Cord blood T cells mediate enhanced antitumor effects compared with adult peripheral blood T cells

Blood

Volumn 126, Issue 26, 2015, Pages 2882-2891

  Hiwarkar, Prashant ^a,b   Qasim, Waseem ^a,c   Ricciardelli, Ida ^a   Gilmour, Kimberly ^c   Quezada, Sergio ^d   Saudemont, Aurore ^e,f   Amrolia, Persis ^a,c   Veys, Paul ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b BIRMINGHAM CHILDREN S HOSPITAL   (United Kingdom)

^c GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e ANTHONY NOLAN RESEARCH INSTITUTE   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIBODY; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; INTERLEUKIN 4; PERFORIN; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; B CELL LYMPHOMA; B-CELL LYMPHOMA CELL LINE; BLOOD; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER INFILTRATION; CANCER REGRESSION; CANCER SIZE; CANCER SURVIVAL; CD25+ T LYMPHOCYTE; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; EFFECTOR CELL; EPSTEIN BARR VIRUS; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VIVO STUDY; LETHARGY; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTIC INFILTRATION; MEMORY CELL; METASTASIS; MICROENVIRONMENT; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 TH2 BALANCE; TUMOR MICROENVIRONMENT; TUMOR REJECTION; UMBILICAL CORD BLOOD; WEIGHT REDUCTION; ANIMAL; CORD BLOOD STEM CELL TRANSPLANTATION; DISEASE MODEL; DRUG SCREENING; FETUS BLOOD; GRAFT VERSUS TUMOR EFFECT; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LYMPHOMA, B-CELL; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE; T LYMPHOCYTE SUBPOPULATION; TRANSPLANTATION; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; CORD BLOOD STEM CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; FETAL BLOOD; GRAFT VS TUMOR EFFECT; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; LYMPHOMA, B-CELL; MICE; MICE, INBRED NOD; MICE, SCID; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84954513645     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-06-654780     Document Type: Article

References (55)

