Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor

Vincent Dussupt; Rajeshwer S. Sankhala; Gregory D. Gromowski; Gina Donofrio; Rafael A. De La Barrera; Rafael A. Larocca; Weam Zaky; Letzibeth Mendez-Rivera; Misook Choe; Edgar Davidson; Michael K. McCracken; James D. Brien; Peter Abbink; Hongjun Bai; Aubrey L. Bryan; Candace Hope Bias; Irina Maljkovic Berry; Nubia Botero; Tanya Cook; Nicole A. Doria-Rose; Ariadna Grinyo i. Escuer; Justice Akuoku Frimpong; Aviva Geretz; Mayda Hernandez; Bradley S. Hollidge; Ningbo Jian; Kareem Kabra; David J. Leggat; Jinyan Liu; Amelia K. Pinto; Wiriya Rutvisuttinunt; Ian Setliff; Ursula Tran; Samantha Townsley; Benjamin J. Doranz; Morgane Rolland; Adrian B. McDermott; Ivelin S. Georgiev; Rasmi Thomas; Merlin L. Robb; Kenneth H. Eckels; Elizabeth Barranco; Michael Koren; Darci R. Smith; Richard G. Jarman; Sarah L. George; Kathryn E. Stephenson; Dan H. Barouch; Kayvon Modjarrad; Nelson L. Michael; M. Gordon Joyce; Shelly J. Krebs

doi:10.1038/s41591-019-0746-2

Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor

Vincent Dussupt, Rajeshwer S. Sankhala, Gregory D. Gromowski, Gina Donofrio, Rafael A. De La Barrera, Rafael A. Larocca, Weam Zaky, Letzibeth Mendez-Rivera, Misook Choe, Edgar Davidson, Michael K. McCracken, James D. Brien, Peter Abbink, Hongjun Bai, Aubrey L. Bryan, Candace Hope Bias, Irina Maljkovic Berry, Nubia Botero, Tanya Cook, Nicole A. Doria-RoseAriadna Grinyo i. Escuer, Justice Akuoku Frimpong, Aviva Geretz, Mayda Hernandez, Bradley S. Hollidge, Ningbo Jian, Kareem Kabra, David J. Leggat, Jinyan Liu, Amelia K. Pinto, Wiriya Rutvisuttinunt, Ian Setliff, Ursula Tran, Samantha Townsley, Benjamin J. Doranz, Morgane Rolland, Adrian B. McDermott, Ivelin S. Georgiev, Rasmi Thomas, Merlin L. Robb, Kenneth H. Eckels, Elizabeth Barranco, Michael Koren, Darci R. Smith, Richard G. Jarman, Sarah L. George, Kathryn E. Stephenson, Dan H. Barouch, Kayvon Modjarrad, Nelson L. Michael, M. Gordon Joyce^*, Shelly J. Krebs

^*Corresponding author for this work

Research output: Contribution to journal › Letter › peer-review

58 Scopus citations

Abstract

Zika virus (ZIKV) has caused significant disease, with widespread cases of neurological pathology and congenital neurologic defects. Rapid vaccine development has led to a number of candidates capable of eliciting potent ZIKV-neutralizing antibodies (reviewed in refs. ^1–3). Despite advances in vaccine development, it remains unclear how ZIKV vaccination affects immune responses in humans with prior flavivirus immunity. Here we show that a single-dose immunization of ZIKV purified inactivated vaccine (ZPIV)^4–7 in a dengue virus (DENV)-experienced human elicited potent cross-neutralizing antibodies to both ZIKV and DENV. Using a unique ZIKV virion-based sorting strategy, we isolated and characterized multiple antibodies, including one termed MZ4, which targets a novel site of vulnerability centered on the Envelope (E) domain I/III linker region and protects mice from viremia and viral dissemination following ZIKV or DENV-2 challenge. These data demonstrate that Zika vaccination in a DENV-experienced individual can boost pre-existing flavivirus immunity and elicit protective responses against both ZIKV and DENV. ZPIV vaccination in Puerto Rican individuals with prior flavivirus experience yielded similar cross-neutralizing potency after a single vaccination, highlighting the potential benefit of ZIKV vaccination in flavivirus-endemic areas.

