Formation of Infectious Dengue Virus–Antibody Immune Complex In Vivo in Marmosets (Callithrix jacchus) After Passive Transfer of Anti-Dengue Virus Monoclonal Antibodies and Infection with Dengue Virus (original) (raw)

Print ISSN:

0002-9637

Online ISSN:

1476-1645

• Introduction
• Materials and Methods
  • Primates.
  • DENV strains and propagation.
  • Antibodies.
  • Inoculation of marmosets with DENV.
  • Quantification of viremia by quantitative reverse transcriptase polymerase chain reaction and plaque assay.
  • Serological studies.
  • Statistics.
• Results
  • Detection of infectious DENV–Ab immune complex using FcγR-expressing cells in marmosets passively transferred with mAbs.
  • Detection of mouse IgG Ab in plasma samples from marmosets after administration of mAbs.
  • Absence of marmoset anti-DENV IgM and IgG on days 0, 2, and 4 after DENV inoculation.
  • Neutralizing Ab in marmosets after Ab administration and DENV inoculation.
  • Limited effect of administration of a DENV infection-enhancing mAb in marmosets.
• Discussion

ProCite

RefWorks

Reference Manager

• 1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI, 2013. The global distribution and burden of dengue. Nature 496: 504–507.
  • PubMed
    BhattSGethingPWBradyOJMessinaJPFarlowAWMoyesCLDrakeJMBrownsteinJSHoenAGSankohOMyersMFGeorgeDBJaenischTWintGRSimmonsCPScottTWFarrarJJHaySI, 2013. The global distribution and burden of dengue. Nature 496: 504–507.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. WHO, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
  • PubMed
    WHO, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB, 1984. Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120: 653–669.
  • PubMed
    SangkawibhaNRojanasuphotSAhandrikSViriyapongseSJatanasenSSalitulVPhanthumachindaBHalsteadSB, 1984. Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120: 653–669.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Guzman MG, Kouri GP, Bravo J, Calunga M, Soler M, Vazquez S, Venereo C, 1984. Dengue haemorrhagic fever in Cuba. I. Serological confirmation of clinical diagnosis. Trans R Soc Trop Med Hyg 78: 235–238.
  • PubMed
    GuzmanMGKouriGPBravoJCalungaMSolerMVazquezSVenereoC, 1984. Dengue haemorrhagic fever in Cuba. I. Serological confirmation of clinical diagnosis. Trans R Soc Trop Med Hyg 78: 235–238.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Guzman MG, Alvarez M, Halstead SB, 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158: 1445–1459.
  • PubMed
    GuzmanMGAlvarezMHalsteadSB, 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158: 1445–1459.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS, 1989. Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40: 444–451.
  • PubMed
    KliksSCNisalakABrandtWEWahlLBurkeDS, 1989. Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40: 444–451.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, O'Rourke EJ, 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146: 201–217.
  • PubMed
    HalsteadSBO'RourkeEJ, 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146: 201–217.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Kontny U, Kurane I, Ennis FA, 1988. Gamma interferon augments Fc gamma receptor-mediated dengue virus infection of human monocytic cells. J Virol 62: 3928–3933.
  • PubMed
    KontnyUKuraneIEnnisFA, 1988. Gamma interferon augments Fc gamma receptor-mediated dengue virus infection of human monocytic cells. J Virol 62: 3928–3933.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ruangjirachuporn W, Boonpucknavig S, Nimmanitya S, 1979. Circulating immune complexes in serum from patients with dengue haemorrhagic fever. Clin Exp Immunol 36: 46–53.
  • PubMed
