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CD16+ natural killer cells play a limited role against primary dengue virus infection in tamarins

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Abstract

CD16 is a major molecule expressed on NK cells. To directly assess the role of natural killer (NK) cells in dengue virus (DENV) infection in vivo, CD16 antibody-treated tamarins were inoculated with a DENV-2 strain. This resulted in the transient depletion of CD16+ NK cells, whereas no significant effects on the overall levels or kinetics of plasma viral loads and antiviral antibodies were observed in the treated monkeys when compared to control monkeys. It remains elusive whether the CD16 NK subpopulation could play an important role in the control of primary DENV infection.

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References

  1. Alcon-LePoder S, Sivard P, Drouet MT, Talarmin A, Rice C, Flamand M (2006) Secretion of flaviviral non-structural protein NS1: from diagnosis to pathogenesis. Novartis Found Symp 277:233–247 (discussion 247–253)

    Article  PubMed  CAS  Google Scholar 

  2. Azeredo EL, De Oliveira-Pinto LM, Zagne SM, Cerqueira DI, Nogueira RM, Kubelka CF (2006) NK cells, displaying early activation, cytotoxicity and adhesion molecules, are associated with mild dengue disease. Clin Exp Immunol 143:345–356

    Article  PubMed  CAS  Google Scholar 

  3. Bjorkstrom NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, Bjorklund AT, Flodstrom-Tullberg M, Michaelsson J, Rottenberg ME, Guzman CA, Ljunggren HG, Malmberg KJ (2010) Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 116:3853–3864

    Article  PubMed  Google Scholar 

  4. Caligiuri MA (2008) Human natural killer cells. Blood 112:461–469

    Article  PubMed  CAS  Google Scholar 

  5. Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, Carson WE, Caligiuri MA (2001) Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97:3146–3151

    Article  PubMed  CAS  Google Scholar 

  6. Farag SS, Caligiuri MA (2006) Human natural killer cell development and biology. Blood Rev 20:123–137

    Article  PubMed  CAS  Google Scholar 

  7. Fleit HB, Wright SD, Unkeless JC (1982) Human neutrophil Fc gamma receptor distribution and structure. Proc Natl Acad Sci USA 79:3275–3279

    Article  PubMed  CAS  Google Scholar 

  8. Gayoso I, Sanchez-Correa B, Campos C, Alonso C, Pera A, Casado JG, Morgado S, Tarazona R, Solana R (2011) Immunosenescence of human natural killer cells. J Innate Immun 3:337–343

    Article  PubMed  CAS  Google Scholar 

  9. Green S, Pichyangkul S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Nisalak A, Kurane I, Rothman AL, Ennis FA (1999) Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis 180:1429–1435

    Article  PubMed  CAS  Google Scholar 

  10. Guzman MG, Kouri G, Valdes L, Bravo J, Alvarez M, Vazques S, Delgado I, Halstead SB (2000) Epidemiologic studies on Dengue in Santiago de Cuba, 1997. Am J Epidemiol 152:793–799 (discussion 804)

    Article  PubMed  CAS  Google Scholar 

  11. Halstead SB, Lan NT, Myint TT, Shwe TN, Nisalak A, Kalyanarooj S, Nimmannitya S, Soegijanto S, Vaughn DW, Endy TP (2002) Dengue hemorrhagic fever in infants: research opportunities ignored. Emerg Infect Dis 8:1474–1479

    PubMed  Google Scholar 

  12. Halstead SB (2007) Dengue. Lancet 370:1644–1652

    Article  PubMed  Google Scholar 

  13. Hershkovitz O, Rosental B, Rosenberg LA, Navarro-Sanchez ME, Jivov S, Zilka A, Gershoni-Yahalom O, Brient-Litzler E, Bedouelle H, Ho JW, Campbell KS, Rager-Zisman B, Despres P, Porgador A (2009) NKp44 receptor mediates interaction of the envelope glycoproteins from the West Nile and dengue viruses with NK cells. J Immunol 183:2610–2621

    Article  PubMed  CAS  Google Scholar 

  14. Kurane I, Hebblewaite D, Ennis FA (1986) Characterization with monoclonal antibodies of human lymphocytes active in natural killing and antibody-dependent cell-mediated cytotoxicity of dengue virus-infected cells. Immunology 58:429–436

    PubMed  CAS  Google Scholar 

  15. Lee SH, Miyagi T, Biron CA (2007) Keeping NK cells in highly regulated antiviral warfare. Trends Immunol 28:252–259

    Article  PubMed  CAS  Google Scholar 

  16. Libraty DH, Young PR, Pickering D, Endy TP, Kalayanarooj S, Green S, Vaughn DW, Nisalak A, Ennis FA, Rothman AL (2002) High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J Infect Dis 186:1165–1168

