System-wide Analysis of the T Cell Response

Cell Reports

Volumn 14, Issue 11, 2016, Pages 2733-2744

  Covacu, Ruxandra ^a   Philip, Hagit ^b   Jaronen, Merja ^a   Almeida, Jorge ^c   Kenison, Jessica E ^a   Darko, Samuel ^c   Chao, Chun Cheih ^a   Yaari, Gur ^b   Louzoun, Yoram ^b   Carmel, Liran ^d   Douek, Daniel C ^c   Efroni, Sol ^b   Quintana, Francisco J ^a,e  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BAR ILAN UNIVERSITY   (Israel)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; T LYMPHOCYTE RECEPTOR BETA1; UNCLASSIFIED DRUG; ANTIGEN; CALMODULIN; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA; ZEBRAFISH PROTEIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; IMMUNE RESPONSE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; T LYMPHOCYTE; ZEBRA FISH; ANIMAL; DNA SEQUENCE; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM;

ANIMALS; ANTIGENS; CALMODULIN; MALE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; T-LYMPHOCYTES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84959863408     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.02.056     Document Type: Article

References (62)

1. Akira S., Okazaki K., Sakano H. Two pairs of recombination signals are sufficient to cause immunoglobulin V-(D)-J joining. Science 1987, 238:1134-1138.
2. Argaet V.P., Schmidt C.W., Burrows S.R., Silins S.L., Kurilla M.G., Doolan D.L., Suhrbier A., Moss D.J., Kieff E., Sculley T.B., Misko I.S. Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus. J. Exp. Med. 1994, 180:2335-2340.
3. Arstila T.P., Casrouge A., Baron V., Even J., Kanellopoulos J., Kourilsky P. A direct estimate of the human alphabeta T cell receptor diversity. Science 1999, 286:958-961.
4. Benichou J., Ben-Hamo R., Louzoun Y., Efroni S. Rep-Seq: uncovering the immunological repertoire through next-generation sequencing. Immunology 2012, 135:183-191.
5. Birnbaum M.E., Mendoza J.L., Sethi D.K., Dong S., Glanville J., Dobbins J., Ozkan E., Davis M.M., Wucherpfennig K.W., Garcia K.C. Deconstructing the peptide-MHC specificity of T cell recognition. Cell 2014, 157:1073-1087.
6. Boehm T., Iwanami N., Hess I. Evolution of the immune system in the lower vertebrates. Annu. Rev. Genomics Hum. Genet. 2012, 13:127-149.
7. Boyd S.D., Marshall E.L., Merker J.D., Maniar J.M., Zhang L.N., Sahaf B., Jones C.D., Simen B.B., Hanczaruk B., Nguyen K.D., et al. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med. 2009, 1:12ra23.
8. Burzyn D., Benoist C., Mathis D. Regulatory T cells in nonlymphoid tissues. Nat. Immunol. 2013, 14:1007-1013.
9. Casrouge A., Beaudoing E., Dalle S., Pannetier C., Kanellopoulos J., Kourilsky P. Size estimate of the alpha beta TCR repertoire of naive mouse splenocytes. J. Immunol. 2000, 164:5782-5787.
10. Chen H., Ndhlovu Z.M., Liu D., Porter L.C., Fang J.W., Darko S., Brockman M.A., Miura T., Brumme Z.L., Schneidewind A., et al. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 2012, 13:691-700.
11. Cibotti R., Cabaniols J.P., Pannetier C., Delarbre C., Vergnon I., Kanellopoulos J.M., Kourilsky P. Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice. J. Exp. Med. 1994, 180:861-872.
12. Cooper M.D., Herrin B.R. How did our complex immune system evolve?. Nat. Rev. Immunol. 2010, 10:2-3.
13. Davis M.M., Bjorkman P.J. T-cell antigen receptor genes and T-cell recognition. Nature 1988, 334:395-402.
14. Douek D.C., Betts M.R., Brenchley J.M., Hill B.J., Ambrozak D.R., Ngai K.L., Karandikar N.J., Casazza J.P., Koup R.A. A novel approach to the analysis of specificity, clonality, and frequency of HIV-specific T cell responses reveals a potential mechanism for control of viral escape. J. Immunol 2002, 168:3099-3104.
15. Efron B., Thisted R. Estimating the number of unseen species: How many words did Shakespeare know?. Biometrika 1976, 63:435-447.
16. Fisher R.A., Corbet A.S., Williams C.B. The relation between the number of species and the number of individuals in a random sample of an animal population. J. Anim. Ecol. 1943, 12:42-58.
17. Flajnik M.F., Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 2010, 11:47-59.
