Umbilical cord blood T cells respond against the Melan-A/MART-1 tumor antigen and exhibit reduced alloreactivity as compared with adult blood-derived T cells

Journal of Immunology

Volumn 185, Issue 2, 2010, Pages 856-866

  Merindol, Natacha ^a,c   Grenier, Anne Julie ^a,c   Caty, Martine ^a   Charrier, Emily ^a,c   Duval, Arnaud ^a,c   Duval, Michel ^a,b,c   Champagne, Martin A ^b,c,d   Soudeyns, Hugo ^a,c  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d HÉMA QUÉBEC   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE MARKER; GAMMA INTERFERON; HLA A2 ANTIGEN; MELAN A; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MART1 ANTIGEN; TUMOR ANTIGEN; TUMOR PROTEIN;

ALLOIMMUNITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; CYTOTOXICITY; EFFECTOR CELL; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; PHENOTYPE; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; UMBILICAL CORD BLOOD; ADULT; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOLOGY; FETUS BLOOD; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MONONUCLEAR CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION; T LYMPHOCYTE;

ADULT; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; FETAL BLOOD; FLOW CYTOMETRY; HLA-A2 ANTIGEN; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; NEOPLASM PROTEINS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 77955502916     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902613     Document Type: Article

References (56)

1. Kägi, D., B. Ledermann, K. Bürki, R. M. Zinkernagel, and H. Hengartner. 1996. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 14: 207-232.
2. Zhang, C., J. Lou, N. Li, I. Todorov, C. L. Lin, Y. A. Cao, C. H. Contag, F. Kandeel, S. Forman, and D. Zeng. 2007. Donor CD8+ 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. 178: 838-850. (Pubitemid 46095156)
3. Tse, W., K. D. Bunting, and M. J. Laughlin. 2008. New insights into cord blood stem cell transplantation. Curr. Opin. Hematol. 15: 279-284.
4. Szabolcs, P., and D. Niedzwiecki. 2007. Immune reconstitution after unrelated cord blood transplantation. Cytotherapy 9: 111-122. (Pubitemid 46510976)
5. Vandenbosch, K., P. Ovetchkine, M. A. Champagne, E. Haddad, L. Alexandrov, and M. Duval. 2008. Varicella-zoster virus disease is more frequent after cord blood than after bone marrow transplantation. Biol. Blood Marrow Transplant. 14: 867-871.
6. Harris, D. T., M. J. Schumacher, J. Locascio, F. J. Besencon, G. B. Olson, D. DeLuca, L. Shenker, J. Bard, and E. A. Boyse. 1992. Phenotypic and functional immaturity of human umbilical cord blood T lymphocytes. Proc. Natl. Acad. Sci. USA 89: 10006-10010.
7. Chalmers, I. M., G. Janossy, M. Contreras, and C. Navarrete. 1998. Intracellular cytokine profile of cord and adult blood lymphocytes. Blood 92: 11-18.
8. Risdon, G., J. Gaddy, F. B. Stehman, and H. E. Broxmeyer. 1994. Proliferative and cytotoxic responses of human cord blood T lymphocytes following allogeneic stimulation. Cell. Immunol. 154: 14-24.
9. Nitsche, A., M. Zhang, T. Clauss, W. Siegert, K. Brune, and A. Pahl. 2007. Cytokine profiles of cord and adult blood leukocytes: differences in expression are due to differences in expression and activation of transcription factors. BMC Immunol. 8: 18.
10. Gutman, J. A., C. J. Turtle, T. J. Manley, S. Heimfeld, I. D. Bernstein, S. R. Riddell, and C. Delaney. 2010. Single unit dominance following double unit umbilical cord blood transplantation coincides with a specific CD8+ T cell response against the non-engrafted unit. Blood 115: 757-765.
11. Marchant, A., V. Appay, M. Van Der Sande, N. Dulphy, C. Liesnard, M. Kidd, S. Kaye, O. Ojuola, G. M. Gillespie, A. L. Vargas Cuero, et al. 2003. Mature CD8(+) T lymphocyte response to viral infection during fetal life. J. Clin. Invest. 111: 1747-1755.
12. Rastogi, D., C. Wang, X. Mao, C. Lendor, P. B. Rothman, and R. L. Miller. 2007. Antigen-specific immune responses to influenza vaccine in utero. J. Clin. Invest. 117: 1637-1646.
