Human cytomegalovirus elicits fetal γδ T cell responses in utero

Journal of Experimental Medicine

Volumn 207, Issue 4, 2010, Pages 807-821

  Vermijlen, David ^a   Brouwer, Margreet ^a   Donner, Catherine ^b   Liesnard, Corinne ^b   Tackoen, Marie ^c   Van Rysselberge, Michel ^c   Twité, Nicolas ^a   Goldman, Michel ^a   Marchant, Arnaud ^a   Willems, Fabienne ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b ERASME HOSPITAL   (Belgium)

^c SAINT PIERRE UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; GAMMA INTERFERON; NATURAL KILLER CELL RECEPTOR; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR T BET;

ARTICLE; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; GAMMA DELTA T LYMPHOCYTE; GENE EXPRESSION; GESTATION PERIOD; HISTOCOMPATIBILITY COMPLEX; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNITY; INTRAUTERINE INFECTION; NEWBORN; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

AMINO ACID SEQUENCE; ANTIGENS, CD3; ANTIGENS, SURFACE; CELL COUNT; CELL DIFFERENTIATION; CHEMOKINES; COMPLEMENTARITY DETERMINING REGIONS; CYTOKINES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FETAL BLOOD; FETUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GESTATIONAL AGE; GRANZYMES; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; PREGNANCY; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, CHEMOKINE; RECEPTORS, NATURAL KILLER CELL; T-LYMPHOCYTE SUBSETS;

EID: 77951058003     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20090348     Document Type: Article

References (73)