1. Rubinstein P, Carrier C, Scaradavou A, et al. Outcomes among 562 recipients of placentalblood transplants from unrelated donors. N Engl J Med. 1998;339(22):1565-1577.
2. Rocha V, Cornish J, Sievers EL, et al. Comparison of outcomes of unrelated bone marrow and umbilical cord blood transplants in children with acute leukemia. Blood. 2001;97(10): 2962-2971.
3. Marchant A, Goldman M. T cell-mediated immune responses in human newborns: ready to learn? Clin Exp Immunol. 2005;141(1):10-18[Review].
4. White GP, Watt PM, Holt BJ, Holt PG. Differential patterns of methylation of the IFN-gamma promoter at CpG and non-CpG sites underlie differences in IFN-gamma gene expression between human neonatal and adult CD45ROT cells. J Immunol. 2002;168(6):2820-2827.
5. Silverstein AM. Ontogeny of the immune response. Science. 1964;144(3625):1423-1428.
6. Silverstein AM, Prendergast RA, Kraner KL. Fetal response to antigenic stimulus. IV. Rejection of skin homografts by the fetal lamb. J Exp Med. 1964;119:955-964.
7. Gluckman E, Rocha V, Boyer-Chammard A, et al; Eurocord Transplant Group and the European Blood and Marrow Transplantation Group. Outcome of cord-blood transplantation from related and unrelated donors. N Engl J Med. 1997;337(6):373-381.
8. Brunstein CG, Weisdorf DJ, DeFor T, et al. Marked increased risk of Epstein-Barr virusrelated complications with the addition of antithymocyte globulin to a nonmyeloablative conditioning prior to unrelated umbilical cord blood transplantation. Blood. 2006;108(8):2874-2880.
9. Lindemans CA, Chiesa R, Amrolia PJ, et al. Impact of thymoglobulin prior to pediatric unrelated umbilical cord blood transplantation on immune reconstitution and clinical outcome. Blood. 2014;123(1):126-132.
10. Admiraal R, van Kesteren C, Jol-van der Zijde CM, et al. Association between anti-thymocyte globulin exposure and CD41 immune reconstitution in paediatric haemopoietic cell transplantation: a multicentre, retrospective pharmacodynamic cohort analysis. Lancet Haematol. 2015;2(5):e194-e203.
11. Chiesa R, Gilmour K, Qasim W, et al. Omission of in vivo T-cell depletion promotes rapid expansion of naïve CD41 cord blood lymphocytes and restores adaptive immunity within 2 months after unrelated cord blood transplant. Br J Haematol. 2012;156(5):656-666.
12. Eapen M, Rubinstein P, Zhang MJ, et al. Outcomes of transplantation of unrelated donor umbilical cord blood and bone marrow in children with acute leukaemia: a comparison study. Lancet. 2007;369(9577):1947-1954.
13. Zheng C, Luan Z, Fang J, et al. Comparison of conditioning regimens with or without antithymocyte globulin for unrelated cord blood transplantation in children with high-risk or advanced hematological malignancies. Biol Blood Marrow Transplant. 2015;21(4):707-712.
14. Wagner JE Jr, Eapen M, Carter S, et al; Blood and Marrow Transplant Clinical Trials Network. One-unit versus two-unit cord-blood transplantation for hematologic cancers. N Engl J Med. 2014;371(18):1685-1694.
15. Brunstein CG, Fuchs EJ, Carter SL, et al; Blood and Marrow Transplant Clinical Trials Network. Alternative donor transplantation after reduced intensity conditioning: results of parallel phase 2 trials using partially HLA-mismatched related bone marrow or unrelated double umbilical cord blood grafts. Blood. 2011;118(2):282-288.
16. Barker JN, Fei M, Karanes C, et al; RCI BMT 05-DCB Protocol Team. Results of a prospective multicentre myeloablative double-unit cord blood transplantation trial in adult patients with acute leukaemia and myelodysplasia. Br J Haematol. 2015;168(3):405-412.
17. Comoli P, Labirio M, Basso S, et al. Infusion of autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for prevention of EBV-related lymphoproliferative disorder in solid organ transplant recipients with evidence of active virus replication. Blood. 2002;99(7):2592-2598.
18. Savoldo B, Rooney CM, Di Stasi A, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood. 2007;110(7):2620-2630.
19. Law JP, Hirschkorn DF, Owen RE, Biswas HH, Norris PJ, Lanteri MC. The importance of Foxp3 antibody and fixation/permeabilization buffer combinations in identifying CD41CD251Foxp31 regulatory T cells. Cytometry A. 2009;75(12): 1040-1050.
20. Loughlin PM, Cooke TG, George WD, Gray AJ, Stott DI, Going JJ. Quantifying tumourinfiltrating lymphocyte subsets: a practical immuno-histochemical method. J Immunol Methods. 2007;321(1-2):32-40.
21. King MA, Covassin L, Brehm MA, et al. Human peripheral blood leucocyte non-obese diabeticsevere combined immunodeficiency interleukin-2 receptor gamma chain gene mouse model of xenogeneic graft-versus-host-like disease and the role of host major histocompatibility complex. Clin Exp Immunol. 2009;157(1):104-118.
22. Ali N, Flutter B, Sanchez Rodriguez R, et al. Xenogeneic graft-versus-host-disease in NODscid IL-2Rgnull mice display a T-effector memory phenotype. PLoS One. 2012;7(8):e44219.
23. Covassin L, Laning J, Abdi R, et al. Human peripheral blood CD4 T cell-engrafted non-obese diabetic-scid IL2rg(null) H2-Ab1 (tm1Gru) Tg (human leucocyte antigen D-related 4) mice: a mouse model of human allogeneic graft-versushost disease. Clin Exp Immunol. 2011;166(2): 269-280.
24. Maruo S, Wu Y, Ishikawa S, Kanda T, Iwakiri D, Takada K. Epstein-Barr virus nuclear protein EBNA3C is required for cell cycle progression and growth maintenance of lymphoblastoid cells. Proc Natl Acad Sci USA. 2006;103(51):19500-19505.
