Effector vγ9vδ2 t cells dominate the human fetal γδ t-cell repertoire

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 6, 2015, Pages E556-E565

  Dimova, Tanya ^a,d   Brouwer, Margreet ^a   Gosselin, Françoise ^b   Tassignon, Joël ^c   Leo, Oberdan ^a   Donner, Catherine ^b   Marchant, Arnaud ^a   Vermijlen, David ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b ERASME HOSPITAL   (Belgium)

^c ImmuneHealth   (Belgium)

^d BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

Author keywords

Fetus; Gammadelta; Human; Neonate; V 9V 2

Indexed keywords

GAMMA INTERFERON; GRANZYME; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; PRIMER DNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXPOSURE; FETUS; FETUS BLOOD; GAMMA DELTA T LYMPHOCYTE; GENE SEQUENCE; GENETIC VARIABILITY; GERM LINE; GESTATIONAL AGE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SECOND TRIMESTER PREGNANCY; VGAMMA9VDELTA2 T LYMPHOCYTE; ANIMAL; DNA SEQUENCE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; MICROARRAY ANALYSIS; NONPARAMETRIC TEST; T LYMPHOCYTE SUBPOPULATION;

MURINAE;

ANIMALS; DNA PRIMERS; FETUS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; IMMUNE SYSTEM; MICE; MICROARRAY ANALYSIS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SEQUENCE ANALYSIS, DNA; STATISTICS, NONPARAMETRIC; T-LYMPHOCYTE SUBSETS;

EID: 84922629691     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1412058112     Document Type: Article

References (91)