    Article  PubMed  CAS  Google Scholar 

  17. Libraty DH, Acosta LP, Tallo V, Segubre-Mercado E, Bautista A, Potts JA, Jarman RG, Yoon IK, Gibbons RV, Brion JD, Capeding RZ (2009) A prospective nested case-control study of Dengue in infants: rethinking and refining the antibody-dependent enhancement dengue hemorrhagic fever model. PLoS Med 6:e1000171

    Article  PubMed  Google Scholar 

  18. Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL (2010) CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 116:3865–3874

    Article  PubMed  CAS  Google Scholar 

  19. Mailliard RB, Alber SM, Shen H, Watkins SC, Kirkwood JM, Herberman RB, Kalinski P (2005) IL-18-induced CD83+CCR7+ NK helper cells. J Exp Med 202:941–953

    Article  PubMed  CAS  Google Scholar 

  20. Mathew A, Rothman AL (2008) Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol Rev 225:300–313

    Article  PubMed  CAS  Google Scholar 

  21. Navarro-Sanchez E, Despres P, Cedillo-Barron L (2005) Innate immune responses to dengue virus. Arch Med Res 36:425–435

    Article  PubMed  CAS  Google Scholar 

  22. Omatsu T, Moi ML, Hirayama T, Takasaki T, Nakamura S, Tajima S, Ito M, Yoshida T, Saito A, Katakai Y, Akari H, Kurane I (2011) Common marmoset (Callithrix jacchus) as a primate model of dengue virus infection: development of high levels of viremia and demonstration of protective immunity. J Gen Virol 92:2271–2280. doi:10.1099/vir.0.031229-0

    Article  Google Scholar 

  23. Scalzo AA, Corbett AJ, Rawlinson WD, Scott GM, Degli-Esposti MA (2007) The interplay between host and viral factors in shaping the outcome of cytomegalovirus infection. Immunol Cell Biol 85:46–54

    Article  PubMed  CAS  Google Scholar 

  24. Shresta S, Kyle JL, Robert Beatty P, Harris E (2004) Early activation of natural killer and B cells in response to primary dengue virus infection in A/J mice. Virology 319:262–273

    Article  PubMed  CAS  Google Scholar 

  25. Suwannasaen D, Romphruk A, Leelayuwat C, Lertmemongkolchai G (2010) Bystander T cells in human immune responses to dengue antigens. BMC Immunol 11:47

    Article  PubMed  Google Scholar 

  26. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, Suntayakorn S, Endy TP, Raengsakulrach B, Rothman AL, Ennis FA, Nisalak A (2000) Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181:2–9

    Article  PubMed  CAS  Google Scholar 

  27. Wahid SF, Sanusi S, Zawawi MM, Ali RA (2000) A comparison of the pattern of liver involvement in dengue hemorrhagic fever with classic dengue fever. Southeast Asian J Trop Med Public Health 31:259–263

    PubMed  CAS  Google Scholar 

  28. Woollard DJ, Haqshenas G, Dong X, Pratt BF, Kent SJ, Gowans EJ (2008) Virus-specific T-cell immunity correlates with control of GB virus B infection in marmosets. J Virol 82:3054–3060

    Article  PubMed  CAS  Google Scholar 

  29. Yoshida T, Saito A, Iwasaki Y, Iijima S, Kurosawa T, Katakai Y, Yasutomi Y, Reimann KA, Hayakawa T, Akari H (2010) Characterization of natural Killer cells in tamarins: a technical basis for studies of innate immunity. Front Microbiol 1:128. doi:10.3389/fmicb.2010.00128

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Acknowledgments

We would like to give special thanks to members of the Corporation for Production and Research of Laboratory Primates for technical assistance. We also would like to give special thanks to Ms. Tomoko Ikoma and Ms. Mizuho Fujita for technical assistance. Moreover, we appreciate Dr. Keith A. Reimann (the NIH Nonhuman Primate Reagent Resource R24 RR016001, NIAID contact HHSN272200900037C) for providing CD16 antibody. This work was supported by grants from the Ministry of Health, Labor and Welfare of Japan (to Hirofumi Akari and Ichiro Kurane). This research was also supported by the Environment Research and Technology Development Fund (D-1007) from the Ministry of the Environment of Japan (to Tomoyuki Yoshida and Hirofumi Akari).

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Correspondence to Tomoyuki Yoshida or Hirofumi Akari.

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T. Yoshida and T. Omatsu contributed equally to this study.

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Yoshida, T., Omatsu, T., Saito, A. et al. CD16+ natural killer cells play a limited role against primary dengue virus infection in tamarins. Arch Virol 157, 363–368 (2012). https://doi.org/10.1007/s00705-011-1178-6

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  • DOI: https://doi.org/10.1007/s00705-011-1178-6

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