    RuangjirachupornWBoonpucknavigSNimmanityaS, 1979. Circulating immune complexes in serum from patients with dengue haemorrhagic fever. Clin Exp Immunol 36: 46–53.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Wang WK, Chen HL, Yang CF, Hsieh SC, Juan CC, Chang SM, Yu CC, Lin LH, Huang JH, King CC, 2006. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin Infect Dis 43: 1023–1030.
  • PubMed
    WangWKChenHLYangCFHsiehSCJuanCCChangSMYuCCLinLHHuangJHKingCC, 2006. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin Infect Dis 43: 1023–1030.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Lim CK, Kotaki A, Takasaki T, Kurane I, 2011. Detection of higher levels of dengue viremia using FcγR-expressing BHK-21 cells than FcγR-negative cells in secondary infection but not in primary infection. J Infect Dis 203: 1405–1414.
  • PubMed
    MoiMLLimCKKotakiATakasakiTKuraneI, 2011. Detection of higher levels of dengue viremia using FcγR-expressing BHK-21 cells than FcγR-negative cells in secondary infection but not in primary infection. J Infect Dis 203: 1405–1414.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Kliks SC, Nimmanitya S, Nisalak A, Burke DS, 1988. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg 38: 411–419.
  • PubMed
    KliksSCNimmanityaSNisalakABurkeDS, 1988. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg 38: 411–419.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ito M, Mukai RZ, Takasaki T, Kotaki A, Kurane I, 2010. Antibody-dependent enhancement of dengue virus infection in vitro by undiluted sera from monkeys infected with heterotypic dengue virus. Arch Virol 155: 1617–1624.
  • PubMed
    ItoMMukaiRZTakasakiTKotakiAKuraneI, 2010. Antibody-dependent enhancement of dengue virus infection in vitro by undiluted sera from monkeys infected with heterotypic dengue virus. Arch Virol 155: 1617–1624.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Takasaki T, Saijo M, Kurane I, 2013. Dengue virus infection-enhancing activity of undiluted sera obtained from patients with secondary dengue virus infection. Trans R Soc Trop Med Hyg 107: 51–58.
  • PubMed
    MoiMLTakasakiTSaijoMKuraneI, 2013. Dengue virus infection-enhancing activity of undiluted sera obtained from patients with secondary dengue virus infection. Trans R Soc Trop Med Hyg 107: 51–58.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ng JK, Zhang SL, Tan HC, Yan B, Maria Martinez Gomez J, Tan WY, Lam JH, Tan GK, Ooi EE, Alonso S, 2014. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog 10: e1004031.
  • PubMed
    NgJKZhangSLTanHCYanBMaria Martinez GomezJTanWYLamJHTanGKOoiEEAlonsoS, 2014. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog 10: e1004031.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ, 2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 104: 9422–9427.
  • PubMed
    GoncalvezAPEngleRESt ClaireMPurcellRHLaiCJ, 2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 104: 9422–9427.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, Shotwell H, Casals J, 1973. Studies on the pathogenesis of dengue infection in monkeys. II. Clinical laboratory responses to heterologous infection. J Infect Dis 128: 15–22.
  • PubMed
    HalsteadSBShotwellHCasalsJ, 1973. Studies on the pathogenesis of dengue infection in monkeys. II. Clinical laboratory responses to heterologous infection. J Infect Dis 128: 15–22.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, Mehlhop E, Johnson S, Diamond MS, Beatty PR, Harris E, 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790.
  • PubMed
    BalsitisSJWilliamsKLLachicaRFloresDKyleJLMehlhopEJohnsonSDiamondMSBeattyPRHarrisE, 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. 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 viraemia and demonstration of protective immunity. J Gen Virol 92: 2272–2280.