25. Maruo S, Johannsen E, Illanes D, Cooper A, Kieff E. Epstein-Barr Virus nuclear protein EBNA3A is critical for maintaining lymphoblastoid cell line growth. J Virol. 2003;77(19):10437-10447.
26. De Waele M, Foulon W, Renmans W, et al. Hematologic values and lymphocyte subsets in fetal blood. Am J Clin Pathol. 1988;89(6):742-746.
27. Zhao Y, Dai ZP, Lv P, Gao XM. Phenotypic and functional analysis of human T lymphocytes in early second- and third-trimester fetuses. Clin Exp Immunol. 2002;129(2):302-308.
28. Förster R, Schubel A, Breitfeld D, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 1999;99(1): 23-33.
29. Leung W, Ramírez M, Mukherjee G, et al. Comparisons of alloreactive potential of clinical hematopoietic grafts. Transplantation. 1999; 68(5):628-635.
30. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003; 348(3):203-213.
31. Sato E, Olson SH, Ahn J, et al. Intraepithelial CD81 tumor-infiltrating lymphocytes and a high CD81/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA. 2005;102(51):18538-18543.
32. Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313(5795):1960-1964.
33. Leffers N, Gooden MJ, de Jong RA, et al. Prognostic significance of tumor-infiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother. 2009;58(3):449-459.
34. Fearon ER, Pardoll DM, Itaya T, et al. Interleukin-2 production by tumor cells bypasses T helper function in the generation of an antitumor response. Cell. 1990;60(3):397-403.
35. Dranoff G, Jaffee E, Lazenby A, et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colonystimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci USA. 1993;90(8):3539-3543.
36. Han S, Zhang C, Li Q, et al. Tumour-infiltrating CD4(1) and CD8(1) lymphocytes as predictors of clinical outcome in glioma. Br J Cancer. 2014; 110(10):2560-2568.
37. Liang Y, Huang T, Zhang C, et al. Donor CD81 T cells facilitate induction of chimerism and tolerance without GVHD in autoimmune NOD mice conditioned with anti-CD3 mAb. Blood. 2005;105(5):2180-2188.
38. Zhang C, Lou J, Li N, et al. Donor CD81 T cells mediate graft-versus-leukemia activity without clinical signs of graft-versus-host disease in recipients conditioned with anti-CD3 monoclonal antibody. J Immunol. 2007;178(2):838-850.
39. Johnson BD, Becker EE, Truitt RL. Graft-vs.-host and graft-vs.-leukemia reactions after delayed infusions of donor T-subsets. Biol Blood Marrow Transplant. 1999;5(3):123-132.
40. Lu YF, Gavrilescu LC, Betancur M, Lazarides K, Klingemann H, Van Etten RA. Distinct graftversus-leukemic stem cell effects of early or delayed donor leukocyte infusions in a mouse chronic myeloid leukemia model. Blood. 2012; 119(1):273-284.
41. Tsung K, Meko JB, Peplinski GR, Tsung YL, Norton JA. IL-12 induces T helper 1-directed antitumor response. J Immunol. 1997;158(7): 3359-3365.
42. Aruga A, Aruga E, Tanigawa K, Bishop DK, Sondak VK, Chang AE. Type 1 versus type 2 cytokine release by Vbeta T cell subpopulations determines in vivo antitumor reactivity: IL-10 mediates a suppressive role. J Immunol. 1997; 159(2):664-673.
43. Fowler DH, Breglio J, Nagel G, Hirose C, Gress RE. Allospecific CD41, Th1/Th2 and CD81, Tc1/Tc2 populations in murine GVL: type I cells generate GVL and type II cells abrogate GVL. Biol Blood Marrow Transplant. 1996;2(3):118-125.
44. Blazar BR, Taylor PA, Panoskaltsis-Mortari A, Vallera DA. Rapamycin inhibits the generation of graft-versus-host disease- and graft-versusleukemia-causing T cells by interfering with the production of Th1 or Th1 cytotoxic cytokines. J Immunol. 1998;160(11):5355-5365.
45. Hu HM, Urba WJ, Fox BA. Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from a type 2 to a type 1 cytokine profile. J Immunol. 1998;161(6): 3033-3041.
46. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137-148.
47. Shevach EM. CD41 CD251 suppressor T cells: more questions than answers. Nat Rev Immunol. 2002;2(6):389-400.
48. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer. 2005;5(4):263-274.
49. Sakaguchi S. Naturally arising Foxp3-expressing CD251CD41 regulatory T cells in immunological tolerance to self and non-self. Nat Immunol. 2005; 6(4):345-352.
50. Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW. The prognostic influence of tumourinfiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer. 2011; 105(1):93-103.
51. Maury S, Lemoine FM, Hicheri Y, et al. CD41 CD251 regulatory T cell depletion improves the graft-versus-tumor effect of donor lymphocytes after allogeneic hematopoietic stem cell transplantation. Sci Transl Med. 2010;2(41): 41ra52.
52. Mold JE, Venkatasubrahmanyam S, Burt TD, et al. Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science. 2010;330(6011):1695-1699.
53. Copley MR, Babovic S, Benz C, et al. The Lin28blet-7-Hmga2 axis determines the higher selfrenewal potential of fetal haematopoietic stem cells. Nat Cell Biol. 2013;15(8):916-925.
54. Gardiner CM, Meara AO, Reen DJ. Differential cytotoxicity of cord blood and bone marrowderived natural killer cells. Blood. 1998;91(1): 207-213.
55. Xing D, Ramsay AG, Gribben JG, et al. Cord blood natural killer cells exhibit impaired lytic immunological synapse formation that is reversed with IL-2 exvivo expansion. J Immunother. 2010; 33(7):684-696.