Clonal selection in the human Vδ1 T cell repertoire indicates γδ TCR-dependent adaptive immune surveillance

Nature Communications

Volumn 8, Issue , 2017, Pages

  Davey, Martin S ^a   Willcox, Carrie R ^a   Joyce, Stephen P ^a   Ladell, Kristin ^b   Kasatskaya, Sofya A ^c,d,e   McLaren, James E ^b   Hunter, Stuart ^a   Salim, Mahboob ^a   Mohammed, Fiyaz ^a   Price, David A ^b   Chudakov, Dmitriy M ^c,d,e   Willcox, Benjamin E ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

^e MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; BIOLOGICAL MARKER; CHEMOKINE RECEPTOR CX3CR1; CX3CR1 PROTEIN, HUMAN; INTERLEUKIN 15; LYMPHOCYTE ANTIGEN RECEPTOR;

BIOLOGY; BLOOD; CANCER; CELLS AND CELL COMPONENTS; GENETIC ANALYSIS; IMMUNITY; PHENOTYPE; PROTEIN;

ADAPTIVE IMMUNITY; ADULT; ARTICLE; CLONE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; MALIGNANT NEOPLASM; NEWBORN; NEXT GENERATION SEQUENCING; PHENOTYPE; T LYMPHOCYTE; UMBILICAL CORD BLOOD; VIRUS INFECTION; CELL CLONE; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLEMENTARITY DETERMINING REGION; CYTOLOGY; CYTOTOXICITY; DONOR; GENETIC VARIATION; GENETICS; METABOLISM;

ADULT; BIOMARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONE CELLS; COMPLEMENTARITY DETERMINING REGIONS; CX3C CHEMOKINE RECEPTOR 1; CYTOTOXICITY, IMMUNOLOGIC; GENETIC VARIATION; HUMANS; IMMUNOLOGIC SURVEILLANCE; INTERLEUKIN-15; PHENOTYPE; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; TISSUE DONORS; TUMOR NECROSIS FACTOR RECEPTOR SUPERFAMILY, MEMBER 7;

EID: 85014429718     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14760     Document Type: Article

References (55)