1. Hayday AC (2000) [gamma][delta] cells: A right time and a right place for a conserved third way of protection. Annu Rev Immunol 18:975-1026.
2. Chien YH, Konigshofer Y (2007) Antigen recognition by gammadelta T cells. Immunol Rev 215:46-58.
3. Bonneville M, O'Brien RL, Born WK (2010) Gammadelta T cell effector functions: A blend of innate programming and acquired plasticity. Nat Rev Immunol 10(7): 467-478.
4. Hirano M, et al. (2013) Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501(7467):435-438.
5. Vantourout P, Hayday A (2013) Six-of-the-best: Unique contributions of γδ T cells to immunology. Nat Rev Immunol 13(2):88-100.
6. Willcox CR, et al. (2012) Cytomegalovirus and tumor stress surveillance by binding of a human γδ T cell antigen receptor to endothelial protein C receptor. Nat Immunol 13(9):872-879.
7. Adams EJ, Chien YH, Garcia KC (2005) Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science 308(5719):227-231.
8. Zeng X, et al. (2012) γδ T cells recognize a microbial encoded B cell antigen to initiate a rapid antigen-specific interleukin-17 response. Immunity 37(3):524-534.
9. Hayday A, Vantourout P (2013) A long-playing CD about the γδ TCR repertoire. Immunity 39(6):994-996.
10. Luoma AM, et al. (2013) Crystal structure of Vδ1 T cell receptor in complex with CD1dsulfatide shows MHC-like recognition of a self-lipid by human γδ T cells. Immunity 39(6):1032-1042.
11. Uldrich AP, et al. (2013) CD1d-lipid antigen recognition by the γδ TCR. Nat Immunol 14(11):1137-1145.
12. Pang DJ, Neves JF, Sumaria N, Pennington DJ (2012) Understanding the complexity of γδ T-cell subsets in mouse and human. Immunology 136(3):283-290.
13. Eberl M, et al. (2003) Microbial isoprenoid biosynthesis and human gammadelta T cell activation. FEBS Lett 544(1-3):4-10.
14. Vavassori S, et al. (2013) Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat Immunol 14(9):908-916.
15. Wang H, et al. (2013) Butyrophilin 3A1 plays an essential role in prenyl pyrophosphate stimulation of human Vγ2Vδ2 T cells. J Immunol 191(3):1029-1042.
16. Sandstrom A, et al. (2014) The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity 40(4): 490-500.
17. Karunakaran MM, Göbel TW, Starick L, Walter L, Herrmann T (2014) Vγ9 and Vδ2 T cell antigen receptor genes and butyrophilin 3 (BTN3) emerged with placental mammals and are concomitantly preserved in selected species like alpaca (Vicugna pacos). Immunogenetics 66(4):243-254.
18. Gober HJ, et al. (2003) Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 197(2):163-168.
19. Dieli F, et al. (2007) Targeting human gammadelta T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 67(15):7450-7457.
20. Wilhelm M, et al. (2003) Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood 102(1):200-206.
21. Kalyan S, Kabelitz D (2013) Defining the nature of human γδ T cells: A biographical sketch of the highly empathetic. Cell Mol Immunol 10(1):21-29.
22. Marchant A, Goldman M (2005) T cell-mediated immune responses in human newborns: Ready to learn? Clin Exp Immunol 141(1):10-18.
23. Adkins B, Leclerc C, Marshall-Clarke S (2004) Neonatal adaptive immunity comes of age. Nat Rev Immunol 4(7):553-564.
24. Mold JE, et al. (2010) Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 330(6011):1695-1699.
25. Zhang X, Yu S, Hoffmann K, Yu K, Förster R (2012) Neonatal lymph node stromal cells drive myelodendritic lineage cells into a distinct population of CX3CR1+CD11b+F4/80+ regulatory macrophages in mice. Blood 119(17):3975-3986.
26. Burt TD (2013) Fetal regulatory T cells and peripheral immune tolerance in utero: Implications for development and disease. Am J Reprod Immunol 69(4):346-358.
27. Kollmann TR, Levy O, Montgomery RR, Goriely S (2012) Innate immune function by Toll-like receptors: Distinct responses in newborns and the elderly. Immunity 37(5): 771-783.
28. Ramsburg E, Tigelaar R, Craft J, Hayday A (2003) Age-dependent requirement for gammadelta T cells in the primary but not secondary protective immune response against an intestinal parasite. J Exp Med 198(9):1403-1414.
29. De Rosa SC, et al. (2004) Ontogeny of gamma delta T cells in humans. J Immunol 172(3):1637-1645.
30. Gibbons DL, et al. (2009) Neonates harbour highly active gammadelta T cells with selective impairments in preterm infants. Eur J Immunol 39(7):1794-1806.
31. Vermijlen D, et al. (2010) Human cytomegalovirus elicits fetal gammadelta T cell responses in utero. J Exp Med 207(4):807-821.
32. Moens E, et al. (2011) IL-23R and TCR signaling drives the generation of neonatal Vgamma9Vdelta2 T cells expressing high levels of cytotoxic mediators and producing IFN-gamma and IL-17. J Leukoc Biol 89(5):743-752.
