The neonatal CD8+ T cell repertoire rapidly diversifies during persistent viral infection

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1604-1616

  Venturi, Vanessa ^a   Nzingha, Kito ^b   Amos, Timothy G ^a   Charles, Wisler C ^b   Dekhtiarenko, Iryna ^c   Cicin Sain, Luka ^c,d   Davenport, Miles P ^a   Rudd, Brian D ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b Department of Obstetrics Gynecology   (United States)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL; BRAIN; C57BL MOUSE; CD8+ T LYMPHOCYTE; CYTOLOGY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; NEWBORN; SPLEEN; T LYMPHOCYTE RECEPTOR GENE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; GENES, T-CELL RECEPTOR; IMMUNOLOGIC MEMORY; MICE, INBRED C57BL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; SPLEEN;

EID: 84958581057     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501867     Document Type: Article

References (46)

1. Cheeran, M. C., J. R. Lokensgard, and M. R. Schleiss. 2009. Neuropathogenesis of congenital cytomegalovirus infection: disease mechanisms and prospects for intervention. Clin. Microbiol. Rev. 22: 99-126 (Table of Contents).
2. Adler, S. P., G. Nigro, and L. Pereira. 2007. Recent advances in the prevention and treatment of congenital cytomegalovirus infections. Semin. Perinatol. 31: 10-18.
3. Nigro, G., S. P. Adler, R. La Torre, and A. M. Best, Congenital Cytomegalovirus Collaborating Group. 2005. Passive immunization during pregnancy for congenital cytomegalovirus infection. N. Engl. J. Med. 353: 1350-1362.
4. Pass, R. F. 2005. Congenital cytomegalovirus infection and hearing loss. Herpes 12: 50-55.
5. Pass, R. F., K. B. Fowler, S. B. Boppana, W. J. Britt, and S. Stagno. 2006. Congenital cytomegalovirus infection following first trimester maternal infection: symptoms at birth and outcome. J. Clin. Virol. 35: 216-220.
6. Huang, E. S., C. A. Alford, D. W. Reynolds, S. Stagno, and R. F. Pass. 1980. Molecular epidemiology of cytomegalovirus infections in women and their infants. N. Engl. J. Med. 303: 958-962.
7. Noyola, D. E., G. J. Demmler, W. D. Williamson, C. Griesser, S. Sellers, A. Llorente, T. Littman, S.Williams, L. Jarrett, and M. D. Yow, Congenital CMV Longitudinal Study Group. 2000. Cytomegalovirus urinary excretion and long term outcome in children with congenital cytomegalovirus infection. Pediatr. Infect. Dis. J. 19: 505-510.
8. Bantug, G. R., D. Cekinovic, R. Bradford, T. Koontz, S. Jonjic, and W. J. Britt. 2008. CD8+ T lymphocytes control murine cytomegalovirus replication in the central nervous system of newborn animals. J. Immunol. 181: 2111-2123.
9. Pass, R. F., S. Stagno, W. J. Britt, and C. A. Alford. 1983. Specific cell-mediated immunity and the natural history of congenital infection with cytomegalovirus. J. Infect. Dis. 148: 953-961.
10. Reusser, P., S. R. Riddell, J. D. Meyers, and P. D. Greenberg. 1991. Cytotoxic Tlymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: pattern of recovery and correlation with cytomegalovirus infection and disease. Blood 78: 1373-1380.
11. Nikolich-Zugich, J., D. H. Fremont, M. J. Miley, and I. Messaoudi. 2004. The role of mhc polymorphism in anti-microbial resistance. Microbes Infect. 6: 501-512.
12. Nikolich-Zugich, J., M. K. Slifka, and I. Messaoudi. 2004. The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 4: 123-132.
