1887

Journal of General Virology header logo

Volume 98, Issue 7

A relevant human model for the study of Zika virus antibody-dependent enhancement Free

Abstract

Zika virus (ZIKV) is a mosquito-borne flavivirus that has recently been responsible for a serious outbreak of disease in South and Central America. Infection with ZIKV has been associated with severe neurological symptoms and the development of microcephaly in unborn fetuses. Many of the regions involved in the current outbreak are known to be endemic for another flavivirus, dengue virus (DENV), which indicates that a large percentage of the population may have pre-existing DENV immunity. Thus, it is vital to investigate what impact pre-existing DENV immunity has on ZIKV infection. Here, we use primary human myeloid cells as a model for ZIKV enhancement in the presence of DENV antibodies. We show that sera containing DENV antibodies from individuals living in a DENV-endemic area are able to enhance ZIKV infection in a human macrophage-derived cell line and primary human macrophages. We also demonstrate altered pro-inflammatory cytokine production in macrophages with enhanced ZIKV infection. Our study indicates an important role for pre-existing DENV immunity on ZIKV infection in primary human immune cells and establishes a relevant model to study ZIKV antibody-dependent enhancement.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibody-dependent enhancement , Dengue immunity , macrophages , primary cell model and Zika virus
© 2017 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000833
2017-07-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/7/1702.html?itemId=/content/journal/jgv/10.1099/jgv.0.000833&mimeType=html&fmt=ahah

