z., Sander J., Höchst B., et al. Functional classification of memory CD8(+) T cells by CX3CR1 expression. Nat. Commun. 2015, 6:8306.
21. Darrah P.A., Patel D.T., De Luca P.M., Lindsay R.W.B., Davey D.F., Flynn B.J., et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 2007, 13:843-850.
22. Appay V., Dunbar P.R., Callan M., Klenerman P., Gillespie G.M.A., Papagno L., et al. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 2002, 8:379-385.
23. Ahmed R., Bevan M.J., Reiner S.L., Fearon D.T. The precursors of memory: models and controversies. Nat. Rev. Immunol. 2009, 9:662-668.
24. Wherry E.J., Teichgräber V., Becker T.C., Masopust D., Kaech S.M., Antia R., et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 2003, 4:225-234.
25. Ahmed R., Gray D. Immunological memory and protective immunity: understanding their relation. Science 1996, 272:54-60.
26. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., et al. Inflammation directs memory precursor and short-lived effector CD8+ T cell fates via the graded expression of T-bet transcription factor. Immunity 2007, 27:281-295.
27. Joshi N.S., Kaech S.M. Effector CD8 T cell development: a balancing act between memory cell potential and terminal differentiation. J. Immunol. 2008, 180:1309-1315.
28. Gett A.V., Sallusto F., Lanzavecchia A., Geginat J. T cell fitness determined by signal strength. Nat. Immunol. 2003, 4:355-360.
29. Lanzavecchia A., Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2002, 2:982-987.
30. Gattinoni L., Klebanoff C.A., Restifo N.P. Paths to stemness: building the ultimate antitumour T cell. Nat. Rev. Cancer 2012, 12:671-684.
31. Simons B.D., Clevers H. Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 2011, 145:851-862.
32. Weissman I.L. Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000, 100:157-168.
33. Fearon D.T., Manders P., Wagner S.D. Arrested differentiation, the self-renewing memory lymphocyte, and vaccination. Science 2001, 293:248-250.
34. Gattinoni L., Lugli E., Ji Y., Pos Z., Paulos C.M., Quigley M.F., et al. A human memory T cell subset with stem cell-like properties. Nat. Med. 2011, 17:1290-1297.
35. Schmueck-Henneresse M., Sharaf R., Vogt K., Weist B.J.D., Landwehr-Kenzel S., Fuehrer H., et al. Peripheral blood-derived virus-specific memory stem T cells mature to functional effector memory subsets with self-renewal potency. J. Immunol. 2015, 194:5559-5567.
36. Zhang Y., Joe G., Hexner E., Zhu J., Emerson S.G. Host-reactive CD8+ memory stem cells in graft-versus-host disease. Nat. Med. 2005, 11:1299-1305.
37. Gattinoni L., Zhong X.-S., Palmer D.C., Ji Y., Hinrichs C.S., Yu Z., et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 2009, 15:808-813.
38. Fuertes Marraco S.A., Soneson C., Cagnon L., Gannon P.O., Allard M., Abed Maillard S., et al. Long-lasting stem cell-like memory CD8+ T cells with a naïve-like profile upon yellow fever vaccination. Sci. Transl. Med. 2015, 7:282ra48.
39. Oliveira G., Ruggiero E., Stanghellini M.T.L., Cieri N., D'Agostino M., Fronza R., et al. Tracking genetically engineered lymphocytes long-term reveals the dynamics of T cell immunological memory. Sci. Transl. Med. 2015, 7. 317ra198.
40. Buchholz V.R., Schumacher T.N.M., Busch D.H. T cell fate at the single-cell level. Annu. Rev. Immunol. 2015, Dec 11. [Epub ahead of print].
41. Gerlach C., van Heijst J.W.J., Swart E., Sie D., Armstrong N., Kerkhoven R.M., et al. One naive T cell, multiple fates in CD8+ T cell differentiation. J. Exp. Med. 2010, 207:1235-1246.
42. Gerlach C., Rohr J.C., Perié L., van Rooij N., van Heijst J.W.J., Velds A., et al. Heterogeneous differentiation patterns of individual CD8+ T cells. Science 2013, 340:635-639.
43. Stemberger C., Huster K.M., Koffler M., Anderl F., Schiemann M., Wagner H., et al. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 2007, 27:985-997.
44. Buchholz V.R., Flossdorf M., Hensel I., Kretschmer L., Weissbrich B., Gräf P., et al. Disparate individual fates compose robust CD8+ T cell immunity. Science 2013, 340:630-635.
45. Graef P., Buchholz V.R., Stemberger C., Flossdorf M., Henkel L., Schiemann M., et al. Serial transfer of single-cell-derived immunocompetence reveals stemness of CD8(+) central memory T cells. Immunity 2014, 41:116-126.
46. Flossdorf M., Rössler J., Buchholz V.R., Busch D.H., Höfer T. CD8(+) T cell diversification by asymmetric cell division. Nat. Immunol. 2015, 16:891-893.
47. Stemberger C., Graef P., Odendahl M., Albrecht J., Dössinger G., Anderl F., et al. Lowest numbers of primary CD8+ T cells can reconstitute protective immunity upon adoptive immunotherapy. Blood 2014, 124:628-637.