18. Freeman J.D., Warren R.L., Webb J.R., Nelson B.H., Holt R.A. Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res. 2009, 19:1817-1824.
19. Fujimoto S., Yamagishi H. Isolation of an excision product of T-cell receptor alpha-chain gene rearrangements. Nature 1987, 327:242-243.
20. Fulton R.B., Hamilton S.E., Xing Y., Best J.A., Goldrath A.W., Hogquist K.A., Jameson S.C. The TCR's sensitivity to self peptide-MHC dictates the ability of naive CD8(+) T cells to respond to foreign antigens. Nat. Immunol. 2015, 16:107-117.
21. Guo P., Hirano M., Herrin B.R., Li J., Yu C., Sadlonova A., Cooper M.D. Dual nature of the adaptive immune system in lampreys. Nature 2009, 459:796-801.
22. Haire R.N., Rast J.P., Litman R.T., Litman G.W. Characterization of three isotypes of immunoglobulin light chains and T-cell antigen receptor alpha in zebrafish. Immunogenetics 2000, 51:915-923.
23. Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013, 496:498-503.
24. Ishizuka J., Stewart-Jones G.B., van der Merwe A., Bell J.I., McMichael A.J., Jones E.Y. The structural dynamics and energetics of an immunodominant T cell receptor are programmed by its Vbeta domain. Immunity 2008, 28:171-182.
25. Jiang N., Weinstein J.A., Penland L., White R.A., Fisher D.S., Quake S.R. Determinism and stochasticity during maturation of the zebrafish antibody repertoire. Proc. Natl. Acad. Sci. USA 2011, 108:5348-5353.
26. Kettleborough R.N., Busch-Nentwich E.M., Harvey S.A., Dooley C.M., de Bruijn E., van Eeden F., Sealy I., White R.J., Herd C., Nijman I.J., et al. A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 2013, 496:494-497.
27. Kosmrlj A., Read E.L., Qi Y., Allen T.M., Altfeld M., Deeks S.G., Pereyra F., Carrington M., Walker B.D., Chakraborty A.K. Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 2010, 465:350-354.
28. Krogsgaard M., Li Q.J., Sumen C., Huppa J.B., Huse M., Davis M.M. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 2005, 434:238-243.
29. Li H., Ye C., Ji G., Wu X., Xiang Z., Li Y., Cao Y., Liu X., Douek D.C., Price D.A., Han J. Recombinatorial biases and convergent recombination determine interindividual TCRbeta sharing in murine thymocytes. J. Immunol. 2012, 189:2404-2413.
30. Lieschke G.J., Trede N.S. Fish immunology. Curr. Biol. 2009, 19:R678-R682.
31. Linnemann C., Heemskerk B., Kvistborg P., Kluin R.J., Bolotin D.A., Chen X., Bresser K., Nieuwland M., Schotte R., Michels S., et al. High-throughput identification of antigen-specific TCRs by TCR gene capture. Nat. Med. 2013, 19:1534-1541.
32. Malissen M., McCoy C., Blanc D., Trucy J., Devaux C., Schmitt-Verhulst A.M., Fitch F., Hood L., Malissen B. Direct evidence for chromosomal inversion during T-cell receptor beta-gene rearrangements. Nature 1986, 319:28-33.
33. Mandl J.N., Monteiro J.P., Vrisekoop N., Germain R.N. T cell-positive selection uses self-ligand binding strength to optimize repertoire recognition of foreign antigens. Immunity 2013, 38:263-274.
34. McBerry C., Gonzalez R.M., Shryock N., Dias A., Aliberti J. SOCS2-induced proteasome-dependent TRAF6 degradation: a common anti-inflammatory pathway for control of innate immune responses. PLoS ONE 2012, 7:e38384.
35. Meeker N.D., Smith A.C., Frazer J.K., Bradley D.F., Rudner L.A., Love C., Trede N.S. Characterization of the zebrafish T cell receptor beta locus. Immunogenetics 2010, 62:23-29.
36. Miles J.J., Bulek A.M., Cole D.K., Gostick E., Schauenburg A.J., Dolton G., Venturi V., Davenport M.P., Tan M.P., Burrows S.R., et al. Genetic and structural basis for selection of a ubiquitous T cell receptor deployed in Epstein-Barr virus infection. PLoS Pathog. 2010, 6:e1001198.
37. Miles J.J., Douek D.C., Price D.A. Bias in the αβ T-cell repertoire: implications for disease pathogenesis and vaccination. Immunol. Cell Biol. 2011, 89:375-387.
38. Moss P.A., Moots R.J., Rosenberg W.M., Rowland-Jones S.J., Bodmer H.C., McMichael A.J., Bell J.I. Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. USA 1991, 88:8987-8990.
39. Newell E.W., Davis M.M. Beyond model antigens: high-dimensional methods for the analysis of antigen-specific T cells. Nat. Biotechnol. 2014, 32:149-157.