  • PubMed
    OmatsuTMoiMLHirayamaTTakasakiTNakamuraSTajimaSItoMYoshidaTSaitoAKatakaiYAkariHKuraneI, 2011. Common marmoset (Callithrix jacchus) as a primate model of dengue virus infection: development of high levels of viraemia and demonstration of protective immunity. J Gen Virol 92: 2272–2280.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Takasaki T, Omatsu T, Nakamura S, Katakai Y, Ami Y, Suzaki Y, Saijo M, Akari H, Kurane I, 2014. Demonstration of marmosets (Callithrix jacchus) as a non-human primate model for secondary dengue virus infection: high levels of viraemia and serotype cross-reactive antibody responses consistent with secondary infection of humans. J Gen Virol 95: 591–600.
  • PubMed
    MoiMLTakasakiTOmatsuTNakamuraSKatakaiYAmiYSuzakiYSaijoMAkariHKuraneI, 2014. Demonstration of marmosets (Callithrix jacchus) as a non-human primate model for secondary dengue virus infection: high levels of viraemia and serotype cross-reactive antibody responses consistent with secondary infection of humans. J Gen Virol 95: 591–600.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Henchal EA, Gentry MK, McCown JM, Brandt WE, 1982. Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31: 830–836.
  • PubMed
    HenchalEAGentryMKMcCownJMBrandtWE, 1982. Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31: 830–836.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Takasaki T, Saijo M, Kurane I, 2014. Determination of antibody concentration as the main parameter in a dengue virus antibody-dependent enhancement assay using FcγR-expressing BHK cells. Arch Virol 159: 103–116.
  • PubMed
    MoiMLTakasakiTSaijoMKuraneI, 2014. Determination of antibody concentration as the main parameter in a dengue virus antibody-dependent enhancement assay using FcγR-expressing BHK cells. Arch Virol 159: 103–116.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Lim CK, Kotaki A, Takasaki T, Kurane I, 2010. Development of an antibody-dependent enhancement assay for dengue virus using stable BHK-21 cell lines expressing Fc gammaRIIA. J Virol Methods 163: 205–209.
  • PubMed
    MoiMLLimCKKotakiATakasakiTKuraneI, 2010. Development of an antibody-dependent enhancement assay for dengue virus using stable BHK-21 cell lines expressing Fc gammaRIIA. J Virol Methods 163: 205–209.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ito M, Takasaki T, Yamada K, Nerome R, Tajima S, Kurane I, 2004. Development and evaluation of fluorogenic TaqMan reverse transcriptase PCR assays for detection of dengue virus types 1 to 4. J Clin Microbiol 42: 5935–5937.
  • PubMed
    ItoMTakasakiTYamadaKNeromeRTajimaSKuraneI, 2004. Development and evaluation of fluorogenic TaqMan reverse transcriptase PCR assays for detection of dengue virus types 1 to 4. J Clin Microbiol 42: 5935–5937.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Lim CK, Chua KB, Takasaki T, Kurane I, 2012. Dengue virus infection-enhancing activity in serum samples with neutralizing activity as determined by using FcγR-expressing cells. PLoS Negl Trop Dis 6: e1536.
  • PubMed
    MoiMLLimCKChuaKBTakasakiTKuraneI, 2012. Dengue virus infection-enhancing activity in serum samples with neutralizing activity as determined by using FcγR-expressing cells. PLoS Negl Trop Dis 6: e1536.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ito M, Katakai Y, Ono F, Akari H, Mukai RZ, Takasaki T, Kotaki A, Kurane I, 2011. Serotype-specific and cross-reactive neutralizing antibody responses in cynomolgus monkeys after infection with multiple dengue virus serotypes. Arch Virol 156: 1073–1077.
  • PubMed
