Pre-Existing Dengue Immunity Drives a DENV-Biased Plasmablast Response in ZIKV-Infected Patient
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients
2.2. Viruses, Viral Antigens and Recombinant Proteins
2.3. ELISpot Assay
2.4. Flow Cytometry and Single-Cell Sorting of Plasmablasts
2.5. Monoclonal Antibody Production
2.6. Ig Variable Chain Repertoire and Clonality Analysis
2.7. ELISA
2.8. Antibody Competition ELISA
2.9. Focus Reduction Neutralization Test
2.10. Antibody Dependent Enhancement Assay
3. Results
3.1. ZIKV Infection Induces Strong Recall Response in Flavivirus-Experienced Individual
3.2. Robust Plasmablast Response Following ZIKV Infection
3.3. Recall Response Drives Expansion of Clonally-Linked, Cross-Reactive Plasmablasts
3.4. Primary and Recall ZIKV Plasmablast Responses Differ in Frequency and Breadth of Cross-Reactivity.
3.5. Neutralization Bias towards DENV Observed in ZIKV Plasmablast Response of Dengue-Experienced Patient
3.6. Potent Antibody-Dependent Enhancement of ZIKV by ZK016 mAbs
3.7. NS1 Protein Targeted by Type-Specific and Cross-Reactive ZIKV Plasmablasts
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Duffy, M.R.; Chen, T.H.; Hancock, W.T.; Powers, A.M.; Kool, J.L.; Lanciotti, R.S.; Pretrick, M.; Marfel, M.; Holzbauer, S.; Dubray, C.; et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 2009, 360, 2536–2543. [Google Scholar] [CrossRef] [PubMed]
- Cao-Lormeau, V.M.; Roche, C.; Teissier, A.; Robin, E.; Berry, A.L.; Mallet, H.P.; Sall, A.A.; Musso, D. Zika virus, French polynesia, South pacific, 2013. Emerg. Infect. Dis. 2014, 20, 1085–1086. [Google Scholar] [CrossRef] [PubMed]
- Gatherer, D.; Kohl, A. Zika virus: A previously slow pandemic spreads rapidly through the Americas. J. Gen. Virol. 2016, 97, 269–273. [Google Scholar] [CrossRef] [PubMed]
- Plourde, A.R.; Bloch, E.M. A Literature Review of Zika Virus. Emerg. Infect. Dis. 2016, 22, 1185–1192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Styczynski, A.R.; Malta, J.; Krow-Lucal, E.R.; Percio, J.; Nobrega, M.E.; Vargas, A.; Lanzieri, T.M.; Leite, P.L.; Staples, J.E.; Fischer, M.X.; et al. Increased rates of Guillain-Barre syndrome associated with Zika virus outbreak in the Salvador metropolitan area, Brazil. PLoS Negl. Trop. Dis. 2017, 11, e0005869. [Google Scholar] [CrossRef] [PubMed]
- Leal, M.C.; van der Linden, V.; Bezerra, T.P.; de Valois, L.; Borges, A.C.G.; Antunes, M.M.C.; Brandt, K.G.; Moura, C.X.; Rodrigues, L.C.; Ximenes, C.R. Characteristics of Dysphagia in Infants with Microcephaly Caused by Congenital Zika Virus Infection, Brazil, 2015. Emerg. Infect. Dis. 2017, 23, 1253–1259. [Google Scholar] [CrossRef] [PubMed]
- Aragao, M.; Holanda, A.C.; Brainer-Lima, A.M.; Petribu, N.C.L.; Castillo, M.; van der Linden, V.; Serpa, S.C.; Tenorio, A.G.; Travassos, P.T.C.; Cordeiro, M.T.; et al. Nonmicrocephalic Infants with Congenital Zika Syndrome Suspected Only after Neuroimaging Evaluation Compared with Those with Microcephaly at Birth and Postnatally: How Large Is the Zika Virus "Iceberg"? AJNR Am. J. Neuroradiol. 2017, 38, 1427–1434. [Google Scholar] [CrossRef] [PubMed]
- Krauer, F.; Riesen, M.; Reveiz, L.; Oladapo, O.T.; Martinez-Vega, R.; Porgo, T.V.; Haefliger, A.; Broutet, N.J.; Low, N. Zika Virus Infection as a Cause of Congenital Brain Abnormalities and Guillain-Barre Syndrome: Systematic Review. PLoS Med. 2017, 14, e1002203. [Google Scholar] [CrossRef]