1. Adams, E.J., Y.H. Chien, and K.C. Garcia. 2005. Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science. 308:227-231. doi:10.1126/science.1106885
2. Andrade, F., E. Fellows, D.E. Jenne, A. Rosen, and C.S. Young. 2007. Granzyme H destroys the function of critical adenoviral proteins required for viral DNA replication and granzyme B inhibition. EMBO J. 26:2148-2157. doi:10.1038/sj.emboj.7601650 (Pubitemid 46625785)
3. Appay, V., P.R. Dunbar, M. Callan, P. Klenerman, G.M. Gillespie, L. Papagno, G.S. Ogg, A. King, F. Lechner, C.A. Spina, et al. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8:379-385. doi:10.1038/nm0402-379 (Pubitemid 34407033)
4. Battistini, L., G. Borsellino, G. Sawicki, F. Poccia, M. Salvetti, G. Ristori, and C.F. Brosnan. 1997. Phenotypic and cytokine analysis of human peripheral blood gamma delta T cells expressing NK cell receptors. J. Immunol. 159:3723-3730. (Pubitemid 127469626)
5. + cells with restricted T cell receptor δ gene junctional repertoire in the peripheral blood of healthy donors. J. Exp. Med. 178:121-127. doi:10.1084/jem.178.1.121
6. Bolovan-Fritts, C.A., R.N. Trout, and S.A. Spector. 2004. Human cytomegalovirus-specific CD4+-T-cell cytokine response induces fractalkine in endothelial cells. J. Virol. 78:13173-13181. doi:10.1128/JVI.78.23.13173-13181. 2004
7. Bovenschen, N., P.J. de Koning, R. Quadir, R. Broekhuizen, J.M. Damen, C.J. Froelich, M. Slijper, and J.A. Kummer. 2008. NK cell protease granzyme M targets alpha-tubulin and disorganizes the microtubule network. J. Immunol. 180:8184-8191.
8. Brandes, M., K. Willimann, G. Bioley, N. Lévy, M. Eberl, M. Luo, R. Tampé, F. Lévy, P. Romero, and B. Moser. 2009. Cross-presenting human gammadelta T cells induce robust CD8+ alphabeta T cell responses. Proc. Natl. Acad. Sci. USA. 106:2307-2312. doi:10.1073/pnas.0810059106
9. 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:W503-W508. doi:10.1093/nar/gkn316
10. Caccamo, N., G. Sireci, S. Meraviglia, F. Dieli, J. Ivanyi, and A. Salerno. 2006. gammadelta T cells condition dendritic cells in vivo for priming pulmonary CD8 T cell responses against Mycobacterium tuberculosis. Eur. J. Immunol. 36:2681-2690. doi:10.1002/eji.200636220 (Pubitemid 44608452)
11. Cairo, C., G. Mancino, G. Cappelli, C.D. Pauza, E. Galli, E. Brunetti, and V. Colizzi. 2008. Vdelta2 T-lymphocyte responses in cord blood samples from Italy and Côte d'Ivoire. Immunology. 124:380-387. doi:10.1111/j.1365-2567. 2007.02784.x (Pubitemid 351793470)
12. Chen, L., W. He, S.T. Kim, J. Tao, Y. Gao, H. Chi, A.M. Intlekofer, B. Harvey, S.L. Reiner, Z. Yin, et al. 2007. Epigenetic and transcriptional programs lead to default IFN-gamma production by gammadelta T cells. J. Immunol. 178:2730-2736. (Pubitemid 46333149)
13. Chien, Y.H., and Y. Konigshofer. 2007. Antigen recognition by gammadelta T cells. Immunol. Rev. 215:46-58. doi:10.1111/j.1600-065X.2006.00470.x
14. Chowdhury, D., and J. Lieberman. 2008. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26:389-420. doi:10.1146/annurev.immunol.26.021607.090404 (Pubitemid 351611623)
15. Conti, L., R. Casetti, M. Cardone, B. Varano, A. Martino, F. Belardelli, F. Poccia, and S. Gessani. 2005. Reciprocal activating interaction between dendritic cells and pamidronate-stimulated gammadelta T cells: role of CD86 and inflammatory cytokines. J. Immunol. 174:252-260. (Pubitemid 40007411)
16. Dalle, J.H., J. Menezes, E. Wagner, M. Blagdon, J. Champagne, M.A. Champagne, and M. Duval. 2005. Characterization of cord blood natural killer cells: implications for transplantation and neonatal infections. Pediatr. Res. 57:649-655. doi:10.1203/01.PDR.0000156501.55431.20
17. Davis, M.M., J.J. Boniface, Z. Reich, D. Lyons, J. Hampl, B. Arden, and Y. Chien. 1998. Ligand recognition by alpha beta T cell receptors. Annu. Rev. Immunol. 16:523-544. doi:10.1146/annurev.immunol.16.1.523
18. Day, E.K., A.J. Carmichael, I.J. ten Berge, E.C. Waller, J.G. Sissons, and M.R. Wills. 2007. Rapid CD8+ T cell repertoire focusing and selection of high-affinity clones into memory following primary infection with a persistent human virus: human cytomegalovirus. J. Immunol. 179:3203-3213.