33. Cairo C, et al. (2014) Cord blood Vγ2Vδ2 T cells provide a molecular marker for the influence of pregnancy-associated malaria on neonatal immunity. J Infect Dis 209(10): 1653-1662.
34. Lewis DB, Wilson CB (2006) Infectious Disease of the Fetus and Newborn Infant, eds Remington JS, Klein JO (Elsevier Saunders, Philadelphia), pp 87-210.
35. Carding SR, Egan PJ (2002) Gammadelta T cells: Functional plasticity and heterogeneity. Nat Rev Immunol 2(5):336-345.
36. Shibata K (2012) Close link between development and function of gamma-delta T cells. Microbiol Immunol 56(4):217-227.
37. Prinz I, Silva-Santos B, Pennington DJ (2013) Functional development of γδ T cells. Eur J Immunol 43(8):1988-1994.
38. Morita CT, Parker CM, Brenner MB, Band H (1994) TCR usage and functional capabilities of human gamma delta T cells at birth. J Immunol 153(9):3979-3988.
39. Wang H, Fang Z, Morita CT (2010) Vgamma2Vdelta2 T Cell Receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J Immunol 184(11):6209-6222.
40. Davodeau F, et al. (1993) Peripheral selection of antigen receptor junctional features in a major human gamma delta subset. Eur J Immunol 23(4):804-808.
41. Li W, et al. (2010) Effect of IL-18 on expansion of gammadelta T cells stimulated by zoledronate and IL-2. J Immunother 33(3):287-296.
42. Jensen KD, et al. (2008) Thymic selection determines gammadelta T cell effector fate: Antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity 29(1):90-100.
43. Ribot JC, et al. (2009) CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat Immunol 10(4):427-436.
44. Turchinovich G, Hayday AC (2011) Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γδ T cells. Immunity 35(1):59-68.
45. Cruz-Guilloty F, et al. (2009) Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J Exp Med 206(1):51-59.
46. Pham D, Vincentz JW, Firulli AB, Kaplan MH (2012) Twist1 regulates Ifng expression in Th1 cells by interfering with Runx3 function. J Immunol 189(2):832-840.
47. Savage AK, et al. (2008) The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29(3):391-403.
48. Kreslavsky T, et al. (2009) TCR-inducible PLZF transcription factor required for innate phenotype of a subset of gammadelta T cells with restricted TCR diversity. Proc Natl Acad Sci USA 106(30):12453-12458.
49. Alonzo ES, Sant'Angelo DB (2011) Development of PLZF-expressing innate T cells. Curr Opin Immunol 23(2):220-227.
50. Pereira P, Boucontet L (2012) Innate NKTγδ and NKTαβ cells exert similar functions and compete for a thymic niche. Eur J Immunol 42(5):1272-1281.
51. Rivera J, Proia RL, Olivera A (2008) The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol 8(10):753-763.
52. Marcolino I, et al. (2004) Frequent expression of the natural killer cell receptor KLRG1 in human cord blood T cells: Correlation with replicative history. Eur J Immunol 34(10):2672-2680.
53. Shiratori I, Ogasawara K, Saito T, Lanier LL, Arase H (2004) Activation of natural killer cells and dendritic cells upon recognition of a novel CD99-like ligand by paired immunoglobulin-like type 2 receptor. J Exp Med 199(4):525-533.
54. Gumbleton M, Kerr WG (2013) Role of inositol phospholipid signaling in natural killer cell biology. Front Immunol 4:47.
55. Pont F, et al. (2012) The gene expression profile of phosphoantigen-specific human γδ T lymphocytes is a blend of αβ T-cell and NK-cell signatures. Eur J Immunol 42(1): 228-240.
56. Parker CM, et al. (1990) Evidence for extrathymic changes in the T cell receptor gamma/delta repertoire. J Exp Med 171(5):1597-1612.
57. De Libero G, et al. (1991) Selection by two powerful antigens may account for the presence of the major population of human peripheral gamma/delta T cells. J Exp Med 173(6):1311-1322.
58. Peakman M, Buggins AG, Nicolaides KH, Layton DM, Vergani D (1992) Analysis of lymphocyte phenotypes in cord blood from early gestation fetuses. Clin Exp Immunol 90(2):345-350.
59. Krangel MS, Yssel H, Brocklehurst C, Spits H (1990) A distinct wave of human T cell receptor gamma/delta lymphocytes in the early fetal thymus: Evidence for controlled gene rearrangement and cytokine production. J Exp Med 172(3):847-859.
60. McVay LD, Carding SR, Bottomly K, Hayday AC (1991) Regulated expression and structure of T cell receptor gamma/delta transcripts in human thymic ontogeny. EMBO J 10(1):83-91.
61. McVay LD, Jaswal SS, Kennedy C, Hayday A, Carding SR (1998) The generation of human gammadelta T cell repertoires during fetal development. J Immunol 160(12): 5851-5860.
