CCR7+ selected gene-modified T cells maintain a central memory phenotype and display enhanced persistence in peripheral blood in vivo

Journal for ImmunoTherapy of Cancer

Volumn 5, Issue 1, 2017, Pages

  Kueberuwa, Gray ^a   Gornall, Hannah ^a   Alcantar Orozco, Erik Marcelo ^a   Bouvier, Deborah ^a   Kapacee, Zainul Abedin ^a   Hawkins, Robert Edward ^a   Gilham, David Edward ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Adoptive cell therapy; CCR7; CD62L; Central memory; Differentiation status; DMF5; Immunotherapy; Transgenic TCR

Indexed keywords

ALLOPHYCOCYANIN; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; INTERLEUKIN 7 RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MITOGENIC AGENT; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; CCR7 PROTEIN, HUMAN;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL SELECTION; CELLULAR IMMUNITY; CENTRAL MEMORY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; EFFECTOR MEMORY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MEMORY; MEMORY T LYMPHOCYTE; MITOGENESIS; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; ADOPTIVE IMMUNOTHERAPY; ANIMAL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; K-562 CELL LINE; PHENOTYPE; T LYMPHOCYTE; TRANSPLANTATION;

ANIMALS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOTHERAPY, ADOPTIVE; K562 CELLS; MICE; PHENOTYPE; RECEPTORS, CCR7; T-LYMPHOCYTES;

EID: 85013333304     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-017-0216-7     Document Type: Article

References (49)