19. De Libero, G. 1999. Control of gammadelta T cells by NK receptors. Microbes Infect. 1:263-267. doi:10.1016/S1286-4579(99)80043-4
20. De Rosa, S.C., J.P. Andrus, S.P. Perfetto, J.J. Mantovani, L.A. Herzenberg, L.A. Herzenberg, and M. Roederer. 2004. Ontogeny of gamma delta T cells in humans. J. Immunol. 172:1637-1645.
21. Déchanet, J., P. Merville, A. Lim, C. Retière, V. Pitard, X. Lafarge, S. Michelson, C. Méric, M.M. Hallet, P. Kourilsky, et al. 1999. Implication of gammadelta T cells in the human immune response to cytomegalovirus. J. Clin. Invest. 103:1437-1449. doi:10.1172/JCI5409 (Pubitemid 29535500)
22. Devilder, M.C., S. Maillet, I. Bouyge-Moreau, E. Donnadieu, M. Bonneville, and E. Scotet. 2006. Potentiation of antigen-stimulated V gamma 9V delta 2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. J. Immunol. 176:1386-1393. (Pubitemid 43134280)
23. Dieli, F., D. Vermijlen, F. Fulfaro, N. Caccamo, S. Meraviglia, G. Cicero, A. Roberts, S. Buccheri, M. D'Asaro, N. Gebbia, et al. 2007. Targeting human gammadelta T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 67:7450-7457. doi:10.1158/0008-5472.CAN-07-0199 (Pubitemid 47206575)
24. Dollard, S.C., S.D. Grosse, and D.S. Ross. 2007. New estimates of the prevalence of neurological and sensory sequelae and mortality associated with congenital cytomegalovirus infection. Rev. Med. Virol. 17:355-363. doi:10.1002/rmv.544
25. Eberl, M., R. Engel, S. Aberle, P. Fisch, H. Jomaa, and H. Pircher. 2005. Human Vgamma9/Vdelta2 effector memory T cells express the killer cell lectin-like receptor G1 (KLRG1). J. Leukoc. Biol. 77:67-70.
26. Eberl, M., G.W. Roberts, S. Meuter, J.D. Williams, N. Topley, and B. Moser. 2009. A rapid crosstalk of human gammadelta T cells and monocytes drives the acute inflammation in bacterial infections. PLoS Pathog. 5:e1000308. doi:10.1371/journal.ppat.1000308
27. Gibbons, D.L., S.F. Haque, T. Silberzahn, K. Hamilton, C. Langford, P. Ellis, R. Carr, and A.C. Hayday. 2009. Neonates harbour highly active gammadelta T cells with selective impairments in preterm infants. Eur. J. Immunol. 39:1794-1806. doi:10.1002/eji.200939222
28. Goriely, S., C. Van Lint, R. Dadkhah, M. Libin, D. De Wit, D. Demonté, F. Willems, and M. Goldman. 2004. A defect in nucleosome remodeling prevents IL-12(p35) gene transcription in neonatal dendritic cells. J. Exp. Med. 199:1011-1016. doi:10.1084/jem.20031272
29. neg γδ T cells against cytomegalovirus-infected cells and tumor intestinal epithelial cells. J. Exp. Med. 201:1567-1578. doi:10.1084/jem.20041851
30. Hayday, A.C. 2000. [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu. Rev. Immunol. 18:975-1026. doi:10.1146/annurev.immunol.18.1.975
31. Hayday, A.C. 2009. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity. 31:184-196. doi:10.1016/j.immuni.2009. 08.006
32. Hinz, T., D. Wesch, F. Halary, S. Marx, A. Choudhary, B. Arden, O. Janssen, M. Bonneville, and D. Kabelitz. 1997. Identification of the complete expressed human TCR V gamma repertoire by flow cytometry. Int. Immunol. 9:1065-1072. doi:10.1093/intimm/9.8.1065
33. Holtmeier, W., and D. Kabelitz. 2005. gammadelta T cells link innate and adaptive immune responses. Chem. Immunol. Allergy. 86:151-183. doi:10.1159/000086659
34. Ismaili, J., V. Olislagers, R. Poupot, J.J. Fournié, and M. Goldman. 2002. Human gamma delta T cells induce dendritic cell maturation. Clin. Immunol. 103:296-302. doi:10.1006/clim.2002.5218
35. Kabelitz, D., T. Ackermann, T. Hinz, F. Davodeau, H. Band, M. Bonneville, O. Janssen, B. Arden, and S. Schondelmaier. 1994. New monoclonal antibody (23D12) recognizing three different V gamma elements of the human gamma delta T cell receptor. 23D12+ cells comprise a major subpopulation of gamma delta T cells in postnatal thymus. J. Immunol. 152:3128-3136.
36. Kabelitz, D., D. Wesch, and W. He. 2007. Perspectives of gammadelta T cells in tumor immunology. Cancer Res. 67:5-8. doi:10.1158/0008-5472. CAN-06-3069
37. Kersten, C.M., R.T. McCluskey, L.A. Boyle, and J.T. Kurnick. 1996. Escherichia coli and Pseudomonas aeruginosa induce expansion of V delta 2 cells in adult peripheral blood, but of V delta 1 cells in cord blood. J. Immunol. 157:1613-1619.