- Fagbami, A.H. Zika virus infections in Nigeria: Virological and seroepidemiological investigations in Oyo State. J. Hyg. (Lond.) 1979, 83, 213–219. [Google Scholar] [CrossRef]
- Hayes, E.B. Zika virus outside Africa. Emerg. Infect. Dis. 2009, 15, 1347–1350. [Google Scholar] [CrossRef]
- Lim, S.K.; Lim, J.K.; Yoon, I.K. An Update on Zika Virus in Asia. Infect. Chemother. 2017, 49, 91–100. [Google Scholar] [CrossRef]
- Sirohi, D.; Chen, Z.; Sun, L.; Klose, T.; Pierson, T.C.; Rossmann, M.G.; Kuhn, R.J. The 3.8 A resolution cryo-EM structure of Zika virus. Science 2016, 352, 467–470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Priyamvada, L.; Quicke, K.M.; Hudson, W.H.; Onlamoon, N.; Sewatanon, J.; Edupuganti, S.; Pattanapanyasat, K.; Chokephaibulkit, K.; Mulligan, M.J.; Wilson, P.C.; 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. [Google Scholar] [CrossRef] [PubMed]
- Musso, D.; Cao-Lormeau, V.M.; Gubler, D.J. Zika virus: Following the path of dengue and chikungunya? Lancet 2015, 386, 243–244. [Google Scholar] [CrossRef]
- Rodriguez-Morales, A.J.; Villamil-Gomez, W.E.; Franco-Paredes, C. The arboviral burden of disease caused by co-circulation and co-infection of dengue, chikungunya and Zika in the Americas. Travel. Med. Infect. Dis. 2016, 14, 177–179. [Google Scholar] [CrossRef] [PubMed]
- Ribeiro, L.S.; Marques, R.E.; Jesus, A.M.; Almeida, R.P.; Teixeira, M.M. Zika crisis in Brazil: Challenges in research and development. Curr. Opin. Virol. 2016, 18, 76–81. [Google Scholar] [CrossRef] [PubMed]
- Moi, M.L.; Takasaki, T.; Kurane, I. Efficacy of tetravalent dengue vaccine in Thai schoolchildren. Lancet 2013, 381, 1094. [Google Scholar] [CrossRef]
- Halstead, S.B. Achieving safe, effective, and durable Zika virus vaccines: Lessons from dengue. Lancet Infect. Dis. 2017, 17, e378–e382. [Google Scholar] [CrossRef]
- Swanstrom, J.A.; Plante, J.A.; Plante, K.S.; Young, E.F.; McGowan, E.; Gallichotte, E.N.; Widman, D.G.; Heise, M.T.; de Silva, A.M.; Baric, R.S. Dengue Virus Envelope Dimer Epitope Monoclonal Antibodies Isolated from Dengue Patients Are Protective against Zika Virus. MBio 2016, 7, e01123-16. [Google Scholar] [CrossRef]
- Stettler, K.; Beltramello, M.; Espinosa, D.A.; Graham, V.; Cassotta, A.; Bianchi, S.; Vanzetta, F.; Minola, A.; Jaconi, S.; Mele, F.; et al. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 2016, 353, 823–826. [Google Scholar] [CrossRef] [Green Version]
- Rogers, T.F.; Goodwin, E.C.; Briney, B.; Sok, D.; Beutler, N.; Strubel, A.; Nedellec, R.; Le, K.; Brown, M.E.; Burton, D.R.; et al. Zika virus activates de novo and cross-reactive memory B cell responses in dengue-experienced donors. Sci. Immunol. 2017, 2, eaan6809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barba-Spaeth, G.; Dejnirattisai, W.; Rouvinski, A.; Vaney, M.C.; Medits, I.; Sharma, A.; Simon-Loriere, E.; Sakuntabhai, A.; Cao-Lormeau, V.M.; Haouz, A.; et al. Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nature 2016, 536, 48–53. [Google Scholar] [CrossRef]
- Dejnirattisai, W.; Supasa, P.; Wongwiwat, W.; Rouvinski, A.; Barba-Spaeth, G.; Duangchinda, T.; Sakuntabhai, A.; Cao-Lormeau, V.M.; Malasit, P.; Rey, F.A.; et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat. Immunol. 2016, 17, 1102–1108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sapparapu, G.; Fernandez, E.; Kose, N.; Bin, C.; Fox, J.M.; Bombardi, R.G.; Zhao, H.; Nelson, C.A.; Bryan, A.L.; Barnes, T.; et al. Neutralizing human antibodies prevent Zika virus replication and fetal disease in mice. Nature 2016, 540, 443–447. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magnani, D.M.; Rogers, T.F.; Beutler, N.; Ricciardi, M.J.; Bailey, V.K.; Gonzalez-Nieto, L.; Briney, B.; Sok, D.; Le, K.; Strubel, A.; et al. Neutralizing human monoclonal antibodies prevent Zika virus infection in macaques. Sci. Transl. Med. 2017, 9, eaan8184. [Google Scholar] [CrossRef] [PubMed]