References

  1. Hayes EB. Zika virus outside Africa. Emerg Infect Dis 2009; 15:1347–1350 [View Article][PubMed]
     [Google Scholar]
  2. Grard G, Caron M, Mombo IM, Nkoghe D, Mboui Ondo S et al. Zika virus in Gabon (Central Africa) – 2007: a new threat from Aedes albopictus?. PLoS Negl Trop Dis 2014; 8:e2681 [View Article][PubMed]
     [Google Scholar]
  3. Fauci AS, Morens DM. Zika virus in the Americas—yet another Arbovirus threat. N Engl J Med 2016; 374:601–604 [View Article][PubMed]
     [Google Scholar]
  4. Oliveira Melo AS, Malinger G, Ximenes R, Szejnfeld PO, Alves Sampaio S et al. Zika virus intrauterine infection causes fetal brain abnormality and microcephaly: tip of the iceberg?. Ultrasound Obstet Gynecol 2016; 47:6–7 [View Article][PubMed]
     [Google Scholar]
  5. Schuler-Faccini L, Ribeiro EM, Feitosa IM, Horovitz DD, Cavalcanti DP et al. Possible association between Zika virus infection and microcephaly — Brazil, 2015. MMWR Morb Mortal Wkly Rep 2016; 65:59–62 [View Article][PubMed]
     [Google Scholar]
  6. Staples JE, Dziuban EJ, Fischer M, Cragan JD, Rasmussen SA et al. Interim guidelines for the evaluation and testing of Infants with possible congenital Zika virus infection — United States, 2016. MMWR Morb Mortal Wkly Rep 2016; 65:63–67 [View Article][PubMed]
     [Google Scholar]
  7. Martines RB, Bhatnagar J, Keating MK, Silva-Flannery L, Muehlenbachs A et al. Notes from the field: evidence of Zika virus infection in brain and placental tissues from two congenitally infected newborns and two fetal losses — Brazil, 2015. MMWR Morb Mortal Wkly Rep 2016; 65:159–160 [View Article][PubMed]
     [Google Scholar]
  8. Oehler E, Watrin L, Larre P, Leparc-Goffart I, Lastere S et al. Zika virus infection complicated by Guillain-Barre syndrome – case report, French Polynesia, December 2013. Euro Surveill 2014; 19:20720 [View Article][PubMed]
     [Google Scholar]
  9. Wise J. Study links Zika virus to Guillain-Barré syndrome. BMJ 2016; 352:i1242[PubMed] [CrossRef]
     [Google Scholar]
  10. Fagbami AH, Halstead SB, Marchette NJ, Larsen K. Cross-infection enhancement among African flaviviruses by immune mouse ascitic fluids. Cytobios 1987; 49:49–55[PubMed]
     [Google Scholar]
  11. Halstead SB, Porterfield JS, O'Rourke EJ. Enhancement of dengue virus infection in monocytes by flavivirus antisera. Am J Trop Med Hyg 1980; 29:638–642 [View Article][PubMed]
     [Google Scholar]
  12. Morens DM, Halstead SB, Marchette NJ. Profiles of antibody-dependent enhancement of dengue virus type 2 infection. Microb Pathog 1987; 3:231–237 [View Article][PubMed]
     [Google Scholar]
  13. Costa VV, Fagundes CT, Valadão DF, Ávila TV, Cisalpino D et al. Subversion of early innate antiviral responses during antibody-dependent enhancement of dengue virus infection induces severe disease in immunocompetent mice. Med Microbiol Immunol 2014; 203:231–250 [View Article][PubMed]
     [Google Scholar]
  14. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL et al. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 2010; 6:e1000790 [View Article][PubMed]
     [Google Scholar]
  15. Halstead SB, Mahalingam S, Marovich MA, Ubol S, Mosser DM. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 2010; 10:712–722 [View Article][PubMed]
     [Google Scholar]
  16. Priyamvada L, Quicke KM, Hudson WH, Onlamoon N, Sewatanon J et al. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc Natl Acad Sci USA 2016; 113:7852–7857 [View Article][PubMed]
     [Google Scholar]
  17. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A et al. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 2016; 353:823–826 [View Article][PubMed]
     [Google Scholar]
  18. Kawiecki AB, Christofferson RC. Zika virus–induced antibody response enhances dengue virus serotype 2 replication in vitro. J Infect Dis 2016; 214:1357–1360 [View Article][PubMed]
     [Google Scholar]
  19. Dai L, Song J, Lu X, Deng YQ, Musyoki AM et al. Structures of the Zika virus envelope protein and its complex with a flavivirus broadly protective antibody. Cell Host Microbe 2016; 19:696–704 [View Article][PubMed]
     [Google Scholar]
  20. Barba-Spaeth G, Dejnirattisai W, Rouvinski A, Vaney MC, Medits I et al. Structural basis of potent Zika–dengue virus antibody cross-neutralization. Nature 2016; 536:48–53 [View Article][PubMed]
     [Google Scholar]
  21. Halstead SB. Dengue antibody-dependent enhancement: knowns and unknowns. Microbiol Spectr 2014; 2: [View Article][PubMed]
     [Google Scholar]
  22. Quicke KM, Bowen JR, Johnson EL, McDonald CE, Ma H et al. Zika virus infects human placental macrophages. Cell Host Microbe 2016; 20:83–90 [View Article][PubMed]
     [Google Scholar]
  23. Chen RF, Wang L, Cheng JT, Yang KD. Induction of IFNα or IL-12 depends on differentiation of THP-1 cells in dengue infections without and with antibody enhancement. BMC Infect Dis 2012; 12:340 [View Article][PubMed]
     [Google Scholar]
  24. Cao-Lormeau VM, Blake A, Mons S, Lastère S, Roche C et al. Guillain-Barré syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 2016; 387:1531–1539 [View Article][PubMed]
     [Google Scholar]
  25. Araúz D, de Urriola L, Jones J, Castillo M, Martínez A et al. Febrile or exanthematous illness associated with Zika, dengue, and chikungunya viruses, Panama. Emerg Infect Dis 2016; 22:1515–1517 [View Article][PubMed]
     [Google Scholar]
  26. Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with Zika virus. Nat Immunol 2016; 17:1102–1108 [View Article][PubMed]
     [Google Scholar]
  27. Harrison SC. Immunogenic cross-talk between dengue and Zika viruses. Nat Immunol 2016; 17:1010–1012 [View Article][PubMed]
     [Google Scholar]