48. Klebanoff C.A., Scott C.D., Leonardi A.J., Yamamoto T.N., Cruz A.C., Ouyang C., et al. Memory T cell-driven differentiation of naive cells impairs adoptive immunotherapy. J. Clin. Invest. 2016, 126:318-334.
49. Ibrahim S.F., van den Engh G. Flow cytometry and cell sorting. Adv. Biochem. Eng. Biotechnol. 2007, 106:19-39.
50. Knabel M., Franz T.J., Schiemann M., Wulf A., Villmow B., Schmidt B., et al. Reversible MHC multimer staining for functional isolation of T-cell populations and effective adoptive transfer. Nat. Med. 2002, 8:631-637.
51. Stemberger C., Dreher S., Tschulik C., Piossek C., Bet J., Yamamoto T.N., Novel serial positive enrichment technology enables clinical multiparameter cell sorting., et al. PLOS ONE 2012, 7:e35798.
52. Inci F., Filippini C., Baday M., Ozen M.O., Calamak S., Durmus N.G., et al. Multitarget, quantitative nanoplasmonic electrical field-enhanced resonating device (NE2RD) for diagnostics. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E4354-E4363.
53. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002, 298:850-854.
54. Rosenberg S.A., Yang J.C., Sherry R.M., Kammula U.S., Hughes M.S., Phan G.Q., et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 2011, 17:4550-4557.
55. Yee C., Thompson J.A., Byrd D., Riddell S.R., Roche P., Celis E., et al. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1616-1673.
56. Dudley M.E., Yang J.C., Sherry R., Hughes M.S., Royal R., Kammula U., et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 2008, 26:5233-5239.
57. Gattinoni L., Finkelstein S.E., Klebanoff C.A., Antony P.A., Palmer D.C., Spiess P.J., et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J. Exp. Med. 2005, 202:907-912.
58. + tumor-reactive repertoire infiltrating human tumors. J. Clin. Invest. 2014, 124:2246-2259.
59. Powell D.J., Dudley M.E., Robbins P.F., Rosenberg S.A. Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 2005, 105:241-250.
60. Li Y., Bleakley M., Yee C. IL-21 influences the frequency, phenotype, and affinity of the antigen-specific CD8 T cell response. J. Immunol. 2005, 175:2261-2269.
61. Chapuis A.G., Ragnarsson G.B., Nguyen H.N., Chaney C.N., Pufnock J.S., Schmitt T.M., et al. Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci. Transl. Med. 2013, 5:174ra27.
62. Hinrichs C.S., Spolski R., Paulos C.M., Gattinoni L., Kerstann K.W., Palmer D.C., et al. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 2008, 111:5326-5333.
63. Cieri N., Camisa B., Cocchiarella F., Forcato M., Oliveira G., Provasi E., et al. IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood 2013, 121:573-584.
64. Klebanoff C.A., Gattinoni L., Torabi-Parizi P., Kerstann K., Cardones A.R., Finkelstein S.E., et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9571-9576.
65. Walter E.A., Greenberg P.D., Gilbert M.J., Finch R.J., Watanabe K.S., Thomas E.D., et al. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 1995, 333:1038-1044.
66. Heslop H.E., Ng C.Y., Li C., Smith C.A., Loftin S.K., Krance R.A., et al. 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.
67. Berger C., Jensen M.C., Lansdorp P.M., Gough M., Elliott C., Riddell S.R. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 2008, 118:294-305.
68. Berger C., Berger M., Anderson D., Riddell S.R. A non-human primate model for analysis of safety, persistence, and function of adoptively transferred T cells. J. Med. Primatol. 2011, 40:88-103.
69. Kalos M., June C.H. Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 2013, 39:49-60.
70. Brentjens R.J., Davila M.L., Riviere I., Park J., Wang X., Cowell L.G., et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013, 5:177ra38.
71. June C.H., Riddell S.R., Schumacher T.N. Adoptive cellular therapy: a race to the finish line. Sci. Transl. Med. 2015, 7:280ps7.
72. Kalos M., Levine B.L., Porter D.L., Katz S., Grupp S.A., Bagg A., et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 2011, 3:95ra73.
73. Kochenderfer J.N., Dudley M.E., Carpenter R.O., Kassim S.H., Rose J.J., Telford W.G., et al. Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood 2013, 122:4129-4139.
74. Maude S.L., Frey N., Shaw P.A., Aplenc R., Barrett D.M., Bunin N.J., et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 2014, 371:1507-1517.
75. Sommermeyer D., Hudecek M., Kosasih P.L., Gogishvili T., Maloney D.G., Turtle C.J., et al. Chimeric antigen receptor-modified T cells derived from defined CD8(+) and CD4(+) subsets confer superior antitumor reactivity in vivo. Leukemia 2015.
76. Singh N., Perazzelli J., Grupp S.A., Barrett D.M. Early memory phenotypes drive T cell proliferation in patients with pediatric malignancies. Sci. Transl. Med. 2016, 8:320ra3.