Evolution of T Cell Responses during Measles Virus Infection and RNA Clearance

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Nelson, Ashley N ^a   Putnam, Nicole ^a,b   Hauer, Debra ^a   Baxter, Victoria K ^a,c   Adams, Robert J ^a   Griffin, Diane E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; RETINOID RELATED ORPHAN RECEPTOR GAMMA; T LYMPHOCYTE RECEPTOR; VIRUS RNA;

ANIMAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LINE; EVOLUTION; GENE EXPRESSION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LEUKOCYTE COUNT; MALE; MEASLES; MEASLES VIRUS; METABOLISM; RHESUS MONKEY; T LYMPHOCYTE; VIREMIA; VIROLOGY; VIRUS LOAD; VIRUS SHEDDING;

ANIMALS; BIOLOGICAL EVOLUTION; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CYTOKINES; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; LEUKOCYTE COUNT; MACACA MULATTA; MALE; MEASLES; MEASLES VIRUS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; RNA, VIRAL; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES; VIRAL LOAD; VIREMIA; VIRUS SHEDDING;

EID: 85029322913     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-10965-z     Document Type: Article

References (54)

1. Moss, W. J. & Griffin, D. E. Measles. Lancet 379, 153-164, doi: 10.1016/S0140-6736(10)62352-5 (2012).
2. Beckford, A. P., Kaschula, R. O. & Stephen, C. Factors associated with fatal cases of measles. A retrospective autopsy study. South Afr. Med. J. 68, 858-863 (1985).
3. Miller, D. L. Frequency of complications of measles, 1963. Brit. Med. J. 2, 75-78 (1964).
4. Polack, F. P. et al. Production of atypical measles in rhesus macaques: evidence for disease mediated by immune complex formation and eosinophils in the presence of fusion-inhibiting antibody. Nature Med. 5, 629-634, doi: 10.1038/9473 (1999).
5. Permar, S. R. et al. Prolonged measles virus shedding in human immunodeficiency virus-infected children, detected by reverse transcriptase-polymerase chain reaction. J. Infect. Dis. 183, 532-538, doi: 10.1086/318533 (2001).
6. Riddell, M. A., Moss, W. J., Hauer, D., Monze, M. & Griffin, D. E. Slow clearance of measles virus RNA after acute infection. J. Clin. Virol. 39, 312-317, doi: 10.1016/j.jcv.2007.05.006 (2007).
7. Lin, W. H., Kouyos, R. D., Adams, R. J., Grenfell, B. T. & Griffin, D. E. Prolonged persistence of measles virus RNA is characteristic of primary infection dynamics. Proc. Natl. Acad. Sci. USA 109, 14989-14994, doi: 10.1073/pnas.1211138109 (2012).
8. Kaplan, L. J., Daum, R. S., Smaron, M. & McCarthy, C. A. Severe measles in immunocompromised patients. JAMA 267, 1237-1241 (1992).
9. Permar, S. R., Griffin, D. E. & Letvin, N. L. Immune containment and consequences of measles virus infection in healthy and immunocompromised individuals. Clin. Vaccine Immunol. 13, 437-443, doi: 10.1128/CVI.13.4.437-443.2006 (2006).
10. Jaye, A., Magnusen, A. F., Sadiq, A. D., Corrah, T. & Whittle, H. C. Ex vivo analysis of cytotoxic T lymphocytes to measles antigens during infection and after vaccination in Gambian children. J. Clin. Invest. 102, 1969-1977, doi: 10.1172/JCI3290 (1998).
11. Permar, S. R. et al. Role of CD8(+) lymphocytes in control and clearance of measles virus infection of rhesus monkeys. J. Virol. 77, 4396-4400 (2003).
12. Nakayamada, S., Takahashi, H., Kanno, Y. & O'Shea, J. J. Helper T cell diversity and plasticity. Curr. Opin. Immunol. 24, 297-302, doi: 10.1016/j.coi.2012.01.014 (2012).
13. Griffin, D. E. & Ward, B. J. Differential CD4 T cell activation in measles. J. Infect. Dis. 168, 275-281 (1993).
14. Moss, W. J., Ryon, J. J., Monze, M. & Griffin, D. E. Differential regulation of interleukin (IL)-4, IL-5, and IL-10 during measles in Zambian children. J. Infect. Dis. 186, 879-887, doi: 10.1086/344230 (2002).