1. Hayday, A. C. [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu. Rev. Immunol. 18, 975-1026 (2000).
2. Bonneville, M., O'Brien, R. L. & Born, W. K. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10, 467-478 (2010).
3. Chien, Y. H., Meyer, C. & Bonneville, M. gammadelta T cells: first line of defense and beyond. Annu. Rev. Immunol. 32, 121-155 (2014).
4. Gerber, D. J. et al. IL-4-producing gamma delta T cells that express a very restricted TCR repertoire are preferentially localized in liver and spleen. J. Immunol. 163, 3076-3082 (1999).
5. Kashani, E. et al. A clonotypic Vgamma4Jgamma1/Vdelta5Ddelta2Jdelta1 innate gammadelta T-cell population restricted to the CCR6(+)CD27(-) subset. Nat. Commun. 6, 6477 (2015).
6. Sherwood, A. M. et al. Deep sequencing of the human TCRgamma and TCRbeta repertoires suggests that TCRbeta rearranges after alphabeta and gammadelta T cell commitment. Sci. Transl. Med. 3, 90ra61 (2011).
7. Dimova, T. et al. Effector Vgamma9Vdelta2 T cells dominate the human fetal gammadelta T-cell repertoire. Proc. Natl Acad. Sci. USA 112, E556-E565 (2015).
8. Rhodes, D. A., Reith, W. & Trowsdale, J. Regulation of immunity by butyrophilins. Annu. Rev. Immunol. 34, 151-172 (2016).
9. Correia, D. V. et al. Differentiation of human peripheral blood Vdelta1+ T cells expressing the natural cytotoxicity receptor NKp30 for recognition of lymphoid leukemia cells. Blood 118, 992-1001 (2011).
10. Wencker, M. et al. Innate-like T cells straddle innate and adaptive immunity by altering antigen-receptor responsiveness. Nat. Immunol. 15, 80-87 (2014).
11. Couzi, L. et al. Common features of gammadelta T cells and CD8(+) alphabeta T cells responding to human cytomegalovirus infection in kidney transplant recipients. J. Infect. Dis. 200, 1415-1424 (2009).
12. Dechanet, J. et al. Implication of gammadelta T cells in the human immune response to cytomegalovirus. J. Clin. Investig. 103, 1437-1449 (1999).
13. Farnault, L. et al. Clinical evidence implicating gamma-delta T cells in EBV control following cord blood transplantation. Bone Marrow Transplant. 48, 1478-1479 (2013).
14. Fujishima, N. et al. Skewed T cell receptor repertoire of Vdelta1(+) gammadelta T lymphocytes after human allogeneic haematopoietic stem cell transplantation and the potential role for Epstein-Barr virus-infected B cells in clonal restriction. Clin. Exp. Immunol. 149, 70-79 (2007).
15. Halary, F. et al. Shared reactivity of V{delta}2(neg) {gamma}{delta} T cells against cytomegalovirus-infected cells and tumor intestinal epithelial cells. J. Exp. Med. 201, 1567-1578 (2005).
16. Pitard, V. et al. Long-term expansion of effector/memory Vdelta2-gammadelta T cells is a specific blood signature of CMV infection. Blood 112, 1317-1324 (2008).
17. Akbar, A. N. & Fletcher, J. M. Memory T cell homeostasis and senescence during aging. Curr. Opin. Immunol. 17, 480-485 (2005).
18. Khan, N. et al. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J. Immunol. 169, 1984-1992 (2002).
19. Alejenef, A. et al. Cytomegalovirus drives Vdelta2neg gammadelta T cell inflation in many healthy virus carriers with increasing age. Clin. Exp. Immunol. 176, 418-428 (2014).
20. Roux, A. et al. Differential impact of age and cytomegalovirus infection on the gammadelta T cell compartment. J. Immunol. 191, 1300-1306 (2013).
21. Dieli, F. et al. Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J. Exp. Med. 198, 391-397 (2003).
22. Rock, E. P., Sibbald, P. R., Davis, M. M. & Chien, Y. H. CDR3 length in antigenspecific immune receptors. J. Exp. Med. 179, 323-328 (1994).
23. Venturi, V., Price, D. A., Douek, D. C. & Davenport, M. P. The molecular basis for public T-cell responses? Nat. Rev. Immunol. 8, 231-238 (2008).
24. Wang, H., Fang, Z. & Morita, C. T. Vgamma2Vdelta2 T Cell Receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J. Immunol. 184, 6209-6222 (2010).
25. Dellabona, P., Padovan, E., Casorati, G., Brockhaus, M. & Lanzavecchia, A. An invariant V alpha 24-J alpha Q/V beta 11 T cell receptor is expressed in all individuals by clonally expanded CD4-8-T cells. J. Exp. Med. 180, 1171-1176 (1994).
26. Tilloy, F. et al. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J. Exp. Med. 189, 1907-1921 (1999).
27. Hamann, D. et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186, 1407-1418 (1997).
28. Hayday, A. C. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196 (2009).