- Barrett, A.D.T. Current status of Zika vaccine development: Zika vaccines advance into clinical evaluation. NPJ Vaccines 2018, 3, 24. [Google Scholar] [CrossRef]
- Barouch, D.H.; Thomas, S.J.; Michael, N.L. Prospects for a Zika Virus Vaccine. Immunity 2017, 46, 176–182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halstead, S.B.; Marchette, N.J.; Sung Chow, J.S.; Lolekha, S. Dengue virus replication enhancement in peripheral blood leukocytes from immune human beings. Proc. Soc. Exp. Biol. Med. 1976, 151, 136–139. [Google Scholar] [CrossRef]
- Halstead, S.B. Biologic Evidence Required for Zika Disease Enhancement by Dengue Antibodies. Emerg. Infect. Dis. 2017, 23, 569–573. [Google Scholar] [CrossRef] [Green Version]
- Durbin, A.P. Dengue Antibody and Zika: Friend or Foe? Trends Immunol. 2016, 37, 635–636. [Google Scholar] [CrossRef]
- Lai, L.; Rouphael, N.; Xu, Y.; Natrajan, M.S.; Beck, A.; Hart, M.; Feldhammer, M.; Feldpausch, A.; Hill, C.; Wu, H.; et al. Innate, T and B Cell Responses in Acute Human Zika Patients. Clin. Infect. Dis. 2017, 66, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Ricciardi, M.J.; Magnani, D.M.; Grifoni, A.; Kwon, Y.C.; Gutman, M.J.; Grubaugh, N.D.; Gangavarapu, K.; Sharkey, M.; Silveira, C.G.T.; Bailey, V.K.; et al. Ontogeny of the B- and T-cell response in a primary Zika virus infection of a dengue-naive individual during the 2016 outbreak in Miami, FL. PLoS Negl. Trop. Dis. 2017, 11, e0006000. [Google Scholar] [CrossRef] [PubMed]
- Priyamvada, L.; Cho, A.; Onlamoon, N.; Zheng, N.Y.; Huang, M.; Kovalenkov, Y.; Chokephaibulkit, K.; Angkasekwinai, N.; Pattanapanyasat, K.; Ahmed, R.; et al. B Cell Responses during Secondary Dengue Virus Infection Are Dominated by Highly Cross-Reactive, Memory-Derived Plasmablasts. J. Virol. 2016, 90, 5574–5585. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, K.; Garman, L.; Wrammert, J.; Zheng, N.Y.; Capra, J.D.; Ahmed, R.; Wilson, P.C. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat. Protoc. 2009, 4, 372–384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wrammert, J.; Smith, K.; Miller, J.; Langley, W.A.; Kokko, K.; Larsen, C.; Zheng, N.Y.; Mays, I.; Garman, L.; Helms, C.; et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 2008, 453, 667–671. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kauffman, R.C.; Bhuiyan, T.R.; Nakajima, R.; Mayo-Smith, L.M.; Rashu, R.; Hoq, M.R.; Chowdhury, F.; Khan, A.I.; Rahman, A.; Bhaumik, S.K.; et al. Single-Cell Analysis of the Plasmablast Response to Vibrio cholerae Demonstrates Expansion of Cross-Reactive Memory B Cells. MBio 2016, 7, e02021-16. [Google Scholar] [CrossRef] [PubMed]
- Rabe, I.B.; Staples, J.E.; Villanueva, J.; Hummel, K.B.; Johnson, J.A.; Rose, L.; Hills, S.; Wasley, A.; Fischer, M.; Powers, A.M. Interim Guidance for Interpretation of Zika Virus Antibody Test Results. MMWR Morb. Mortal. Wkly. Rep. 2016, 65, 543–546. [Google Scholar] [CrossRef]
- Zika MAC-ELISA. Available online: https://www.cdc.gov/zika/pdfs/zika-mac-elisa-instructions-for-use.pdf (accessed on 15 July 2018).