15. Lin, W. W., Nelson, A., Ryon, J. J., Moss, W. J. & Griffin, D. E. Plasma cytokines and chemokines in Zambian children with measles: innate responses and association with HIV-1 co-infection and in-hospital mortality. J. Infect. Dis. doi: 10.1093/infdis/jix012 (2017).
16. Lin, W. H. et al. Vaxfectin adjuvant improves antibody responses of juvenile rhesus macaques to a DNA vaccine encoding the measles virus hemagglutinin and fusion proteins. J. Virol. 87, 6560-6568, doi: 10.1128/JVI.00635-13 (2013).
17. Pantaleo, G. & Harari, A. Functional signatures in antiviral T-cell immunity for monitoring virus-associated diseases. Nature Rev. Immunol. 6, 417-423, doi: 10.1038/nri1840 (2006).
18. Kannanganat, S., Ibegbu, C., Chennareddi, L., Robinson, H. L. & Amara, R. R. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J. Virol. 81, 8468-8476, doi: 10.1128/JVI.00228-07 (2007).
19. Kannanganat, S. et al. Human immunodeficiency virus type 1 controllers but not noncontrollers maintain CD4 T cells coexpressing three cytokines. J. Virol. 81, 12071-12076, doi: 10.1128/JVI.01261-07 (2007).
20. Gibson, L. et al. Reduced frequencies of polyfunctional CMV-specific T cell responses in infants with congenital CMV infection. J. Clin. Immunol. 35, 289-301, doi: 10.1007/s10875-015-0139-3 (2015).
21. Han, Q. et al. Polyfunctional responses by human T cells result from sequential release of cytokines. Proc. Natl. Acad. Sci. USA 109, 1607-1612, doi: 10.1073/pnas.1117194109 (2012).
22. Ivanov, I. I. et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17 + T helper cells. Cell 126, 1121-1133, doi: 10.1016/j.cell.2006.07.035 (2006).
23. Lin, W. H., Pan, C. H., Adams, R. J., Laube, B. L. & Griffin, D. E. Vaccine-induced measles virus-specific T cells do not prevent infection or disease but facilitate subsequent clearance of viral RNA. mBio 5, e01047, doi: 10.1128/mBio.01047-14 (2014).
24. Griffin, D. E., Ward, B. J., Jauregui, E., Johnson, R. T. & Vaisberg, A. Immune activation in measles. New Engl. J. Med. 320, 1667-1672, doi: 10.1056/NEJM198906223202506 (1989).
25. Griffin, D. E., Ward, B. J., Jauregui, E., Johnson, R. T. & Vaisberg, A. Immune activation during measles: interferon-gamma and neopterin in plasma and cerebrospinal fluid in complicated and uncomplicated disease. J. Infect. Dis. 161, 449-453 (1990).
26. Zilliox, M. J., Moss, W. J. & Griffin, D. E. Gene expression changes in peripheral blood mononuclear cells during measles virus infection. Clin. Vaccine Immunol. 14, 918-923, doi: 10.1128/CVI.00031-07 (2007).
27. Binder, G. K. & Griffin, D. E. Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons. Science 293, 303-306, doi: 10.1126/science.1059742 (2001).
28. Schmitz, J. E. et al. Control of viremia in simian immunodeficiency virus infection by CD8 + lymphocytes. Science 283, 857-860 (1999).
29. Thimme, R. et al. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J. Virol. 77, 68-76 (2003).
30. Swain, S. L., McKinstry, K. K. & Strutt, T. M. Expanding roles for CD4(+) T cells in immunity to viruses. Nature Rev. Immunol. 12, 136-148, doi: 10.1038/nri3152 (2012).
31. Korn, T., Bettelli, E., Oukka, M. & Kuchroo, V. K. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27, 485-517, doi: 10.1146/annurev.immunol.021908.132710 (2009).
32. Shivakoti, R. et al. Limited in vivo production of type I or type III interferon after infection of macaques with vaccine or wild-type strains of measles virus. J. Interferon & Cytokine Res. 35, 292-301, doi: 10.1089/jir.2014.0122 (2015).
33. Suryawanshi, A. et al. Role of IL-17 and Th17 cells in herpes simplex virus-induced corneal immunopathology. J. Immunol. 187, 1919-1930, doi: 10.4049/jimmunol.1100736 (2011).