  28. Swanstrom JA, Plante JA, Plante KS, Young EF, McGowan E et al. Dengue virus envelope dimer epitope monoclonal antibodies isolated from dengue patients are protective against Zika virus. MBio 2016; 7:e01123-16 [View Article][PubMed]
     [Google Scholar]
  29. Paul LM, Carlin ER, Jenkins MM, Tan AL, Barcellona CM et al. Dengue virus antibodies enhance Zika virus infection. Clin Transl Immunology 2016; 5:e117 [View Article][PubMed]
     [Google Scholar]
  30. Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 2002; 10:100–103 [View Article][PubMed]
     [Google Scholar]
  31. Burke DS, Kliks S. Antibody-dependent enhancement in dengue virus infections. J Infect Dis 2006; 193:601–603 [View Article][PubMed]
     [Google Scholar]
  32. Mackenzie JS, Gubler DJ, Petersen LR. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 2004; 10:S98–S109 [View Article][PubMed]
     [Google Scholar]
  33. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J et al. Dengue: a continuing global threat. Nat Rev Microbiol 2010; 8:S7–S16 [View Article][PubMed]
     [Google Scholar]
  34. Murray KO, Rodriguez LF, Herrington E, Kharat V, Vasilakis N et al. Identification of dengue fever cases in Houston, Texas, with evidence of autochthonous transmission between 2003 and 2005. Vector Borne Zoonotic Dis 2013; 13:835–845 [View Article][PubMed]
     [Google Scholar]
  35. Muñoz-Jordán JL, Santiago GA, Margolis H, Stark L. Genetic relatedness of dengue viruses in Key West, Florida, USA, 2009-2010. Emerg Infect Dis 2013; 19:652–654 [View Article][PubMed]
     [Google Scholar]
  36. Hall WC, Crowell TP, Watts DM, Barros VL, Kruger H et al. Demonstration of yellow fever and dengue antigens in formalin-fixed paraffin-embedded human liver by immunohistochemical analysis. Am J Trop Med Hyg 1991; 45:408–417 [View Article][PubMed]
     [Google Scholar]
  37. Bhoopat L, Bhamarapravati N, Attasiri C, Yoksarn S, Chaiwun B et al. Immunohistochemical characterization of a new monoclonal antibody reactive with dengue virus-infected cells in frozen tissue using immunoperoxidase technique. Asian Pac J Allergy Immunol 1996; 14:107–113[PubMed]
     [Google Scholar]
  38. Puerta-Guardo H, Raya-Sandino A, González-Mariscal L, Rosales VH, Ayala-Dávila J et al. The cytokine response of U937-derived macrophages infected through antibody-dependent enhancement of dengue virus disrupts cell apical-junction complexes and increases vascular permeability. J Virol 2013; 87:7486–7501 [View Article][PubMed]
     [Google Scholar]
  39. Tsai TT, Chuang YJ, Lin YS, Chang CP, Wan SW et al. Antibody-dependent enhancement infection facilitates dengue virus-regulated signaling of IL-10 production in monocytes. PLoS Negl Trop Dis 2014; 8:e3320 [View Article][PubMed]
     [Google Scholar]
  40. Rolph MS, Zaid A, Rulli NE, Mahalingam S. Downregulation of interferon-β in antibody-dependent enhancement of dengue viral infections of human macrophages is dependent on interleukin-6. J Infect Dis 2011; 204:489–491 [View Article][PubMed]
     [Google Scholar]
  41. Dong T, Moran E, Vinh Chau N, Simmons C, Luhn K et al. High pro-inflammatory cytokine secretion and loss of high avidity cross-reactive cytotoxic T-cells during the course of secondary dengue virus infection. PLoS One 2007; 2:e1192 [View Article][PubMed]
     [Google Scholar]
  42. Krishnamurthy PK, Deng Y, Sigurdsson EM. Mechanistic studies of antibody-mediated clearance of Tau aggregates using an ex vivo brain slice model. Front Psychiatry 2011; 2:59 [View Article][PubMed]
     [Google Scholar]
  43. Huang X, Yue Y, Li D, Zhao Y, Qiu L et al. Antibody-dependent enhancement of dengue virus infection inhibits RLR-mediated Type-I IFN-independent signalling through upregulation of cellular autophagy. Sci Rep 2016; 6:22303 [View Article][PubMed]
     [Google Scholar]
  44. Masliah E, Rockenstein E, Adame A, Alford M, Crews L et al. Effects of α-synuclein immunization in a mouse model of Parkinson's disease. Neuron 2005; 46:857–868 [View Article][PubMed]
     [Google Scholar]
  45. Tampellini D, Magrané J, Takahashi RH, Li F, Lin MT et al. Internalized antibodies to the Aβ domain of APP reduce neuronal Aβ and protect against synaptic alterations. J Biol Chem 2007; 282:18895–18906 [View Article][PubMed]
     [Google Scholar]
  46. Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 2005; 3:e156 [View Article][PubMed]
     [Google Scholar]
  47. Govindarajan D, Guan L, Meschino S, Fridman A, Bagchi A et al. A rapid and improved method to generate recombinant dengue virus vaccine candidates. PLoS One 2016; 11:e0152209 [View Article][PubMed]
     [Google Scholar]
  48. Londono-Renteria B, Drame PM, Weitzel T, Rosas R, Gripping C et al. An. gambiae gSG6-P1 evaluation as a proxy for human-vector contact in the Americas: a pilot study. Parasit Vectors 2015; 8:533 [View Article][PubMed]
     [Google Scholar]
  49. Colpitts TM, Cox J, Nguyen A, Feitosa F, Krishnan MN et al. Use of a tandem affinity purification assay to detect interactions between West Nile and dengue viral proteins and proteins of the mosquito vector. Virology 2011; 417:179–187 [View Article][PubMed]
     [Google Scholar]
  50. Colpitts TM, Barthel S, Wang P, Fikrig E. Dengue virus capsid protein binds core histones and inhibits nucleosome formation in human liver cells. PLoS One 2011; 6:e24365 [View Article][PubMed]
     [Google Scholar]
  51. Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 2008; 14:1232–1239 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000833
Loading
A relevant in vitro human model for the study of Zika virus antibody-dependent enhancement
J. Gen. Virol. 98, 1702 (2017); https://doi.org/10.1099/jgv.0.000833
/content/journal/jgv/10.1099/jgv.0.000833
/content/journal/jgv/10.1099/jgv.0.000833
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error