    ItoMKatakaiYOnoFAkariHMukaiRZTakasakiTKotakiAKuraneI, 2011. Serotype-specific and cross-reactive neutralizing antibody responses in cynomolgus monkeys after infection with multiple dengue virus serotypes. Arch Virol 156: 1073–1077.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Boonnak K, Slike BM, Donofrio GC, Marovich MA, 2013. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J Immunol 190: 5659–5665.
  • PubMed
    BoonnakKSlikeBMDonofrioGCMarovichMA, 2013. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J Immunol 190: 5659–5665.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chan KR, Ong EZ, Tan HC, Zhang SL, Zhang Q, Tang KF, Kaliaperumal N, Lim AP, Hibberd ML, Chan SH, Connolly JE, Krishnan MN, Lok SM, Hanson BJ, Lin CN, Ooi EE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2727.
  • PubMed
    ChanKROngEZTanHCZhangSLZhangQTangKFKaliaperumalNLimAPHibberdMLChanSHConnollyJEKrishnanMNLokSMHansonBJLinCNOoiEE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2727.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, Mahalingam S, Marovich MA, Ubol S, Mosser DM, 2010. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 10: 712–722.
  • PubMed
    HalsteadSBMahalingamSMarovichMAUbolSMosserDM, 2010. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 10: 712–722.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ubol S, Halstead SB, 2010. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin Vaccine Immunol 17: 1829–1835.
  • PubMed
    UbolSHalsteadSB, 2010. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin Vaccine Immunol 17: 1829–1835.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ubol S, Phuklia W, Kalayanarooj S, Modhiran N, 2010. Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 201: 923–935.
  • PubMed
    UbolSPhukliaWKalayanaroojSModhiranN, 2010. Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 201: 923–935.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, 2009. Pathogenesis: Risk factors prior to infection. Halstead SB, Pasvol G, Hoffman SL, ed. Dengue (Tropical Medicine: Science and Practice). London, United Kingdom: Imperial College Press, 219–256.
  • PubMed
    HalsteadSB, 2009. Pathogenesis: Risk factors prior to infection. HalsteadSBPasvolGHoffmanSL, ed. Dengue (Tropical Medicine: Science and Practice). London, United Kingdom: Imperial College Press, 219–256.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, 1979. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140: 527–533.
  • PubMed
    HalsteadSB, 1979. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140: 527–533.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. The Marmoset Genome Sequencing and Analysis Consortium, 2014. The common marmoset genome provides insight into primate biology and evolution. Nat Genet 46: 850–857.
  • PubMed
    The Marmoset Genome Sequencing and Analysis Consortium, 2014. The common marmoset genome provides insight into primate biology and evolution. Nat Genet 46: 850–857.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chan KR, Ong EZ, Tan HC, Zhang SL, Zhang Q, Tang KF, Kaliaperumal N, Lim AP, Hibberd ML, Chan SH, Connolly JE, Krishnan MN, Lok SM, Hanson BJ, Lin CN, Ooi EE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2777.
  • PubMed
    ChanKROngEZTanHCZhangSLZhangQTangKFKaliaperumalNLimAPHibberdMLChanSHConnollyJEKrishnanMNLokSMHansonBJLinCNOoiEE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2777.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Nimmerjahn F, Lux A, 2014. LILR-B1 blocks activating FcγR signaling to allow antibody dependent enhancement of dengue virus infection. Proc Natl Acad Sci USA 111: 2404–2405.
  • PubMed
    NimmerjahnFLuxA, 2014. LILR-B1 blocks activating FcγR signaling to allow antibody dependent enhancement of dengue virus infection. Proc Natl Acad Sci USA 111: 2404–2405.
    )| false
  • Search Google Scholar
  • Export Citation