62. Delfau MH, Hance AJ, Lecossier D, Vilmer E, Grandchamp B (1992) Restricted diversity of V gamma 9-JP rearrangements in unstimulated human gamma/delta T lymphocytes. Eur J Immunol 22(9):2437-2443.
63. Sherwood AM, et al. (2011) Deep sequencing of the human TCRγ and TCRβ repertoires suggests that TCRβ rearranges after αβ and γδ T cell commitment. Sci Transl Med 3(90):90ra61.
64. McVay LD, Carding SR (1996) Extrathymic origin of human gamma delta T cells during fetal development. J Immunol 157(7):2873-2882.
65. Ikuta K, et al. (1990) A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 62(5):863-874.
66. Bukowski JF, Morita CT, Brenner MB (1999) Human gamma delta T cells recognize alkylamines derived from microbes, edible plants, and tea: Implications for innate immunity. Immunity 11(1):57-65.
67. Aagaard K, et al. (2014) The placenta harbors a unique microbiome. Sci Transl Med 6(237):37ra65.
68. Lewis JM, et al. (2006) Selection of the cutaneous intraepithelial gammadelta+ T cell repertoire by a thymic stromal determinant. Nat Immunol 7(8):843-850.
69. Vermijlen D, Prinz I (2014) Ontogeny of Innate T Lymphocytes - Some Innate Lymphocytes are More Innate than Others. Front Immunol 5:486.
70. Ribot JC, Ribeiro ST, Correia DV, Sousa AE, Silva-Santos B (2014) Human γδ thymocytes are functionally immature and differentiate into cytotoxic type 1 effector T cells upon IL-2/IL-15 signaling. J Immunol 192(5):2237-2243.
71. Chen L, et al. (2007) Epigenetic and transcriptional programs lead to default IFNgamma production by gammadelta T cells. J Immunol 178(5):2730-2736.
72. Yin Z, et al. (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(4):1566-1571.
73. Fahl SP, Coffey F, Wiest DL (2014) Origins of γδ T cell effector subsets: A riddle wrapped in an enigma. J Immunol 193(9):4289-4294.
74. Zhang X, et al. (2014) CD4 T cells with effector memory phenotype and function develop in the sterile environment of the fetus. Sci Transl Med 6(238):38ra72.
75. Anthony DA, Andrews DM, Watt SV, Trapani JA, Smyth MJ (2010) Functional dissection of the granzyme family: Cell death and inflammation. Immunol Rev 235(1): 73-92.
76. Joeckel LT, et al. (2011) Mouse granzyme K has pro-inflammatory potential. Cell Death Differ 18(7):1112-1119.
77. Spencer CT, et al. (2013) Granzyme A produced by γ(9)δ(2) T cells induces human macrophages to inhibit growth of an intracellular pathogen. PLoS Pathog 9(1):e1003119.
78. Glatzel A, et al. (2002) Patterns of chemokine receptor expression on peripheral blood gamma delta T lymphocytes: Strong expression of CCR5 is a selective feature of V delta 2/V gamma 9 gamma delta T cells. J Immunol 168(10):4920-4929.
79. Hamilton G, Colbert JD, Schuettelkopf AW, Watts C (2008) Cystatin F is a cathepsin C-directed protease inhibitor regulated by proteolysis. EMBO J 27(3):499-508.
80. Cairo C, et al. (2008) Vdelta2 T-lymphocyte responses in cord blood samples from Italy and Côte d'Ivoire. Immunology 124(3):380-387.
81. Hayday AC (2009) Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 31(2):184-196.
82. Klein JO, Baker CJ, Remington JS, Wilson CB (2006) Infectious Disease of the Fetus and Newborn Infant, eds Remington JS, Klein JO (Elsevier Saunders, Philadelphia), pp 3-25.
83. Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157(1):121-141.
84. PrabhuDas M, et al. (2011) Challenges in infant immunity: Implications for responses to infection and vaccines. Nat Immunol 12(3):189-194.
85. Gerdts V, Babiuk LA, Griebel PJ; van Drunen Littel-van den Hurk (2000) Fetal immunization by a DNA vaccine delivered into the oral cavity. Nat Med 6(8):929-932.
86. Ismaili J, Olislagers V, Poupot R, Fournié JJ, Goldman M (2002) Human gamma delta T cells induce dendritic cell maturation. Clin Immunol 103(3 Pt 1):296-302.
87. Fiore F, et al. (2007) Enhanced ability of dendritic cells to stimulate innate and adaptive immunity on short-term incubation with zoledronic acid. Blood 110(3): 921-927.
88. Liesnard C, et al. (2000) Prenatal diagnosis of congenital cytomegalovirus infection: Prospective study of 237 pregnancies at risk. Obstet Gynecol 95(6 Pt 1):881-888.
89. Bade B, et al. (2005) Differential expression of the granzymes A, K andM and perforin in human peripheral blood lymphocytes. Int Immunol 17(11):1419-1428.
90. Brochet X, Lefranc MP, Giudicelli V (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):W503-8.
91. Wang X, Spandidos A, Wang H, Seed B (2012) PrimerBank: A PCR primer database for quantitative gene expression analysis, 2012 update. Nucleic Acids Res 40(Database issue): D1144-D1149.