Original language	English
Pages (from-to)	228-235
Number of pages	8
Journal	Nature Medicine
Volume	26
Issue number	2
DOIs	https://doi.org/10.1038/s41591-019-0746-2
State	Published - 1 Feb 2020
Externally published	Yes

Access to Document

10.1038/s41591-019-0746-2

Cite this

Dussupt, V., Sankhala, R. S., Gromowski, G. D., Donofrio, G., De La Barrera, R. A., Larocca, R. A., Zaky, W., Mendez-Rivera, L., Choe, M., Davidson, E., McCracken, M. K., Brien, J. D., Abbink, P., Bai, H., Bryan, A. L., Bias, C. H., Berry, I. M., Botero, N., Cook, T., ... Krebs, S. J. (2020). Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor. Nature Medicine, 26(2), 228-235. https://doi.org/10.1038/s41591-019-0746-2

@article{1117cf12b9aa40fa8c2dfb6e45893d8c,

title = "Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor",

abstract = "Zika virus (ZIKV) has caused significant disease, with widespread cases of neurological pathology and congenital neurologic defects. Rapid vaccine development has led to a number of candidates capable of eliciting potent ZIKV-neutralizing antibodies (reviewed in refs. 1–3). Despite advances in vaccine development, it remains unclear how ZIKV vaccination affects immune responses in humans with prior flavivirus immunity. Here we show that a single-dose immunization of ZIKV purified inactivated vaccine (ZPIV)4–7 in a dengue virus (DENV)-experienced human elicited potent cross-neutralizing antibodies to both ZIKV and DENV. Using a unique ZIKV virion-based sorting strategy, we isolated and characterized multiple antibodies, including one termed MZ4, which targets a novel site of vulnerability centered on the Envelope (E) domain I/III linker region and protects mice from viremia and viral dissemination following ZIKV or DENV-2 challenge. These data demonstrate that Zika vaccination in a DENV-experienced individual can boost pre-existing flavivirus immunity and elicit protective responses against both ZIKV and DENV. ZPIV vaccination in Puerto Rican individuals with prior flavivirus experience yielded similar cross-neutralizing potency after a single vaccination, highlighting the potential benefit of ZIKV vaccination in flavivirus-endemic areas.",

author = "Vincent Dussupt and Sankhala, {Rajeshwer S.} and Gromowski, {Gregory D.} and Gina Donofrio and {De La Barrera}, {Rafael A.} and Larocca, {Rafael A.} and Weam Zaky and Letzibeth Mendez-Rivera and Misook Choe and Edgar Davidson and McCracken, {Michael K.} and Brien, {James D.} and Peter Abbink and Hongjun Bai and Bryan, {Aubrey L.} and Bias, {Candace Hope} and Berry, {Irina Maljkovic} and Nubia Botero and Tanya Cook and Doria-Rose, {Nicole A.} and Escuer, {Ariadna Grinyo i.} and Frimpong, {Justice Akuoku} and Aviva Geretz and Mayda Hernandez and Hollidge, {Bradley S.} and Ningbo Jian and Kareem Kabra and Leggat, {David J.} and Jinyan Liu and Pinto, {Amelia K.} and Wiriya Rutvisuttinunt and Ian Setliff and Ursula Tran and Samantha Townsley and Doranz, {Benjamin J.} and Morgane Rolland and McDermott, {Adrian B.} and Georgiev, {Ivelin S.} and Rasmi Thomas and Robb, {Merlin L.} and Eckels, {Kenneth H.} and Elizabeth Barranco and Michael Koren and Smith, {Darci R.} and Jarman, {Richard G.} and George, {Sarah L.} and Stephenson, {Kathryn E.} and Barouch, {Dan H.} and Kayvon Modjarrad and Michael, {Nelson L.} and Joyce, {M. Gordon} and Krebs, {Shelly J.}",

note = "Publisher Copyright: {\textcopyright} 2020, This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.",

year = "2020",

month = feb,

day = "1",

doi = "10.1038/s41591-019-0746-2",

language = "English",

volume = "26",

pages = "228--235",

journal = "Nature Medicine",

issn = "1078-8956",

number = "2",

}

Dussupt, V, Sankhala, RS, Gromowski, GD, Donofrio, G, De La Barrera, RA, Larocca, RA, Zaky, W, Mendez-Rivera, L, Choe, M, Davidson, E, McCracken, MK, Brien, JD, Abbink, P, Bai, H, Bryan, AL, Bias, CH, Berry, IM, Botero, N, Cook, T, Doria-Rose, NA, Escuer, AGI, Frimpong, JA, Geretz, A, Hernandez, M, Hollidge, BS, Jian, N, Kabra, K, Leggat, DJ, Liu, J, Pinto, AK, Rutvisuttinunt, W, Setliff, I, Tran, U, Townsley, S, Doranz, BJ, Rolland, M, McDermott, AB, Georgiev, IS, Thomas, R, Robb, ML, Eckels, KH, Barranco, E, Koren, M, Smith, DR, Jarman, RG, George, SL, Stephenson, KE, Barouch, DH, Modjarrad, K, Michael, NL, Joyce, MG & Krebs, SJ 2020, 'Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor', Nature Medicine, vol. 26, no. 2, pp. 228-235. https://doi.org/10.1038/s41591-019-0746-2

TY - JOUR

T1 - Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor

AU - Dussupt, Vincent

AU - Sankhala, Rajeshwer S.

AU - Gromowski, Gregory D.

AU - Donofrio, Gina

AU - De La Barrera, Rafael A.