13. Valmori, D., N. Gervois, D. Rimoldi, J. F. Fonteneau, A. Bonelo, D. Liénard, L. Rivoltini, F. Jotereau, J. C. Cerottini, and P. Romero. 1998. Diversity of the fine specificity displayed by HLA-Ap0201-restricted CTL specific for the immunodominant Melan-A/MART-1 antigenic peptide. J. Immunol. 161: 6956-6962. (Pubitemid 28562243)
14. Romero, P., D. Valmori, M. J. Pittet, A. Zippelius, D. Rimoldi, F. Lévy, V. Dutoit, M. Ayyoub, V. Rubio-Godoy, O. Michielin, et al. 2002. Antigenicity and immunogenicity of Melan-A/MART-1 derived peptides as targets for tumor reactive CTL in human melanoma. Immunol. Rev. 188: 81-96.
15. Pittet, M. J., A. Gati, F. A. Le Gal, G. Bioley, P. Guillaume, M. de Smedt, J. Plum, D. E. Speiser, J. C. Cerottini, P. Y. Dietrich, et al. 2006. Ex vivo characterization of allo-MHC-restricted T cells specific for a single MHC-peptide complex. J. Immunol. 176: 2330-2336.
16. Yee, C., P. A. Savage, P. P. Lee, M. M. Davis, and P. D. Greenberg. 1999. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J. Immunol. 162: 2227-2234.
17. Lissina, A., K. Ladell, A. Skowera, M. Clement, E. Edwards, R. Seggewiss, H. A. van den Berg, E. Gostick, K. Gallagher, E. Jones, et al. 2009. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunol. Methods 340: 11-24.
18. Brunner, K. T., J. Mauel, J. C. Cerottini, and B. Chapuis. 1968. Quantitative assay of the lytic action of immune lymphoid cells on 51-Cr-labelled allogeneic target cells in vitro; inhibition by isoantibody and by drugs. Immunology 14: 181-196.
19. Sun, Y., E. Iglesias, A. Samri, G. Kamkamidze, T. Decoville, G. Carcelain, and B. Autran. 2003. A systematic comparison of methods to measure HIV-1 specific CD8 T cells. J. Immunol. Methods 272: 23-34. (Pubitemid 36050742)
20. + T cells during the early phase of pediatric human immunodeficiency virus infection: characterization of expanded cell populations by T cell receptor phenotyping. J. Infect. Dis. 181: 107-120.
21. Brochet, X., M. P. Lefranc, and V. Giudicelli. 2008. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36(Web Server issue): W503-W508.
22. + T lymphocytes. J. Immunol. 178: 4112-4119.
23. Precopio, M. L., M. R. Betts, J. Parrino, D. A. Price, E. Gostick, D. R. Ambrozak, T. E. Asher, D. C. Douek, A. Harari, G. Pantaleo, et al. 2007. Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8(+) T cell responses. J. Exp. Med. 204: 1405-1416.
24. Rock, E. P., P. R. Sibbald, M. M. Davis, and Y. H. Chien. 1994. CDR3 length in antigen-specific immune receptors. J. Exp. Med. 179: 323-328.
25. Allan, S. E., A. N. Alstad, N. Merindol, N. K. Crellin, M. Amendola, R. Bacchetta, L. Naldini, M. G. Roncarolo, H. Soudeyns, and M. K. Levings. 2008. Generation of potent and stable human CD4+ T regulatory cells by activation-independent expression of FOXP3. Mol. Ther. 16: 194-202.
26. Currier, J. R., H. Deulofeut, K. S. Barron, P. J. Kehn, and M. A. Robinson. 1996. Mitogens, superantigens, and nominal antigens elicit distinctive patterns of TCRB CDR3 diversity. Hum. Immunol. 48: 39-51.
27. + T cells. J. Exp. Med. 186: 1407-1418.
28. Berthou, C., S. Legros-Maïda, A. Soulié, A. Wargnier, J. Guillet, C. Rabian, E. Gluckman, and M. Sasportes. 1995. Cord blood T lymphocytes lack constitutive perforin expression in contrast to adult peripheral blood T lymphocytes. Blood 85: 1540-1546.
29. Moretta, A., F. Locatelli, G. Mingrat, G. Rondini, D. Montagna, P. Comoli, S. Gandossini, E. Montini, M. Labirio, and R. Maccario. 1999. Characterisation of CTL directed towards non-inherited maternal alloantigens in human cord blood. Bone Marrow Transplant. 24: 1161-1166. (Pubitemid 30021207)
30. Porcu, P., J. Gaddy, and H. E. Broxmeyer. 1998. Alloantigen-induced unresponsiveness in cord blood T lymphocytes is associated with defective activation of Ras. Proc. Natl. Acad. Sci. USA 95: 4538-4543.
31. McHeyzer-Williams, M. G., and M. M. Davis. 1995. Antigen-specific development of primary and memory T cells in vivo. Science 268: 106-111.
32. Early, E., and D. J. Reen. 1999. Rapid conversion of naive to effector T cell function counteracts diminished primary human newborn T cell responses. Clin. Exp. Immunol. 116: 527-533.
