Diversification of the antigen-specific T cell receptor repertoire after varicella zoster vaccination

Science Translational Medicine

Volumn 8, Issue 332, 2016, Pages

  Qi, Qian ^a,b   Cavanagh, Mary M ^a,b   Saux, Sabine Le ^a,b   Namkoong, Hong ^a,b   Kim, Chulwoo ^a,b   Turgano, Emerson ^b   Liu, Yi ^c   Wang, Chen ^a   Mackey, Sally ^a   Swan, Gary E ^a   Dekker, Cornelia L ^a   Olshen, Richard A ^c   Boyd, Scott D ^a   Weyand, Cornelia M ^a,b   Tian, Lu ^c   Goronzy, Jörg J ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; VARICELLA ZOSTER VACCINE; VIRUS ANTIGEN; CHICKENPOX VACCINE; LYMPHOCYTE ANTIGEN RECEPTOR;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL CLONE; CONTROLLED STUDY; GENE; GENETIC REGULATION; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; MONOZYGOTIC TWINS; PRIORITY JOURNAL; TRBJ GENE; TRBV GENE; VIRUS REACTIVATION; CELL PROLIFERATION; CLINICAL TRIAL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; VACCINATION; VARICELLA ZOSTER VIRUS;

ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHICKENPOX VACCINE; CLONE CELLS; HERPESVIRUS 3, HUMAN; HUMANS; IMMUNOLOGIC MEMORY; RECEPTORS, ANTIGEN, T-CELL; VACCINATION;

EID: 84962626942     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaf1725     Document Type: Article

References (41)