40. Nikolich-Zugich J., Slifka M.K., Messaoudi I. The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 2004, 4:123-132.
41. Okazaki K., Davis D.D., Sakano H. T cell receptor beta gene sequences in the circular DNA of thymocyte nuclei: direct evidence for intramolecular DNA deletion in V-D-J joining. Cell 1987, 49:477-485.
42. Padovan E., Casorati G., Dellabona P., Meyer S., Brockhaus M., Lanzavecchia A. Expression of two T cell receptor alpha chains: dual receptor T cells. Science 1993, 262:422-424.
43. Park C.O., Kupper T.S. The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat. Med. 2015, 21:688-697.
44. Quigley M.F., Greenaway H.Y., Venturi V., Lindsay R., Quinn K.M., Seder R.A., Douek D.C., Davenport M.P., Price D.A. Convergent recombination shapes the clonotypic landscape of the naive T-cell repertoire. Proc. Natl. Acad. Sci. USA 2010, 107:19414-19419.
45. Quintana F.J., Iglesias A.H., Farez M.F., Caccamo M., Burns E.J., Kassam N., Oukka M., Weiner H.L. Adaptive autoimmunity and Foxp3-based immunoregulation in zebrafish. PLoS ONE 2010, 5:e9478.
46. Robins H.S., Campregher P.V., Srivastava S.K., Wacher A., Turtle C.J., Kahsai O., Riddell S.R., Warren E.H., Carlson C.S. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 2009, 114:4099-4107.
47. Rudolph M.G., Stanfield R.L., Wilson I.A. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 2006, 24:419-466.
48. Stefanová I., Dorfman J.R., Germain R.N. Self-recognition promotes the foreign antigen sensitivity of naive T lymphocytes. Nature 2002, 420:429-434.
49. Tonegawa S. Somatic generation of antibody diversity. Nature 1983, 302:575-581.
50. Trede N.S., Langenau D.M., Traver D., Look A.T., Zon L.I. The use of zebrafish to understand immunity. Immunity 2004, 20:367-379.
51. Tubo N.J., Pagán A.J., Taylor J.J., Nelson R.W., Linehan J.L., Ertelt J.M., Huseby E.S., Way S.S., Jenkins M.K. Single naive CD4+ T cells from a diverse repertoire produce different effector cell types during infection. Cell 2013, 153:785-796.
52. Turner S.J., Doherty P.C., McCluskey J., Rossjohn J. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 2006, 6:883-894.
53. Turner S.J., La Gruta N.L., Kedzierska K., Thomas P.G., Doherty P.C. Functional implications of T cell receptor diversity. Curr. Opin. Immunol. 2009, 21:286-290.
54. Venturi V., Kedzierska K., Price D.A., Doherty P.C., Douek D.C., Turner S.J., Davenport M.P. Sharing of T cell receptors in antigen-specific responses is driven by convergent recombination. Proc. Natl. Acad. Sci. USA 2006, 103:18691-18696.
55. Venturi V., Price D.A., Douek D.C., Davenport M.P. The molecular basis for public T-cell responses?. Nat. Rev. Immunol. 2008, 8:231-238.
56. Vermijlen D., Brouwer M., Donner C., Liesnard C., Tackoen M., Van Rysselberge M., Twité N., Goldman M., Marchant A., Willems F. Human cytomegalovirus elicits fetal gammadelta T cell responses in utero. J. Exp. Med. 2010, 207:807-821.
57. Wang C., Sanders C.M., Yang Q., Schroeder H.W., Wang E., Babrzadeh F., Gharizadeh B., Myers R.M., Hudson J.R., Davis R.W., Han J. High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc. Natl. Acad. Sci. USA 2010, 107:1518-1523.
58. Weinstein J.A., Jiang N., White R.A., Fisher D.S., Quake S.R. High-throughput sequencing of the zebrafish antibody repertoire. Science 2009, 324:807-810.
59. Yager E.J., Ahmed M., Lanzer K., Randall T.D., Woodland D.L., Blackman M.A. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 2008, 205:711-723.
60. Yancopoulos G.D., Blackwell T.K., Suh H., Hood L., Alt F.W. Introduced T cell receptor variable region gene segments recombine in pre-B cells: evidence that B and T cells use a common recombinase. Cell 1986, 44:251-259.
61. Yu W., Jiang N., Ebert P.J., Kidd B.A., Müller S., Lund P.J., Juang J., Adachi K., Tse T., Birnbaum M.E., et al. Clonal deletion prunes but does not eliminate self-specific αβ CD8(+) T lymphocytes. Immunity 2015, 42:929-941.
62. Zhu J., Peng T., Johnston C., Phasouk K., Kask A.S., Klock A., Jin L., Diem K., Koelle D.M., Wald A., et al. Immune surveillance by CD8αα+ skin-resident T cells in human herpes virus infection. Nature 2013, 497:494-497.