33. Szabolcs, P., K. D. Park, M. Reese, L. Marti, G. Broadwater, and J. Kurtzberg. 2003. Coexistent naïve phenotype and higher cycling rate of cord blood T cells as compared to adult peripheral blood. Exp. Hematol. 31: 708-714.
34. Aggarwal, S., A. Gupta, S. Nagata, and S. Gupta. 1997. Programmed cell death (apoptosis) in cord blood lymphocytes. J. Clin. Immunol. 17: 63-73.
35. Hassan, J., and D. J. Reen. 2001. Human recent thymic emigrants - identification, expansion, and survival characteristics. J. Immunol. 167: 1970-1976.
36. Goodwin, V. J., T. A. Sato, M. D. Mitchell, and J. A. Keelan. 1998. Antiinflammatory effects of interleukin-4, interleukin-10, and transforming growth factor-beta on human placental cells in vitro. Am. J. Reprod. Immunol. 40: 319-325.
37. Mazur, M. A., C. C. Davis, and P. Szabolcs. 2008. Ex vivo expansion and Th1/Tc1 maturation of umbilical cord blood T cells by CD3/CD28 costimulation. Biol. Blood Marrow Transplant. 14: 1190-1196.
38. + T cells. Blood 111: 1378-1386.
39. + T cells are subject to immunomodulation by direct TLR2 or TLR5 stimulation. J. Immunol. 182: 55-62.
40. Zhang, S. Y., S. Boisson-Dupuis, A. Chapgier, K. Yang, J. Bustamante, A. Puel, C. Picard, L. Abel, E. Jouanguy, and J. L. Casanova. 2008. Inborn errors of interferon (IFN)-mediated immunity in humans: insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense. Immunol. Rev. 226: 29-40.
41. Ribeiro-do-Couto, L. M., L. C. Boeije, J. S. Kroon, B. Hooibrink, B. S. Breur-Vriesendorp, L. A. Aarden, and C. J. Boog. 2001. High IL-13 production by human neonatal T cells: neonate immune system regulator? Eur. J. Immunol. 31: 3394-3402.
42. + T cells. Blood 113: 6648-6657.
43. Alexander-Miller, M. A. 2000. Differential expansion and survival of high and low avidity cytotoxic T cell populations during the immune response to a viral infection. Cell. Immunol. 201: 58-62.
44. Alexander-Miller, M. A., G. R. Leggatt, and J. A. Berzofsky. 1996. Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93: 4102-4107.
45. + T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
46. + T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204: 2473-2485.
47. Hanley, P. J., C. R. Cruz, B. Savoldo, A. M. Leen, M. Stanojevic, M. Khalil, W. Decker, J. J. Molldrem, H. Liu, A. P. Gee, et al. 2009. Functionally active virus-specific T cells that target CMV, adenovirus, and EBV can be expanded from naive T-cell populations in cord blood and will target a range of viral epitopes. Blood 114: 1958-1967.
48. Obst, R., C. Münz, S. Stevanović, and H. G. Rammensee. 1998. Allo- and self-restricted cytotoxic T lymphocytes against a peptide library: evidence for a functionally diverse allorestricted T cell repertoire. Eur. J. Immunol. 28: 2432-2443.
49. Münz, C., R. Obst, W. Osen, S. Stevanović, and H. G. Rammensee. 1999. Alloreactivity as a source of high avidity peptide-specific human CTL. J. Immunol. 162: 25-34.
50. + T cell differentiation in peripheral blood. Eur. J. Immunol. 35: 2608-2616.
51. + T cells differently expressing three cytolytic effector molecules. J. Immunol. 177: 4330-4340.
52. Harari, A., V. Dutoit, C. Cellerai, P. A. Bart, R. A. Du Pasquier, and G. Pantaleo. 2006. Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol. Rev. 211: 236-254.
53. + CTL. J. Immunol. 174: 6809-6819.
54. Xu, X. N., M. A. Purbhoo, N. Chen, J. Mongkolsapaya, J. H. Cox, U. C. Meier, S. Tafuro, P. R. Dunbar, A. K. Sewell, C. S. Hourigan, et al. 2001. A novel approach to antigen-specific deletion of CTL with minimal cellular activation using alpha3 domain mutants of MHC class I/peptide complex. Immunity 14: 591-602.
55. Brunstein, C. G., K. S. Baker, and J. E. Wagner. 2007. Umbilical cord blood transplantation for myeloid malignancies. Curr. Opin. Hematol. 14: 162-169.
56. Arora, M., S. Nagaraj, J. E. Wagner, J. N. Barker, C. G. Brunstein, L. J. Burns, T. E. Defor, M. L. McMillan, J. S. Miller, and D. J. Weisdorf. 2007. Chronic graft-versus-host disease (cGVHD) following unrelated donor hematopoietic stem cell transplantation (HSCT): higher response rate in recipients of unrelated donor (URD) umbilical cord blood (UCB). Biol. Blood Marrow Transplant. 13: 1145-1152.