,

,

,

,

,

,

,

,

,

, and

View More View Less

• Abstract/Excerpt
• Author Notes

Infection with a dengue virus (DENV) serotype induces cross-reactive, weakly neutralizing antibodies to different dengue serotypes. It has been postulated that cross-reactive antibodies form a virus–antibody immune complex and enhance DENV infection of Fc gamma receptor (FcγR)-bearing cells. We determined whether infectious DENV–antibody immune complex is formed in vivo in marmosets after passive transfer of DENV-specific monoclonal antibody (mAb) and DENV inoculation and whether infectious DENV–antibody immune complex is detectable using FcγR-expressing cells. Marmosets showed that DENV–antibody immune complex was exclusively infectious to FcγR-expressing cells on days 2, 4, and 7 after passive transfer of each of the mAbs (mAb 4G2 and mAb 6B6C) and DENV inoculation. Although DENV–antibody immune complex was detected, contribution of the passively transferred antibody to overall viremia levels was limited in this study. The results indicate that DENV cross-reactive antibodies form DENV–antibody immune complex in vivo, which is infectious to FcγR-bearing cells but not FcγR-negative cells.

Author Notes

* Address correspondence to Ichiro Kurane or Tomohiko Takasaki, National Institute of Infectious Diseases, Tokyo, Japan. E-mails: kurane@nih.go.jp or takasaki@nih.go.jp

Financial support: This work was supported by Research on Emerging and Re-Emerging Infectious Diseases Grants H23-shinkou-ippan-010 and H26-shinkou-jitsuyouka-007 from the Ministry of Health, Labour and Welfare, Japan and Kiban B Grant-in-Aid for Scientific Research 25293112 and Young Scientists B Grant-in-Aid for Scientific Research 26870872 from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Authors' addresses: Meng Ling Moi, Chang-Kweng Lim, Masayuki Saijo, and Tomohiko Takasaki, Department of Virology 1, National Institute of Infectious Diseases, Tokyo, Japan, E-mails: sherry@nih.go.jp, ck@nih.go.jp, msaijo@nih.go.jp, and takasaki@nih.go.jp. Yasushi Ami and Yuriko Suzaki, Division of Experimental Animal Research, National Institute of Infectious Diseases, Musashimurayama, Tokyo, Japan, E-mails: yami@nih.go.jp and ysuzaki@nih.go.jp. Kenji Shirai, Kazutaka Kitaura, and Ryuji Suzuki, Department of Rheumatology and Clinical Immunology, Clinical Research Center for Allergy and Rheumatology, Sagamihara National Hospital, National Hospital Organization, Kanagawa, Japan, E-mails: k.shirai0727@gmail.com, kitaura@nih.go.jp, and r-suzuki@sagamihara-hosp.gr.jp. Yuka Saito, Department of Virology 1, National Institute of Infectious Diseases, Tokyo, Japan, and College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa, Japan, E-mail: saito-y@nih.go.jp. Ichiro Kurane, National Institute of Infectious Diseases, Tokyo, Japan, E-mail: kurane@nih.go.jp.

Copyright:

© The American Society of Tropical Medicine and Hygiene 2015

Received:

23 Jul 2014

|

Accepted:

20 Nov 2014

|

Published Online:

04 Feb 2015

Print ISSN:

0002-9637

Online ISSN:

1476-1645

• Introduction
• Materials and Methods
  • Primates.
  • DENV strains and propagation.
  • Antibodies.
  • Inoculation of marmosets with DENV.
  • Quantification of viremia by quantitative reverse transcriptase polymerase chain reaction and plaque assay.
  • Serological studies.
  • Statistics.
• Results
  • Detection of infectious DENV–Ab immune complex using FcγR-expressing cells in marmosets passively transferred with mAbs.
  • Detection of mouse IgG Ab in plasma samples from marmosets after administration of mAbs.
  • Absence of marmoset anti-DENV IgM and IgG on days 0, 2, and 4 after DENV inoculation.
  • Neutralizing Ab in marmosets after Ab administration and DENV inoculation.
  • Limited effect of administration of a DENV infection-enhancing mAb in marmosets.
• Discussion