1. Kershaw MH, Westwood JA, Darcy PK. Gene-engineered T cells for cancer therapy. Nat Rev Cancer. 2013;13:525-41.
2. Berger C, Jensen MC, Lansdorp PM, Gough M, Elliott C, Riddell SR. 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.
3. Hinrichs CS, Borman ZA, Cassard L, Gattinoni L, Spolski R, Yu Z, Sanchez-Perez L, Muranski P, Kern SJ, Logun C, et al. Adoptively transferred effector cells derived from naïve rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci. 2009;106:17469-74.
4. Tanel A, Fonseca SG, Yassine-Diab B, et al. Cellular and molecular mechanisms of memory T-cell survival. Expert Rev Vaccines. 2009;8(3):299-312.
5. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu ZY, Finkelstein SE, Theoret MR, Rosenberg SA, Restifo NP. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8(+) T cells. J Clin Investig. 2005;115:1616-26.
6. Klebanoff CA, Gattinoni L, Restifo NP. Sorting through subsets: which T cell populations mediate highly effective adoptive immunotherapy? J Immunother. 2012;35:651-60.
7. Lugli E, Dominguez MH, Gattinoni L, Chattopadhyay PK, Bolton DL, Song K, Klatt NR, Brenchley JM, Vaccari M, Gostick E, et al. Superior T memory stem cell persistence supports long-lived T cell memory. J Clin Invest. 2013;123:594-9.
8. Klebanoff CA, Gattinoni L, Palmer DC, Muranski P, Ji Y, Hinrichs CS, Borman ZA, Kerkar SP, Scott CD, Finkelstein SE, et al. Determinants of successful CD8(+) T cell adoptive immunotherapy for large established tumors in mice. Clin Cancer Res. 2011;17:5343-52.
9. Chapuis AG, Thompson JA, Margolin KA, Rodmyre R, Lai IP, Dowdy K, Farrar EA, Bhatia S, Sabath DE, Cao J, et al. Transferred melanoma-specific CD8+ T cells persist, mediate tumor regression, and acquire central memory phenotype. Proc Natl Acad Sci. 2012;109:4592-7.
10. Powell DJ, Dudley ME, Robbins PF, Rosenberg SA. 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(1):241-50.
11. Huang J, Khong HT, Dudley ME, El-Gamil M, Li YF, Rosenberg SA, Robbins PF. Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother. 2005;28:258-67.
12. Huang J, Kerstann KW, Ahmadzadeh M, Li YF, El-Gamil M, Rosenberg SA, Robbins PF. Modulation by IL-2 of CD70 and CD27 expression on CD8+ T cells: importance for the therapeutic effectiveness of cell transfer immunotherapy. J Immunol. 2006;176:7726-35.
13. Guest RD, Kirillova N, Mowbray S, Gornall H, Rothwell DG, Cheadle EJ, Austin E, Smith K, Watt SM, Kuhlcke K, et al. Definition and application of good manufacturing process-compliant production of CEA-specific chimeric antigen receptor expressing T cells for phase I/II clinical trial. Cancer Immunol Immunother. 2014;63:133-45.
14. Kershaw MH, Westwood JA, Parker LL, Wang G, Eshhar Z, Mavroukakis SA, White DE, Wunderlich JR, Canevari S, Rogers-Freezer L, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res. 2006;12:6106-15.
15. Kochenderfer JN, Rosenberg SA. Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat Rev Clin Oncol. 2013;10:267-76.
16. Lamers CHJ, Sleijfer S, Vulto AG, Kruit WHJ, Kliffen M, Debets R, Gratama JW, Stoter G, Oosterwijk E. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol. 2006;24:e20-2.
17. Warren RS, Fisher GA, Bergsland EK, Pennathur-Das R, Nemunaitis J, Venook AP, Hege KM. Clinical studies of regional and systemic gene therapy with autologous CC49-zeta modified T cells in colorectal cancer metastatic to the liver. Cancer Gene Ther. 1998;5:S1-2.
18. Yvon E, Del Vecchio M, Savoldo B, Hoyos V, Dutour A, Anichini A, Dotti G, Brenner MK. Immunotherapy of metastatic melanoma using genetically engineered GD2-specific T cells. Clin Cancer Res. 2009;15:5852-60.
19. Johnson LA, Morgan RA, Dudley ME, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood. 2009;114(3):535-46.
20. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan D-AN, Feldman SA, Davis JL, Morgan RA, Merino MJ, Sherry RM, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther. 2011;19:620-6.
21. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, 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;29:917-24.
22. Scholler J, Brady TL, Binder-Scholl G, Hwang W-T, Plesa G, Hege KM, Vogel AN, Kalos M, Riley JL, Deeks SG, et al. Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci Transl Med. 2012;4:132ra153.
23. Stacchini A, Aragno M, Vallario A, Alfarano A, Circosta P, Gottardi D, Faldella A, Rege-Cambrin G, Thunberg U, Nilsson K, Caligaris-Cappio F. MEC1 and MEC2: two new cell lines derived from B-chronic lymphocytic leukaemia in prolymphocytoid transformation. Leuk Res. 1999;23:127-36.
24. Mato A, Porter DL. A drive through cellular therapy for CLL in 2015: allogeneic cell transplantation and CARs. Blood. 2015;126:478-85.
25. Verhoeyen E, Costa C, Cosset F-L. Lentiviral vector gene transfer into human T cells. In: Baum C, editor. Genetic modification of hematopoietic stem cells: methods and protocols. Totowa: Humana Press; 2009. p. 97-114.
26. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401:708-12.
27. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E. The who's who of T cell differentiation: human memory T cell subsets. Eur J Immunol. 2013;43:2797-809.
28. Farber DL. Biochemical signaling pathways for memory T cell recall. Semin Immunol. 2009;21:84-91.
29. Wrzesinski SH, Wan YY, Flavell RA. Transforming growth factor-β and the immune response: implications for anticancer therapy. Clin Cancer Res. 2007;13:5262-70.
30. Kalaitsidou M, Kueberuwa G, Schuett A, Gilham DE. CAR T cell therapy: toxicity and the relevance of preclinical models. Immunotherapy. 2015;7:487-97.
31. Kueberuwa G, Cawood R, Tedcastle A, Seymour LW. Tissue-specific attenuation of oncolytic sindbis virus without compromised genetic stability. Human Gene Therapy Methods. 2014;25:154-65.
32. Kueberuwa G, Gornall H, Bouvier D, Gilham D. Improving CAR T cell therapy to treat CD19 + malignancies. Hum Gene Ther. 2015;26:A24-5.
33. Tosello V, Odunsi K, Souleimanian NE, Lele S, Shrikant P, Old LJ, Valmori D, Ayyoub M. Differential expression of CCR7 defines two distinct subsets of human memory CD4 + CD25+ Tregs. Clin Immunol. 2008;126:291-302.
34. Geginat J, Lanzavecchia A, Sallusto F. Proliferation and differentiation potential of human CD8+ memory T cell subsets in response to antigen or homeostatic cytokines. Blood. 2003;101(11):4260-66.
35. Cheadle EJ, Sheard V, Hombach AA, Chmielewski M, Riet T, Berrevoets C, Schooten E, Lamers C, Abken H, Debets R, Gilham DE. Chimeric antigen receptors for T cell based therapy. Methods Mol Biol. 2012;907:645-66.
36. Verfuerth S, Sousa PSE, Beloki L, Murray M, Peters MD, Mackinnon S, Lowdell MW, Chakraverty R, Samuel ER. Generation of memory T cells for adoptive transfer using clinical-grade anti-CD62L magnetic beads. Bone Marrow Transplant. 2015;50:1358-64.
37. Riddell SR, Sommermeyer D, Berger C, Liu L, Balakrishnan A, Salter A, Hudecek M, Maloney DG, Turtle CJ. Adoptive therapy with chimeric antigen receptor modified T cells of defined subset composition. Cancer J. 2014;20:141-4.
38. Hinrichs CS, Borman ZA, Cassard L, Gattinoni L, Spolski R, Yu Z, Sanchez-Perez L, Muranski P, Kern SJ, Logun C, et al. Adoptively transferred effector cells derived from naive rather than central memory CD8(+) T cells mediate superior antitumor immunity. Proc Natl Acad Sci U S A. 2009;106:17469-74.
39. Obar JJ, Lefrançois L. Early events governing memory CD8+ T cell differentiation. Int Immunol. 2010;22(8):619-25.
40. Roederer M, Nozzi JL, Nason MC. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry Part A. 2011;79A:167-74.
41. Williams MA, Tyznik AJ, Bevan MJ. Interleukin-2 signals during priming are required for secondary expansion of CD8(+) memory T cells. Nature. 2006;441:890-3.
42. Lin L, Couturier J, Yu X, Medina MA, Kozinetz CA, Lewis DE. Granzyme B secretion by human memory CD4 T cells is less strictly regulated compared to memory CD8 T cells. BMC Immunol. 2014;15:16.
43. Ali N, Flutter B, Sanchez Rodriguez R, Sharif-Paghaleh E, Barber LD, Lombardi G, Nestle F. Xenogeneic Graft-versus-Host-Disease in NOD-scid IL-2RγnullMice Display a T-Effector Memory Phenotype. PLoS ONE. 2012;7(8):e44219.
44. Alcantar-Orozco EM, Gornall H, Baldan V, Hawkins RE, Gilham DE. Potential limitations of the NSG humanized mouse as a model system to optimize engineered human T cell therapy for cancer. Human Gene Therapy Methods. 2013;24:310-20.
45. Hannon M, Lechanteur C, Lucas S, Somja J, Seidel L, Belle L, Bruck F, Baudoux E, Giet O, Chantillon A-M, et al. Infusion of clinical-grade enriched regulatory T cells delays experimental xenogeneic graft-versus-host disease. Transfusion. 2014;54:353-63.
46. Zhou Q, Facciponte J, Jin M, Shen Q, Lin Q. Humanized NOD-SCID IL2rg-/- mice as a preclinical model for cancer research and its potential use for individualized cancer therapies. Cancer Lett. 2014;344:13-9.
47. Barrett DM, Singh N, Liu X, Jiang S, June CH, Grupp SA, Zhao Y. Relation of clinical culture method to T cell memory status and efficacy in xenograft models of adoptive immunotherapy. Cytotherapy. 2014;16:619-30.
48. Zappasodi R, Di Nicola M, Carlo-Stella C, Mortarini R, Molla A, Vegetti C, Albani S, Anichini A, Gianni AM. The effect of artificial antigen-presenting cells with preclustered anti-CD28/-CD3/-LFA-1 monoclonal antibodies on the induction of ex vivo expansion of functional human antitumor T cells. Haematologica. 2008;93(10):1523-34.
49. Scheurich P, Thoma B, Ucer U, Pfizenmaier K. Immunoregulatory activity of recombinant human tumor necrosis factor (TNF)-alpha: induction of TNF receptors on human T cells and TNF-alpha-mediated enhancement of T cell responses. J Immunol. 1987;138:1786-90.