AU - Larocca, Rafael A.

AU - Zaky, Weam

AU - Mendez-Rivera, Letzibeth

AU - Choe, Misook

AU - Davidson, Edgar

AU - McCracken, Michael K.

AU - Brien, James D.

AU - Abbink, Peter

AU - Bai, Hongjun

AU - Bryan, Aubrey L.

AU - Bias, Candace Hope

AU - Berry, Irina Maljkovic

AU - Botero, Nubia

AU - Cook, Tanya

AU - Doria-Rose, Nicole A.

AU - Escuer, Ariadna Grinyo i.

AU - Frimpong, Justice Akuoku

AU - Geretz, Aviva

AU - Hernandez, Mayda

AU - Hollidge, Bradley S.

AU - Jian, Ningbo

AU - Kabra, Kareem

AU - Leggat, David J.

AU - Liu, Jinyan

AU - Pinto, Amelia K.

AU - Rutvisuttinunt, Wiriya

AU - Setliff, Ian

AU - Tran, Ursula

AU - Townsley, Samantha

AU - Doranz, Benjamin J.

AU - Rolland, Morgane

AU - McDermott, Adrian B.

AU - Georgiev, Ivelin S.

AU - Thomas, Rasmi

AU - Robb, Merlin L.

AU - Eckels, Kenneth H.

AU - Barranco, Elizabeth

AU - Koren, Michael

AU - Smith, Darci R.

AU - Jarman, Richard G.

AU - George, Sarah L.

AU - Stephenson, Kathryn E.

AU - Barouch, Dan H.

AU - Modjarrad, Kayvon

AU - Michael, Nelson L.

AU - Joyce, M. Gordon

AU - Krebs, Shelly J.

PY - 2020/2/1

Y1 - 2020/2/1

N2 - Zika virus (ZIKV) has caused significant disease, with widespread cases of neurological pathology and congenital neurologic defects. Rapid vaccine development has led to a number of candidates capable of eliciting potent ZIKV-neutralizing antibodies (reviewed in refs. 1–3). Despite advances in vaccine development, it remains unclear how ZIKV vaccination affects immune responses in humans with prior flavivirus immunity. Here we show that a single-dose immunization of ZIKV purified inactivated vaccine (ZPIV)4–7 in a dengue virus (DENV)-experienced human elicited potent cross-neutralizing antibodies to both ZIKV and DENV. Using a unique ZIKV virion-based sorting strategy, we isolated and characterized multiple antibodies, including one termed MZ4, which targets a novel site of vulnerability centered on the Envelope (E) domain I/III linker region and protects mice from viremia and viral dissemination following ZIKV or DENV-2 challenge. These data demonstrate that Zika vaccination in a DENV-experienced individual can boost pre-existing flavivirus immunity and elicit protective responses against both ZIKV and DENV. ZPIV vaccination in Puerto Rican individuals with prior flavivirus experience yielded similar cross-neutralizing potency after a single vaccination, highlighting the potential benefit of ZIKV vaccination in flavivirus-endemic areas.

AB - Zika virus (ZIKV) has caused significant disease, with widespread cases of neurological pathology and congenital neurologic defects. Rapid vaccine development has led to a number of candidates capable of eliciting potent ZIKV-neutralizing antibodies (reviewed in refs. 1–3). Despite advances in vaccine development, it remains unclear how ZIKV vaccination affects immune responses in humans with prior flavivirus immunity. Here we show that a single-dose immunization of ZIKV purified inactivated vaccine (ZPIV)4–7 in a dengue virus (DENV)-experienced human elicited potent cross-neutralizing antibodies to both ZIKV and DENV. Using a unique ZIKV virion-based sorting strategy, we isolated and characterized multiple antibodies, including one termed MZ4, which targets a novel site of vulnerability centered on the Envelope (E) domain I/III linker region and protects mice from viremia and viral dissemination following ZIKV or DENV-2 challenge. These data demonstrate that Zika vaccination in a DENV-experienced individual can boost pre-existing flavivirus immunity and elicit protective responses against both ZIKV and DENV. ZPIV vaccination in Puerto Rican individuals with prior flavivirus experience yielded similar cross-neutralizing potency after a single vaccination, highlighting the potential benefit of ZIKV vaccination in flavivirus-endemic areas.

UR - http://www.scopus.com/inward/record.url?scp=85079175029&partnerID=8YFLogxK

U2 - 10.1038/s41591-019-0746-2

DO - 10.1038/s41591-019-0746-2

M3 - Letter

C2 - 32015557

AN - SCOPUS:85079175029

SN - 1078-8956

VL - 26

SP - 228

EP - 235

JO - Nature Medicine

JF - Nature Medicine

IS - 2

ER -

Potent Zika and dengue cross-neutralizing antibodies induced by Zika vaccination in a dengue-experienced donor

Abstract

Access to Document

Fingerprint

Cite this