ProCite

RefWorks

Reference Manager

• 1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI, 2013. The global distribution and burden of dengue. Nature 496: 504–507.
  • PubMed
    BhattSGethingPWBradyOJMessinaJPFarlowAWMoyesCLDrakeJMBrownsteinJSHoenAGSankohOMyersMFGeorgeDBJaenischTWintGRSimmonsCPScottTWFarrarJJHaySI, 2013. The global distribution and burden of dengue. Nature 496: 504–507.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. WHO, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
  • PubMed
    WHO, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB, 1984. Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120: 653–669.
  • PubMed
    SangkawibhaNRojanasuphotSAhandrikSViriyapongseSJatanasenSSalitulVPhanthumachindaBHalsteadSB, 1984. Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120: 653–669.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Guzman MG, Kouri GP, Bravo J, Calunga M, Soler M, Vazquez S, Venereo C, 1984. Dengue haemorrhagic fever in Cuba. I. Serological confirmation of clinical diagnosis. Trans R Soc Trop Med Hyg 78: 235–238.
  • PubMed
    GuzmanMGKouriGPBravoJCalungaMSolerMVazquezSVenereoC, 1984. Dengue haemorrhagic fever in Cuba. I. Serological confirmation of clinical diagnosis. Trans R Soc Trop Med Hyg 78: 235–238.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Guzman MG, Alvarez M, Halstead SB, 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158: 1445–1459.
  • PubMed
    GuzmanMGAlvarezMHalsteadSB, 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158: 1445–1459.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS, 1989. Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40: 444–451.
  • PubMed
    KliksSCNisalakABrandtWEWahlLBurkeDS, 1989. Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40: 444–451.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, O'Rourke EJ, 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146: 201–217.
  • PubMed
    HalsteadSBO'RourkeEJ, 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146: 201–217.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Kontny U, Kurane I, Ennis FA, 1988. Gamma interferon augments Fc gamma receptor-mediated dengue virus infection of human monocytic cells. J Virol 62: 3928–3933.
  • PubMed
    KontnyUKuraneIEnnisFA, 1988. Gamma interferon augments Fc gamma receptor-mediated dengue virus infection of human monocytic cells. J Virol 62: 3928–3933.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ruangjirachuporn W, Boonpucknavig S, Nimmanitya S, 1979. Circulating immune complexes in serum from patients with dengue haemorrhagic fever. Clin Exp Immunol 36: 46–53.
  • PubMed
    RuangjirachupornWBoonpucknavigSNimmanityaS, 1979. Circulating immune complexes in serum from patients with dengue haemorrhagic fever. Clin Exp Immunol 36: 46–53.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Wang WK, Chen HL, Yang CF, Hsieh SC, Juan CC, Chang SM, Yu CC, Lin LH, Huang JH, King CC, 2006. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin Infect Dis 43: 1023–1030.
  • PubMed
    WangWKChenHLYangCFHsiehSCJuanCCChangSMYuCCLinLHHuangJHKingCC, 2006. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin Infect Dis 43: 1023–1030.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Lim CK, Kotaki A, Takasaki T, Kurane I, 2011. Detection of higher levels of dengue viremia using FcγR-expressing BHK-21 cells than FcγR-negative cells in secondary infection but not in primary infection. J Infect Dis 203: 1405–1414.
  • PubMed
    MoiMLLimCKKotakiATakasakiTKuraneI, 2011. Detection of higher levels of dengue viremia using FcγR-expressing BHK-21 cells than FcγR-negative cells in secondary infection but not in primary infection. J Infect Dis 203: 1405–1414.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Kliks SC, Nimmanitya S, Nisalak A, Burke DS, 1988. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg 38: 411–419.
  • PubMed
    KliksSCNimmanityaSNisalakABurkeDS, 1988. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg 38: 411–419.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ito M, Mukai RZ, Takasaki T, Kotaki A, Kurane I, 2010. Antibody-dependent enhancement of dengue virus infection in vitro by undiluted sera from monkeys infected with heterotypic dengue virus. Arch Virol 155: 1617–1624.
  • PubMed
    ItoMMukaiRZTakasakiTKotakiAKuraneI, 2010. Antibody-dependent enhancement of dengue virus infection in vitro by undiluted sera from monkeys infected with heterotypic dengue virus. Arch Virol 155: 1617–1624.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Takasaki T, Saijo M, Kurane I, 2013. Dengue virus infection-enhancing activity of undiluted sera obtained from patients with secondary dengue virus infection. Trans R Soc Trop Med Hyg 107: 51–58.