1. K. Haberthur, F. Engelmann, B. Park, A. Barron, A. Legasse, J. Dewane, M. Fischer, A. Kerns, M. Brown, I. Messaoudi, CD4 T cell immunity is critical for the control of simian varicella virus infection in a nonhuman primate model of VZV infection. PLOS Pathog. 7, e1002367 (2011).
2. J. G. Donahue, P. W. Choo, J. E. Manson, R. Platt, The incidence of herpes zoster. Arch. Intern. Med. 155, 1605-1609 (1995).
3. R. A. Seder, P. A. Darrah, M. Roederer, T-cell quality in memory and protection: Implications for vaccine design. Nat. Rev. Immunol. 8, 247-258 (2008).
4. I. Messaoudi, J. A. Guevara Patiño, R. Dyall, J. LeMaoult, J. Nikolich-Žugich, Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 298, 1797-1800 (2002).
5. J. J. Goronzy, Q. Qi, R. A. Olshen, C. M. Weyand, High-throughput sequencing insights into T-cell receptor repertoire diversity in aging. Genome Med. 7, 117 (2015).
6. G. Georgiou, G. C. Ippolito, J. Beausang, C. E. Busse, H. Wardemann, S. R. Quake, The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat. Biotechnol. 32, 158-168 (2014).
7. Q. Qi, Y. Liu, Y. Cheng, J. Glanville, D. Zhang, J.-Y. Lee, R. A. Olshen, C. M. Weyand, S. D. Boyd, J. J. Goronzy, Diversity and clonal selection in the human T-cell repertoire. Proc. Natl. Acad. Sci. U. S. A. 111, 13139-13144 (2014).
8. J. I. Cohen, The varicella-zoster virus genome. Curr. Top. Microbiol. Immunol. 342, 1-14 (2010).
9. W. J. D. Ouwendijk, K. J. Laing, G. M. G. M. Verjans, D. M. Koelle, T-cell immunity to human alphaherpesviruses. Curr. Opin. Virol. 3, 452-460 (2013).
10. + T cells responsive to varicella zoster virus. J. Infect. Dis. 212, 1022-1031 (2015).
11. H. Lal, A. L. Cunningham, O. Godeaux, R. Chlibek, J. Diez-Domingo, S.-J. Hwang, M. J. Levin, J. E. McElhaney, A. Poder, J. Puig-Barberà, T. Vesikari, D. Watanabe, L. Weckx, T. Zahaf, T. C. Heineman; ZOE-50 Study Group, Efficacy of an adjuvanted herpes zoster subunit vaccine in older adults. N. Engl. J. Med. 372, 2087-2096 (2015).
12. + T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27, 203-213 (2007).
13. D. A. Price, S. M. West, M. R. Betts, L. E. Ruff, J. M. Brenchley, D. R. Ambrozak, Y. Edghill-Smith, M. J. Kuroda, D. Bogdan, K. Kunstman, N. L. Letvin, G. Franchini, S. M. Wolinsky, R. A. Koup, D. C. Douek, T cell receptor recognition motifs govern immune escape patterns in acute SIV infection. Immunity 21, 793-803 (2004).
14. E. Cha, M. Klinger, Y. Hou, C. Cummings, A. Ribas, M. Faham, L. Fong, Improved survival with T cell clonotype stability after anti-CTLA-4 treatment in cancer patients. Sci. Transl. Med. 6, 238ra70 (2014).
15. R. M. Welsh, J. W. Che, M. A. Brehm, L. K. Selin, Heterologous immunity between viruses. Immunol. Rev. 235, 244-266 (2010).
16. C. Chiu, M. McCausland, J. Sidney, F.-M. Duh, N. Rouphael, A. Mehta, M. Mulligan, M. Carrington, A. Wieland, N. L. Sullivan, A. Weinberg, M. J. Levin, B. Pulendran, B. Peters, A. Sette, R. Ahmed, Broadly reactive human CD8 T cells that recognize an epitope conserved between VZV, HSV and EBV. PLOS Pathog. 10, e1004008 (2014).
17. G. C. Wang, P. Dash, J. A. McCullers, P. C. Doherty, P. G. Thomas, T cell receptor ab diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci. Transl. Med. 4, 128ra42 (2012).
18. N. L. La Gruta, P. G. Thomas, Interrogating the relationship between naïve and immune antiviral T cell repertoires. Curr. Opin. Virol. 3, 447-451 (2013).
19. + T-cell clones following secondary acute virus infection. Proc. Natl. Acad. Sci. U. S. A. 111, 1485-1490 (2014).
20. A. Gil, M. B. Yassai, Y. N. Naumov, L. K. Selin, Narrowing of human influenza A virus-specific T cell receptor a and b repertoires with increasing age. J. Virol. 89, 4102-4116 (2015).
21. A. Hata, H. Asanuma, M. Rinki, M. Sharp, R. M. Wong, K. Blume, A. M. Arvin, Use of an inactivated varicella vaccine in recipients of hematopoietic-cell transplants. N. Engl. J. Med. 347, 26-34 (2002).
22. M. J. Levin, M. N. Oxman, J. H. Zhang, G. R. Johnson, H. Stanley, A. R. Hayward, M. J. Caulfield, M. R. Irwin, J. G. Smith, J. Clair, I. S. F. Chan, H. Williams, R. Harbecke, R. Marchese, S. E. Straus, A. Gershon, A. Weinberg; Veterans Affairs Cooperative Studies Program Shingles Prevention Study Investigators, Varicella-zoster virus-specific immune responses in elderly recipients of a herpes zoster vaccine. J. Infect. Dis. 197, 825-835 (2008).