13. Rudd, B. D., V. Venturi, M. P. Davenport, and J. Nikolich-Zugich. 2011. Evolution of the antigen-specific CD8+ TCR repertoire across the life span: evidence for clonal homogenization of the old TCR repertoire. J. Immunol. 186: 2056-2064.
14. Zemlin, M., R. L. Schelonka, K. Bauer, and H. W. Schroeder, Jr. 2002. Regulation and chance in the ontogeny of B and T cell antigen receptor repertoires. Immunol. Res. 26: 265-278.
15. Feeney, A. J. 1991. Junctional sequences of fetal T cell receptor beta chains have few N regions. J. Exp. Med. 174: 115-124.
16. Bogue, M., S. Candéias, C. Benoist, and D. Mathis. 1991. A special repertoire of alpha:beta T cells in neonatal mice. EMBO J. 10: 3647-3654.
17. Cabaniols, J. P., N. Fazilleau, A. Casrouge, P. Kourilsky, and J. M. Kanellopoulos. 2001. Most alpha/beta T cell receptor diversity is due to terminal deoxynucleotidyl transferase. J. Exp. Med. 194: 1385-1390.
18. Rudd, B. D., V. Venturi, N. L. Smith, K. Nzingha, E. L. Goldberg, G. Li, J. Nikolich-Zugich, and M. P. Davenport. 2013. Acute neonatal infections 'lockin' a suboptimal CD8+ T cell repertoire with impaired recall responses. PLoS Pathog. 9: e1003572.
19. Hogan, R. J., E. J. Usherwood, W. Zhong, A. A. Roberts, R. W. Dutton, A. G. Harmsen, and D. L. Woodland. 2001. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166: 1813-1822.
20. Hawke, S., P. G. Stevenson, S. Freeman, and C. R. Bangham. 1998. Long-term persistence of activated cytotoxic T lymphocytes after viral infection of the central nervous system. J. Exp. Med. 187: 1575-1582.
21. Masopust, D., V. Vezys, E. J. Usherwood, L. S. Cauley, S. Olson, A. L. Marzo, R. L. Ward, D. L. Woodland, and L. Lefrançois. 2004. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J. Immunol. 172: 4875-4882.
22. Gebhardt, T., L. M. Wakim, L. Eidsmo, P. C. Reading, W. R. Heath, and F. R. Carbone. 2009. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10: 524-530.
23. Gebhardt, T., L. M. Wakim, L. Eidsmo, P. C. Reading, W. R. Heath, and F. R. Carbone. 2009. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10: 524-530.
24. Gebhardt, T., P. G. Whitney, A. Zaid, L. K. Mackay, A. G. Brooks, W. R. Heath, F. R. Carbone, and S. N. Mueller. 2011. Different patterns of peripheral migration by memory CD4(+) and CD8(+) T cells. Nature 477: 216-219.
25. Wakim, L. M., T. Gebhardt, W. R. Heath, and F. R. Carbone. 2008. Cutting edge: local recall responses by memory T cells newly recruited to peripheral nonlymphoid tissues. J. Immunol. 181: 5837-5841.
26. Wakim, L. M., A. Woodward-Davis, and M. J. Bevan. 2010. Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc. Natl. Acad. Sci. USA 107: 17872-17879.
27. Dekhtiarenko, I., M. A. Jarvis, Z. Ruzsics, and L. Cicin-Sain. 2013. The context of gene expression defines the immunodominance hierarchy of cytomegalovirus antigens. J. Immunol. 190: 3399-3409.
28. Dash, P., J. L. McClaren, T. H. Oguin, III, W. Rothwell, B. Todd, M. Y. Morris, J. Becksfort, C. Reynolds, S. A. Brown, P. C. Doherty, and P. G. Thomas. 2011. Paired analysis of TCRa and TCRb chains at the single-cell level in mice. J. Clin. Invest. 121: 288-295.
29. Rudd, B. D., V. Venturi, M. J. Smithey, S. S. Way, M. P. Davenport, and J. Nikolich-Zugich. 2010. Diversity of the CD8+ T cell repertoire elicited against an immunodominant epitope does not depend on the context of infection. J. Immunol. 184: 2958-2965.