  • PubMed
    MoiMLTakasakiTSaijoMKuraneI, 2013. Dengue virus infection-enhancing activity of undiluted sera obtained from patients with secondary dengue virus infection. Trans R Soc Trop Med Hyg 107: 51–58.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ng JK, Zhang SL, Tan HC, Yan B, Maria Martinez Gomez J, Tan WY, Lam JH, Tan GK, Ooi EE, Alonso S, 2014. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog 10: e1004031.
  • PubMed
    NgJKZhangSLTanHCYanBMaria Martinez GomezJTanWYLamJHTanGKOoiEEAlonsoS, 2014. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog 10: e1004031.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ, 2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 104: 9422–9427.
  • PubMed
    GoncalvezAPEngleRESt ClaireMPurcellRHLaiCJ, 2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 104: 9422–9427.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, Shotwell H, Casals J, 1973. Studies on the pathogenesis of dengue infection in monkeys. II. Clinical laboratory responses to heterologous infection. J Infect Dis 128: 15–22.
  • PubMed
    HalsteadSBShotwellHCasalsJ, 1973. Studies on the pathogenesis of dengue infection in monkeys. II. Clinical laboratory responses to heterologous infection. J Infect Dis 128: 15–22.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, Mehlhop E, Johnson S, Diamond MS, Beatty PR, Harris E, 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790.
  • PubMed
    BalsitisSJWilliamsKLLachicaRFloresDKyleJLMehlhopEJohnsonSDiamondMSBeattyPRHarrisE, 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. 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 viraemia and demonstration of protective immunity. J Gen Virol 92: 2272–2280.
  • PubMed
    OmatsuTMoiMLHirayamaTTakasakiTNakamuraSTajimaSItoMYoshidaTSaitoAKatakaiYAkariHKuraneI, 2011. Common marmoset (Callithrix jacchus) as a primate model of dengue virus infection: development of high levels of viraemia and demonstration of protective immunity. J Gen Virol 92: 2272–2280.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Takasaki T, Omatsu T, Nakamura S, Katakai Y, Ami Y, Suzaki Y, Saijo M, Akari H, Kurane I, 2014. Demonstration of marmosets (Callithrix jacchus) as a non-human primate model for secondary dengue virus infection: high levels of viraemia and serotype cross-reactive antibody responses consistent with secondary infection of humans. J Gen Virol 95: 591–600.
  • PubMed
    MoiMLTakasakiTOmatsuTNakamuraSKatakaiYAmiYSuzakiYSaijoMAkariHKuraneI, 2014. Demonstration of marmosets (Callithrix jacchus) as a non-human primate model for secondary dengue virus infection: high levels of viraemia and serotype cross-reactive antibody responses consistent with secondary infection of humans. J Gen Virol 95: 591–600.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Henchal EA, Gentry MK, McCown JM, Brandt WE, 1982. Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31: 830–836.
  • PubMed
    HenchalEAGentryMKMcCownJMBrandtWE, 1982. Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31: 830–836.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Takasaki T, Saijo M, Kurane I, 2014. Determination of antibody concentration as the main parameter in a dengue virus antibody-dependent enhancement assay using FcγR-expressing BHK cells. Arch Virol 159: 103–116.
  • PubMed
    MoiMLTakasakiTSaijoMKuraneI, 2014. Determination of antibody concentration as the main parameter in a dengue virus antibody-dependent enhancement assay using FcγR-expressing BHK cells. Arch Virol 159: 103–116.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Lim CK, Kotaki A, Takasaki T, Kurane I, 2010. Development of an antibody-dependent enhancement assay for dengue virus using stable BHK-21 cell lines expressing Fc gammaRIIA. J Virol Methods 163: 205–209.
  • PubMed
    MoiMLLimCKKotakiATakasakiTKuraneI, 2010. Development of an antibody-dependent enhancement assay for dengue virus using stable BHK-21 cell lines expressing Fc gammaRIIA. J Virol Methods 163: 205–209.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ito M, Takasaki T, Yamada K, Nerome R, Tajima S, Kurane I, 2004. Development and evaluation of fluorogenic TaqMan reverse transcriptase PCR assays for detection of dengue virus types 1 to 4. J Clin Microbiol 42: 5935–5937.
  • PubMed
    ItoMTakasakiTYamadaKNeromeRTajimaSKuraneI, 2004. Development and evaluation of fluorogenic TaqMan reverse transcriptase PCR assays for detection of dengue virus types 1 to 4. J Clin Microbiol 42: 5935–5937.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Moi ML, Lim CK, Chua KB, Takasaki T, Kurane I, 2012. Dengue virus infection-enhancing activity in serum samples with neutralizing activity as determined by using FcγR-expressing cells. PLoS Negl Trop Dis 6: e1536.