23. J. N. Vermeulen, J. M. A. Lange, S. K. Tyring, P. H. Peters, M. Nunez, G. Poland, M. J. Levin, C. Freeman, I. Chalikonda, J. Li, J. G. Smith, M. J. Caulfield, J. E. Stek, I. S. F. Chan, R. Vessey, F. P. Schödel, P. W. Annunziato, K. Schlienger, J. L. Silber, Safety, tolerability, and immunogenicity after 1 and 2 doses of zoster vaccine in healthy adults ≥60 years of age. Vaccine 30, 904-910 (2012).
24. I. V. Zvyagin, M. V. Pogorelyy, M. E. Ivanova, E. A. Komech, M. Shugay, D. A. Bolotin, A. A. Shelenkov, A. A. Kurnosov, D. B. Staroverov, D. M. Chudakov, Y. B. Lebedev, I. Z. Mamedov, Distinctive properties of identical twins' TCR repertoires revealed by high-throughput sequencing. Proc. Natl. Acad. Sci. U. S. A. 111, 5980-5985 (2014).
25. C. Wang, Y. Liu, M. M. Cavanagh, S. Le Saux, Q. Qi, K. M. Roskin, T. J. Looney, J.-Y. Lee, V. Dixit, C. L. Dekker, G. E. Swan, J. J. Goronzy, S. D. Boyd, B-cell repertoire responses to varicellazoster vaccination in human identical twins. Proc. Natl. Acad. Sci. U. S. A. 112, 500-505 (2015).
26. R. Geiger, T. Duhen, A. Lanzavecchia, F. Sallusto, Human naive and memory CD4+ T cell repertoires specific for naturally processed antigens analyzed using libraries of amplified T cells. J. Exp. Med. 206, 1525-1534 (2009).
27. J. D. Ahlers, I. M. Belyakov, Memories that last forever: Strategies for optimizing vaccine T-cell memory. Blood 115, 1678-1689 (2010).
28. D. A. Price, T. E. Asher, N. A. Wilson, M. C. Nason, J. M. Brenchley, I. S. Metzler, V. Venturi, E. Gostick, P. K. Chattopadhyay, M. Roederer, M. P. Davenport, D. I. Watkins, D. C. Douek, Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J. Exp. Med. 206, 923-936 (2009).
29. + T cells in response to infection is markedly efficient. Science 325, 1265-1269 (2009).
30. + T cell populations specific for persistent DNA viruses. J. Exp. Med. 202, 1349-1361 (2005).
31. H. F. Tseng, N. Smith, R. Harpaz, S. R. Bialek, L. S. Sy, S. J. Jacobsen, Herpes zoster vaccine in older adults and the risk of subsequent herpes zoster disease. JAMA 305, 160-166 (2011).
32. E. J. Wherry, T cell exhaustion. Nat. Immunol. 12, 492-499 (2011).
33. + T cells specific for immediate-early 63 protein of varicella-zoster virus. Eur. J. Immunol. 37, 3393-3403 (2007).
34. W. J. Ouwendijk, A. Geluk, S. L. Smits, S. Getu, A. D. M. E. Osterhaus, G. M. G. M. Verjans, Functional characterization of ocular-derived human alphaherpesvirus cross-reactive CD4 T cells. J. Immunol. 192, 3730-3739 (2014).
35. J. C. Nolz, D. Rai, V. P. Badovinac, J. T. Harty, Division-linked generation of death-intermediates regulates the numerical stability of memory CD8 T cells. Proc. Natl. Acad. Sci. U. S. A. 109, 6199-6204 (2012).
36. T. Dong, G. Stewart-Jones, N. Chen, P. Easterbrook, X. Xu, L. Papagno, V. Appay, M. Weekes, C. Conlon, C. Spina, S. Little, G. Screaton, A. Van Der Merwe, D. D. Richman, A. J. McMichael, E. Y. Jones, S. L. Rowland-Jones, HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J. Exp. Med. 200, 1547-1557 (2004).
37. H. Chen, Z. M. Ndhlovu, D. Liu, L. C. Porter, J. W. Fang, S. Darko, M. A. Brockman, T. Miura, Z. L. Brumme, A. Schneidewind, A. Piechocka-Trocha, K. T. Cesa, J. Sela, T. D. Cung, I. Toth, F. Pereyra, X. G. Yu, D. C. Douek, D. E. Kaufmann, T. M. Allen, B. D. Walker, TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 13, 691-700 (2012).
38. V. Vezys, D. Masopust, C. C. Kemball, D. L. Barber, L. A. O'Mara, C. P. Larsen, T. C. Pearson, R. Ahmed, A. E. Lukacher, Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203, 2263-2269 (2006).
39. T. Argaw, J. I. Cohen, M. Klutch, K. Lekstrom, T. Yoshikawa, Y. Asano, P. R. Krause, Nucleotide sequences that distinguish Oka vaccine from parental Oka and other varicella-zoster virus isolates. J. Infect. Dis. 181, 1153-1157 (2000).
40. Y. Gomi, H. Sunamachi, Y. Mori, K. Nagaike, M. Takahashi, K. Yamanishi, Comparison of the complete DNA sequences of the Oka varicella vaccine and its parental virus. J. Virol. 76, 11447-11459 (2002).
41. R. E. Krasnow, L. M. Jack, C. N. Lessov-Schlaggar, A. W. Bergen, G. E. Swan, The Twin Research Registry at SRI International. Twin Res. Hum. Genet. 16, 463-470 (2013).