38. Lafarge, X., P. Merville, M.C. Cazin, F. Bergé, L. Potaux, J.F. Moreau, and J. Déchanet-Merville. 2001. Cytomegalovirus infection in transplant recipients resolves when circulating gammadelta T lymphocytes expand, suggesting a protective antiviral role. J. Infect. Dis. 184:533-541. doi:10.1086/322843
39. Lanier, L.L. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9:495-502. doi:10.1038/ni1581
40. Lee, H.H., C.M. Hoeman, J.C. Hardaway, F.B. Guloglu, J.S. Ellis, R. Jain, R. Divekar, D.M. Tartar, C.L. Haymaker, and H. Zaghouani. 2008. Delayed maturation of an IL-12-producing dendritic cell subset explains the early Th2 bias in neonatal immunity. J. Exp. Med. 205:2269-2280. doi:10.1084/jem.20071371
41. Levy, O. 2007. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat. Rev. Immunol. 7:379-390. doi:10.1038/nri2075
42. Lewis, D.B., and C.B. Wilson. 2001. Developmental immunology and role of host defenses in fetal and neonatal susceptibility to infection. In Infectious Disease of the Fetus and Newborn Infant. J.S. Remington and J.O. Klein, editors. W.B. Saunders Company, Philadelphia, PA. 25-138.
43. Lieberman, J. 2003. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3:361-370. doi:10.1038/nri1083
44. Liesnard, C., C. Donner, F. Brancart, F. Gosselin, M.L. Delforge, and F. Rodesch. 2000. Prenatal diagnosis of congenital cytomegalovirus infection: prospective study of 237 pregnancies at risk. Obstet. Gynecol. 95:881-888. doi:10.1016/S0029-7844(99)00657-2
45. Marchant, A., and M. Goldman. 2005. T cell-mediated immune responses in human newborns: ready to learn? Clin. Exp. Immunol. 141:10-18. doi:10.1111/j.1365-2249.2005.02799.x
46. 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.
47. Marcolino, I., G.K. Przybylski, M. Koschella, C.A. Schmidt, D. Voehringer, M. Schlesier, and H. Pircher. 2004. Frequent expression of the natural killer cell receptor KLRG1 in human cord blood T cells: correlation with replicative history. Eur. J. Immunol. 34:2672-2680. doi:10.1002/eji.200425282
48. Maródi, L. 2006. Neonatal innate immunity to infectious agents. Infect. Immun. 74:1999-2006. doi:10.1128/IAI.74.4.1999-2006.2006
49. Metkar, S.S., C. Menaa, J. Pardo, B. Wang, R. Wallich, M. Freudenberg, S. Kim, S.M. Raja, L. Shi, M.M. Simon, and C.J. Froelich. 2008. Human and mouse granzyme A induce a proinflammatory cytokine response. Immunity. 29:720-733. doi:10.1016/j.immuni.2008.08.014
50. Mold, J.E., J. Michaëlsson, T.D. Burt, M.O. Muench, K.P. Beckerman, M.P. Busch, T.H. Lee, D.F. Nixon, and J.M. McCune. 2008. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science. 322:1562-1565. doi:10.1126/science.1164511
51. Morita, C.T., C.M. Parker, M.B. Brenner, and H. Band. 1994. TCR usage and functional capabilities of human gamma delta T cells at birth. J. Immunol. 153:3979-3988.
52. Morita, C.T., C. Jin, G. Sarikonda, and H. Wang. 2007. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vgamma2Vdelta2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol. Rev. 215:59-76. doi:10.1111/j.1600- 065X.2006.00479.x
53. Parker, C.M., V. Groh, H. Band, S.A. Porcelli, C. Morita, M. Fabbi, D. Glass, J.L. Strominger, and M.B. Brenner. 1990. Evidence for extrathymic changes in the T cell receptor γ/δ repertoire. J. Exp. Med. 171:1597-1612. doi:10.1084/jem.171.5.1597
54. Pennington, D.J., D. Vermijlen, E.L. Wise, S.L. Clarke, R.E. Tigelaar, and A.C. Hayday. 2005. The integration of conventional and unconventional T cells that characterizes cell-mediated responses. Adv. Immunol. 87:27-59. doi:10.1016/S0065-2776(05)87002-6
55. Peyrat, M.A., F. Davodeau, I. Houde, F. Romagné, A. Necker, C. Leget, J.P. Cervoni, N. Cerf-Bensussan, H. Vié, M. Bonneville, and M.M. Hallet. 1995. Repertoire analysis of human peripheral blood lymphocytes using a human V delta 3 region-specific monoclonal antibody. Characterization of dual T cell receptor (TCR) delta-chain expressors and alpha beta T cells expressing V delta 3J alpha C alpha-encoded TCR chains. J. Immunol. 155:3060-3067.