  • PubMed
    MoiMLLimCKChuaKBTakasakiTKuraneI, 2012. Dengue virus infection-enhancing activity in serum samples with neutralizing activity as determined by using FcγR-expressing cells. PLoS Negl Trop Dis 6: e1536.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ito M, Katakai Y, Ono F, Akari H, Mukai RZ, Takasaki T, Kotaki A, Kurane I, 2011. Serotype-specific and cross-reactive neutralizing antibody responses in cynomolgus monkeys after infection with multiple dengue virus serotypes. Arch Virol 156: 1073–1077.
  • PubMed
    ItoMKatakaiYOnoFAkariHMukaiRZTakasakiTKotakiAKuraneI, 2011. Serotype-specific and cross-reactive neutralizing antibody responses in cynomolgus monkeys after infection with multiple dengue virus serotypes. Arch Virol 156: 1073–1077.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Boonnak K, Slike BM, Donofrio GC, Marovich MA, 2013. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J Immunol 190: 5659–5665.
  • PubMed
    BoonnakKSlikeBMDonofrioGCMarovichMA, 2013. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J Immunol 190: 5659–5665.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chan KR, Ong EZ, Tan HC, Zhang SL, Zhang Q, Tang KF, Kaliaperumal N, Lim AP, Hibberd ML, Chan SH, Connolly JE, Krishnan MN, Lok SM, Hanson BJ, Lin CN, Ooi EE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2727.
  • PubMed
    ChanKROngEZTanHCZhangSLZhangQTangKFKaliaperumalNLimAPHibberdMLChanSHConnollyJEKrishnanMNLokSMHansonBJLinCNOoiEE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2727.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, Mahalingam S, Marovich MA, Ubol S, Mosser DM, 2010. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 10: 712–722.
  • PubMed
    HalsteadSBMahalingamSMarovichMAUbolSMosserDM, 2010. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 10: 712–722.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ubol S, Halstead SB, 2010. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin Vaccine Immunol 17: 1829–1835.
  • PubMed
    UbolSHalsteadSB, 2010. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin Vaccine Immunol 17: 1829–1835.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Ubol S, Phuklia W, Kalayanarooj S, Modhiran N, 2010. Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 201: 923–935.
  • PubMed
    UbolSPhukliaWKalayanaroojSModhiranN, 2010. Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 201: 923–935.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, 2009. Pathogenesis: Risk factors prior to infection. Halstead SB, Pasvol G, Hoffman SL, ed. Dengue (Tropical Medicine: Science and Practice). London, United Kingdom: Imperial College Press, 219–256.
  • PubMed
    HalsteadSB, 2009. Pathogenesis: Risk factors prior to infection. HalsteadSBPasvolGHoffmanSL, ed. Dengue (Tropical Medicine: Science and Practice). London, United Kingdom: Imperial College Press, 219–256.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halstead SB, 1979. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140: 527–533.
  • PubMed
    HalsteadSB, 1979. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140: 527–533.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. The Marmoset Genome Sequencing and Analysis Consortium, 2014. The common marmoset genome provides insight into primate biology and evolution. Nat Genet 46: 850–857.
  • PubMed
    The Marmoset Genome Sequencing and Analysis Consortium, 2014. The common marmoset genome provides insight into primate biology and evolution. Nat Genet 46: 850–857.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chan KR, Ong EZ, Tan HC, Zhang SL, Zhang Q, Tang KF, Kaliaperumal N, Lim AP, Hibberd ML, Chan SH, Connolly JE, Krishnan MN, Lok SM, Hanson BJ, Lin CN, Ooi EE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2777.
  • PubMed
    ChanKROngEZTanHCZhangSLZhangQTangKFKaliaperumalNLimAPHibberdMLChanSHConnollyJEKrishnanMNLokSMHansonBJLinCNOoiEE, 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 111: 2722–2777.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Nimmerjahn F, Lux A, 2014. LILR-B1 blocks activating FcγR signaling to allow antibody dependent enhancement of dengue virus infection. Proc Natl Acad Sci USA 111: 2404–2405.
  • PubMed
    NimmerjahnFLuxA, 2014. LILR-B1 blocks activating FcγR signaling to allow antibody dependent enhancement of dengue virus infection. Proc Natl Acad Sci USA 111: 2404–2405.
    )| false
  • Search Google Scholar
  • Export Citation

Save Email this content

Share Link

Copy this link, or click below to email it to a friend

Email this content

or copy the link directly:

The link was not copied. Your current browser may not support copying via this button.