- Lanciotti, R.S.; Kosoy, O.L.; Laven, J.J.; Velez, J.O.; Lambert, A.J.; Johnson, A.J.; Stanfield, S.M.; Duffy, M.R. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg. Infect. Dis. 2008, 14, 1232–1239. [Google Scholar] [CrossRef]
- Costin, J.M.; Zaitseva, E.; Kahle, K.M.; Nicholson, C.O.; Rowe, D.K.; Graham, A.S.; Bazzone, L.E.; Hogancamp, G.; Figueroa Sierra, M.; Fong, R.H.; et al. Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop. J. Virol. 2013, 87, 52–66. [Google Scholar] [CrossRef]
- Oliphant, T.; Nybakken, G.E.; Engle, M.; Xu, Q.; Nelson, C.A.; Sukupolvi-Petty, S.; Marri, A.; Lachmi, B.E.; Olshevsky, U.; Fremont, D.H.; et al. Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J. Virol. 2006, 80, 12149–12159. [Google Scholar] [CrossRef]
- Pauli, N.T.; Kim, H.K.; Falugi, F.; Huang, M.; Dulac, J.; Henry Dunand, C.; Zheng, N.Y.; Kaur, K.; Andrews, S.F.; Huang, Y.; et al. Staphylococcus aureus infection induces protein A-mediated immune evasion in humans. J. Exp. Med. 2014, 211, 2331–2339. [Google Scholar] [CrossRef] [PubMed]
- Halstead, S.B. Dengue Antibody-Dependent Enhancement: Knowns and Unknowns. Microbiol. Spectr. 2014, 2, 249–271. [Google Scholar] [Green Version]
- Zimmerman, M.G.; Quicke, K.M.; O'Neal, J.T.; Arora, N.; Machiah, D.; Priyamvada, L.; Kauffman, R.C.; Register, E.; Adekunle, O.; Swieboda, D.; et al. Cross-Reactive Dengue Virus Antibodies Augment Zika Virus Infection of Human Placental Macrophages. Cell Host Microbe 2018, 24, 731–742. [Google Scholar] [CrossRef] [PubMed]
- Fowler, A.M.; Tang, W.W.; Young, M.P.; Mamidi, A.; Viramontes, K.M.; McCauley, M.D.; Carlin, A.F.; Schooley, R.T.; Swanstrom, J.; Baric, R.S.; et al. Maternally Acquired Zika Antibodies Enhance Dengue Disease Severity in Mice. Cell Host Microbe 2018, 24, 743–750. [Google Scholar] [CrossRef] [PubMed]
- Priyamvada, L.; Hudson, W.; Ahmed, R.; Wrammert, J. Humoral cross-reactivity between Zika and dengue viruses: Implications for protection and pathology. Emerg. Microbes Infect. 2017, 6, e33. [Google Scholar] [CrossRef] [PubMed]
- Sirohi, D.; Kuhn, R.J. Zika Virus Structure, Maturation, and Receptors. J. Infect. Dis. 2017, 216, S935–S944. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shi, Y.; Dai, L.; Song, H.; Gao, G.F. Structures of Zika Virus E & NS1: Relations with Virus Infection and Host Immune Responses. Adv. Exp. Med. Biol. 2018, 1062, 77–87. [Google Scholar]
- Kostyuchenko, V.A.; Lim, E.X.; Zhang, S.; Fibriansah, G.; Ng, T.S.; Ooi, J.S.; Shi, J.; Lok, S.M. Structure of the thermally stable Zika virus. Nature 2016, 533, 425–428. [Google Scholar] [CrossRef] [Green Version]