56. Pitard, V., D. Roumanes, X. Lafarge, L. Couzi, I. Garrigue, M.E. Lafon, P. Merville, J.F. Moreau, and J. Déchanet-Merville. 2008. Longterm expansion of effector/memory Vdelta2-gammadelta T cells is a specific blood signature of CMV infection. Blood. 112:1317-1324. doi:10.1182/blood-2008-01- 136713
57. Ramsburg, E., R. Tigelaar, J. Craft, and A. Hayday. 2003. Age-dependent requirement for γδ T cells in the primary but not secondary protective immune response against an intestinal parasite. J. Exp. Med. 198:1403-1414. doi:10.1084/jem.20030050
58. Romero, V., E. Fellows, D.E. Jenne, and F. Andrade. 2009. Cleavage of La protein by granzyme H induces cytoplasmic translocation and interferes with La-mediated HCV-IRES translational activity. Cell Death Differ. 16:340-348. doi:10.1038/cdd.2008.165
59. Stagno, S. 2001. Cytomegalovirus. In Infectious Diseases of the Fetus and Newborn Infants. J.S. Remington and J.O. Klein, editors. W.B. Saunders Company, Philadelphia, PA. 389-424.
60. Tabi, Z., M. Moutaftsi, and L.K. Borysiewicz. 2001. Human cytomegalovirus pp65- and immediate early 1 antigen-specific HLA class I-restricted cytotoxic T cell responses induced by cross-presentation of viral antigens. J. Immunol. 166:5695-5703.
61. Toulon, A., L. Breton, K.R. Taylor, M. Tenenhaus, D. Bhavsar, C. Lanigan, R. Rudolph, J. Jameson, and W.L. Havran. 2009. A role for human skin-resident T cells in wound healing. J. Exp. Med. 206:743-750. doi:10.1084/jem.20081787
62. Trautmann, L., M. Rimbert, K. Echasserieau, X. Saulquin, B. Neveu, J. Déchanet, V. Cerundolo, and M. Bonneville. 2005. Selection of T cell clones expressing high-affinity public TCRs within Human cytomegalovirus- specific CD8 T cell responses. J. Immunol. 175:6123-6132.
63. van Leeuwen, E.M., G.J. de Bree, I.J. ten Berge, and R.A. van Lier. 2006. Human virus-specific CD8+ T cells: diversity specialists. Immunol. Rev. 211:225-235. doi:10.1111/j.0105-2896.2006.00379.x
64. Vanhecke, D., B. Verhasselt, V. Debacker, G. Leclercq, J. Plum, and B. Vandekerckhove. 1995. Differentiation to T helper cells in the thymus. Gradual acquisition of T helper cell function by CD3+CD4+ cells. J. Immunol. 155:4711-4718.
65. Vermijlen, D., D. Luo, C.J. Froelich, J.P. Medema, J.A. Kummer, E. Willems, F. Braet, and E. Wisse. 2002. Hepatic natural killer cells exclusively kill splenic/blood natural killer-resistant tumor cells by the perforin/granzyme pathway. J. Leukoc. Biol. 72:668-676.
66. Vermijlen, D., P. Ellis, C. Langford, A. Klein, R. Engel, K. Willimann, H. Jomaa, A.C. Hayday, and M. Eberl. 2007. Distinct cytokine-driven responses of activated blood gammadelta T cells: insights into unconventional T cell pleiotropy. J. Immunol. 178:4304-4314.
67. Wang, L., A. Kamath, H. Das, L. Li, and J.F. Bukowski. 2001. Antibacterial effect of human V gamma 2V delta 2 T cells in vivo. J. Clin. Invest. 108:1349-1357.
68. Wang, T., Y. Gao, E. Scully, C.T. Davis, J.F. Anderson, T. Welte, M. Ledizet, R. Koski, J.A. Madri, A. Barrett, et al. 2006. Gamma delta T cells facilitate adaptive immunity against West Nile virus infection in mice. J. Immunol. 177:1825-1832.
69. Wesch, D., T. Hinz, and D. Kabelitz. 1998. Analysis of the TCR Vgamma repertoire in healthy donors and HIV-1-infected individuals. Int. Immunol. 10:1067-1075. doi:10.1093/intimm/10.8.1067 (Pubitemid 28362680)
70. White, G.P., P.M. Watt, B.J. Holt, and P.G. Holt. 2002. 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 CD45RO- T cells. J. Immunol. 168:2820-2827.
71. Wilhelm, M., V. Kunzmann, S. Eckstein, P. Reimer, F. Weissinger, T. Ruediger, and H.P. Tony. 2003. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood. 102:200-206. doi:10.1182/blood-2002-12-3665 (Pubitemid 36759655)
72. Wilkinson, G.W., P. Tomasec, R.J. Stanton, M. Armstrong, V. Prod'homme, R. Aicheler, B.P. McSharry, C.R. Rickards, D. Cochrane, S. Llewellyn-Lacey, et al. 2008. Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 41:206-212. doi:10.1016/j.jcv.2007.10.027
73. Yin, Z., C. Chen, S.J. Szabo, L.H. Glimcher, A. Ray, and J. Craft. 2002. T-Bet expression and failure of GATA-3 cross-regulation lead to default production of IFN-gamma by gammadelta T cells. J. Immunol. 168:1566-1571. (Pubitemid 34135750)