34. Faber, T. E., Groen, H., Welfing, M., Jansen, K. J. & Bont, L. J. Specific increase in local IL-17 production during recovery from primary RSV bronchiolitis. J. Med. Virol. 84, 1084-1088, doi: 10.1002/jmv.23291 (2012).
35. Peters, A., Lee, Y. & Kuchroo, V. K. The many faces of Th17 cells. Curr. Opin. Immunol. 23, 702-706, doi: 10.1016/j.coi.2011.08.007 (2011).
36. Onishi, R. M. & Gaffen, S. L. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 129, 311-321, doi: 10.1111/j.1365-2567.2009.03240.x (2010).
37. Arens, R. et al. Cutting edge: murine cytomegalovirus induces a polyfunctional CD4 T cell response. J. Immunol. 180, 6472-6476 (2008).
38. Hou, W., Kang, H. S. & Kim, B. S. Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J. Exp. Med. 206, 313-328, doi: 10.1084/jem.20082030 (2009).
39. Li, C. et al. IL-17 response mediates acute lung injury induced by the 2009 pandemic influenza A (H1N1) virus. Cell Res. 22, 528-538, doi: 10.1038/cr.2011.165 (2012).
40. Xie, Y. et al. The role of Th17 cells and regulatory T cells in Coxsackievirus B3-induced myocarditis. Virology 421, 78-84, doi: 10.1016/j.virol.2011.09.006 (2011).
41. Crowe, C. R. et al. Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 183, 5301-5310, doi: 10.4049/jimmunol.0900995 (2009).
42. Campillo-Gimenez, L. et al. AIDS progression is associated with the emergence of IL-17-producing cells early after simian immunodeficiency virus infection. J. Immunol. 184, 984-992, doi: 10.4049/jimmunol.0902316 (2010).
43. Cecchinato, V. & Franchini, G. Th17 cells in pathogenic simian immunodeficiency virus infection of macaques. Curr. Opin. HIV AIDS 5, 141-145, doi: 10.1097/COH.0b013e32833653ec (2010).
44. Khowawisetsut, L. et al. Relationships between IL-17(+) subsets, Tregs and pDCs that distinguish among SIV infected elite controllers, low, medium and high viral load rhesus macaques. PloS One 8, e61264, doi: 10.1371/journal.pone.0061264 (2013).
45. Yue, F. Y. et al. Virus-specific interleukin-17-producing CD4 + T cells are detectable in early human immunodeficiency virus type 1 infection. J. Virol. 82, 6767-6771, doi: 10.1128/JVI.02550-07 (2008).
46. Basha, H. I. et al. Characterization of HCV-specific CD4 + Th17 immunity in recurrent hepatitis C-induced liver allograft fibrosis. Am. J. Transplan. 11, 775-785, doi: 10.1111/j.1600-6143.2011.03458.x (2011).
47. Li, S. et al. Peripheral T lymphocyte subset imbalances in children with enterovirus 71-induced hand, foot and mouth disease. Virus Res. 180, 84-91, doi: 10.1016/j.virusres.2013.11.021 (2014).
48. Patera, A. C., Pesnicak, L., Bertin, J. & Cohen, J. I. Interleukin 17 modulates the immune response to vaccinia virus infection. Virology 299, 56-63 (2002).
49. Zhang, J. Y. et al. Interleukin-17-producing CD4(+) T cells increase with severity of liver damage in patients with chronic hepatitis B. Hepatology 51, 81-91, doi: 10.1002/hep.23273 (2010).
50. McKinstry, K. K. et al. Memory CD4 + T cells protect against influenza through multiple synergizing mechanisms. J. Clin. Invest. 122, 2847-2856, doi: 10.1172/JCI63689 (2012).
51. Molesworth-Kenyon, S. J., Yin, R., Oakes, J. E. & Lausch, R. N. IL-17 receptor signaling influences virus-induced corneal inflammation. J. Leuk. Biol. 83, 401-408, doi: 10.1189/jlb.0807571 (2008).
52. Ryon, J. J., Moss, W. J., Monze, M. & Griffin, D. E. Functional and phenotypic changes in circulating lymphocytes from hospitalized Zambian children with measles. Clin. Diag. Lab. Immunol. 9, 994-1003 (2002).
53. Ono, N. et al. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J. Virol. 75, 4399-4401, doi: 10.1128/JVI.75.9.4399-4401.2001 (2001).
54. Pan, C. H. et al. Modulation of disease, T cell responses, and measles virus clearance in monkeys vaccinated with H-encoding alphavirus replicon particles. Proc. Natl. Acad. Sci. USA 102, 11581-11588, doi: 10.1073/pnas.0504592102 (2005).