29. Vantourout, P. & Hayday, A. Six-of-the-best: unique contributions of gammadelta T cells to immunology. Nat. Rev. Immunol. 13, 88-100 (2013).
30. Morita, C. T., Jin, C., Sarikonda, G. & Wang, H. 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 (2007).
31. Gibbons, D. L. et al. Neonates harbour highly active gammadelta T cells with selective impairments in preterm infants. Eur. J. Immunol. 39, 1794-1806 (2009).
32. Ramsburg, E., Tigelaar, R., Craft, J. & Hayday, A. Age-dependent requirement for gammadelta T cells in the primary but not secondary protective immune response against an intestinal parasite. J. Exp. Med. 198, 1403-1414 (2003).
33. Luoma, A. M. et al. Crystal structure of Vdelta1 T cell receptor in complex with CD1d-sulfatide shows MHC-like recognition of a self-lipid by human gammadelta T cells. Immunity 39, 1032-1042 (2013).
34. Sciammas, R. et al. Unique antigen recognition by a herpesvirus-specific TCR-gamma delta cell. J. Immunol. 152, 5392-5397 (1994).
35. Uldrich, A. P. et al. CD1d-lipid antigen recognition by the gammadelta TCR. Nat. Immunol. 14, 1137-1145 (2013).
36. Willcox, C. R. et al. Cytomegalovirus and tumor stress surveillance by binding of a human gammadelta T cell antigen receptor to endothelial protein C receptor. Nat. Immunol. 13, 872-879 (2012).
37. Zeng, X. et al. Gammadelta T cells recognize a microbial encoded B cell antigen to initiate a rapid antigen-specific interleukin-17 response. Immunity 37, 524-534 (2012).
38. Exley, M. A. & Koziel, M. J. To be or not to be NKT: natural killer T cells in the liver. Hepatology 40, 1033-1040 (2004).
39. Vermijlen, D. et al. Human cytomegalovirus elicits fetal gammadelta T cell responses in utero. J. Exp. Med. 207, 807-821 (2010).
40. Lafarge, X. et al. Expression of MHC class I receptors confers functional intraclonal heterogeneity to a reactive expansion of gammadelta T cells. Eur. J. Immunol. 35, 1896-1905 (2005).
41. Bodger, M. P., Janossy, G., Bollum, F. J., Burford, G. D. & Hoffbrand, A. V. The ontogeny of terminal deoxynucleotidyl transferase positive cells in the human fetus. Blood 61, 1125-1131 (1983).
42. Bowie, A. G. & Unterholzner, L. Viral evasion and subversion of patternrecognition receptor signalling. Nat. Rev. Immunol. 8, 911-922 (2008).
43. Fernandez-Messina, L., Reyburn, H. T. & Vales-Gomez, M. Human NKG2Dligands: cell biology strategies to ensure immune recognition. Front. Immunol. 3, 299 (2012).
44. Horst, D., Geerdink, R. J., Gram, A. M., Stoppelenburg, A. J. & Ressing, M. E. Hiding lipid presentation: viral interference with CD1d-restricted invariant natural killer T (iNKT) cell activation. Viruses 4, 2379-2399 (2012).
45. Fernandez, C. S. et al. MAIT cells are depleted early but retain functional cytokine expression in HIV infection. Immunol. Cell Biol. 93, 177-188 (2015).
46. Couzi, L. et al. Cytomegalovirus-induced gammadelta T cells associate with reduced cancer risk after kidney transplantation. J. Am. Soc. Nephrol. 21, 181-188 (2010).
47. Wang, C. et al. High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc. Natl Acad. Sci. USA 107, 1518-1523 (2010).
48. Han, J. et al. Simultaneous amplification and identification of 25 human papillomavirus types with Templex technology. J. Clin. Microbiol. 44, 4157-4162 (2006).
49. Giudicelli, V. & Lefranc, M. P. IMGT/junctionanalysis: IMGT standardized analysis of the V-J and V-D-J junctions of the rearranged immunoglobulins (IG) and T cell receptors (TR). Cold Spring Harb. Protoc. 2011, 716-725 (2011).
50. Yousfi Monod, M., Giudicelli, V., Chaume, D. & Lefranc, M. P. IMGT/ JunctionAnalysis: the first tool for the analysis of the immunoglobulin and T cell receptor complex V-J and V-D-J JUNCTIONs. Bioinformatics 20, i379-i385 (2004).
51. Thomsen, M. C. & Nielsen, M. Seq2Logo: a method for construction and visualization of amino acid binding motifs and sequence profiles including sequence weighting, pseudo counts and two-sided representation of amino acid enrichment and depletion. Nucleic Acids Res. 40, W281-W287 (2012).
52. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
53. Yang, Y. et al. Distinct mechanisms define murine B cell lineage immunoglobulin heavy chain (IgH) repertoires. eLife 4, e09083 (2015).
54. Bolotin, D. A. et al. MiXCR: software for comprehensive adaptive immunity profiling. Nat. Methods 12, 380-381 (2015).
55. Shugay, M. et al. VDJtools: unifying post-analysis of T cell receptor repertoires. PLoS Comput. Biol. 11, e1004503 (2015).