- Dowd, K.A.; DeMaso, C.R.; Pierson, T.C. Genotypic Differences in Dengue Virus Neutralization Are Explained by a Single Amino Acid Mutation That Modulates Virus Breathing. MBio 2015, 6, e01559-15. [Google Scholar] [CrossRef]
- Watanabe, S.; Tan, N.W.W.; Chan, K.W.K.; Vasudevan, S.G. Dengue and Zika Virus Serological Cross-reactivity and their Impact on Pathogenesis in Mice. J. Infect. Dis. 2018. [Google Scholar] [CrossRef]
- Song, H.; Qi, J.; Haywood, J.; Shi, Y.; Gao, G.F. Zika virus NS1 structure reveals diversity of electrostatic surfaces among flaviviruses. Nat. Struct. Mol. Biol. 2016, 23, 456–458. [Google Scholar] [CrossRef] [PubMed]
- Freire, M.; Pol-Fachin, L.; Coelho, D.F.; Viana, I.F.T.; Magalhaes, T.; Cordeiro, M.T.; Fischer, N.; Loeffler, F.F.; Jaenisch, T.; Franca, R.F.; et al. Mapping Putative B-Cell Zika Virus NS1 Epitopes Provides Molecular Basis for Anti-NS1 Antibody Discrimination between Zika and Dengue Viruses. ACS Omega 2017, 2, 3913–3920. [Google Scholar] [CrossRef] [PubMed]
- Brown, W.C.; Akey, D.L.; Konwerski, J.R.; Tarrasch, J.T.; Skiniotis, G.; Kuhn, R.J.; Smith, J.L. Extended surface for membrane association in Zika virus NS1 structure. Nat. Struct. Mol. Biol. 2016, 23, 865–867. [Google Scholar] [CrossRef] [PubMed]
Patient | Age/Sex | Region of ZIKV | Plasmablasts Analyzed | Previous Dengue |
---|---|---|---|---|
Exposure | (DPO *) | Exposure ** | ||
ZK016 | 32/Female | Honduras | 3, 7 | Yes |
ZK018 | 26/Female | Caribbean Islands | 8 | No |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bhaumik, S.K.; Priyamvada, L.; Kauffman, R.C.; Lai, L.; Natrajan, M.S.; Cho, A.; Rouphael, N.; Suthar, M.S.; Mulligan, M.J.; Wrammert, J. Pre-Existing Dengue Immunity Drives a DENV-Biased Plasmablast Response in ZIKV-Infected Patient. Viruses 2019, 11, 19. https://doi.org/10.3390/v11010019
Bhaumik SK, Priyamvada L, Kauffman RC, Lai L, Natrajan MS, Cho A, Rouphael N, Suthar MS, Mulligan MJ, Wrammert J. Pre-Existing Dengue Immunity Drives a DENV-Biased Plasmablast Response in ZIKV-Infected Patient. Viruses. 2019; 11(1):19. https://doi.org/10.3390/v11010019
Chicago/Turabian StyleBhaumik, Siddhartha K., Lalita Priyamvada, Robert C. Kauffman, Lilin Lai, Muktha S. Natrajan, Alice Cho, Nadine Rouphael, Mehul S. Suthar, Mark J. Mulligan, and Jens Wrammert. 2019. "Pre-Existing Dengue Immunity Drives a DENV-Biased Plasmablast Response in ZIKV-Infected Patient" Viruses 11, no. 1: 19. https://doi.org/10.3390/v11010019
APA StyleBhaumik, S. K., Priyamvada, L., Kauffman, R. C., Lai, L., Natrajan, M. S., Cho, A., Rouphael, N., Suthar, M. S., Mulligan, M. J., & Wrammert, J. (2019). Pre-Existing Dengue Immunity Drives a DENV-Biased Plasmablast Response in ZIKV-Infected Patient. Viruses, 11(1), 19. https://doi.org/10.3390/v11010019