30. Lefranc, M. P., V. Giudicelli, C. Ginestoux, J. Bodmer, W. Muller, R. Bontrop, M. Lemaitre, A. Malik, V. Barbié, and D. Chaume. 1999. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 27: 209-212.
31. Venturi, V., K. Kedzierska, S. J. Turner, P. C. Doherty, and M. P. Davenport. 2007. Methods for comparing the diversity of samples of the T cell receptor repertoire. J. Immunol. Methods 321: 182-195.
32. Venturi, V., K. Kedzierska, M. M. Tanaka, S. J. Turner, P. C. Doherty, and M. P. Davenport. 2008. Method for assessing the similarity between subsets of the T cell receptor repertoire. J. Immunol. Methods 329: 67-80.
33. Munks, M. W., K. S. Cho, A. K. Pinto, S. Sierro, P. Klenerman, and A. B. Hill. 2006. Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J. Immunol. 177: 450-458.
34. Munks, M. W., M. C. Gold, A. L. Zajac, C. M. Doom, C. S. Morello, D. H. Spector, and A. B. Hill. 2006. Genome-wide analysis reveals a highly diverse CD8 T cell response to murine cytomegalovirus. J. Immunol. 176: 3760-3766.
35. Koontz, T., M. Bralic, J. Tomac, E. Pernjak-Pugel, G. Bantug, S. Jonjic, and W. J. Britt. 2008. Altered development of the brain after focal herpesvirus infection of the central nervous system. J. Exp. Med. 205: 423-435.
36. Smith, C. J., H. Turula, and C. M. Snyder. 2014. Systemic hematogenous maintenance of memory inflation by MCMV infection. PLoS Pathog. 10: e1004233.
37. Farrington, L. A., T. A. Smith, F. Grey, A. B. Hill, and C. M. Snyder. 2013. Competition for antigen at the level of the APC is a major determinant of immunodominance during memory inflation in murine cytomegalovirus infection. J. Immunol. 190: 3410-3416.
38. Gebhardt, T., S. N. Mueller, W. R. Heath, and F. R. Carbone. 2013. Peripheral tissue surveillance and residency by memory T cells. Trends Immunol. 34: 27-32.
39. Price, D. A., J. M. Brenchley, L. E. Ruff, M. R. Betts, B. J. Hill, M. Roederer, R. A. Koup, S. A. Migueles, E. Gostick, L. Wooldridge, et al. 2005. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
40. 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 highaffinity clones into memory following primary infection with a persistent human virus: human cytomegalovirus. J. Immunol. 179: 3203-3213.
41. Messaoudi, I., J. A. Guevara Patinõ, R. Dyall, J. LeMaoult, and J. Nikolich-Zugich. 2002. Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 298: 1797-1800.
42. Meyer-Olson, D., N. H. Shoukry, K. W. Brady, H. Kim, D. P. Olson, K. Hartman, A. K. Shintani, C. M. Walker, and S. A. Kalams. 2004. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J. Exp. Med. 200: 307-319.
43. Selin, L. K., S. M. Varga, I. C. Wong, and R. M. Welsh. 1998. Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations. J. Exp. Med. 188: 1705-1715.
44. Turner, S. J., N. L. La Gruta, K. Kedzierska, P. G. Thomas, and P. C. Doherty. 2009. Functional implications of T cell receptor diversity. Curr. Opin. Immunol. 21: 286-290.
45. Snyder, C. M., K. S. Cho, E. L. Bonnett, S. van Dommelen, G. R. Shellam, and A. B. Hill. 2008. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29: 650-659.
46. Anderson, K. G., H. Sung, C. N. Skon, L. Lefrancois, A. Deisinger, V. Vezys, and D. Masopust. 2012. Cutting edge: intravascular staining redefines lung CD8 T cell responses. J. Immunol. 189: 2702-2706.