Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA

Sédami Gnidehou; Catherine J. Mitran; Eliana Arango; Shanna Banman; Angie Mena; Evelyn Medawar; Barbara A.S. Lima; Justin Doritchamou; Jahanara Rajwani; Albert Jin; Kenneth Gavina; Francis Ntumngia; Patrick Duffy; David Narum; Nicaise Tuikue Ndam; Morten A. Nielsen; Ali Salanti; Flora S. Kano; Luzia H. Carvalho; John H. Adams; Amanda Maestre; Michael F. Good; Stephanie K. Yanow

doi:10.1093/infdis/jiy467

Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA

Sédami Gnidehou, Catherine J. Mitran, Eliana Arango, Shanna Banman, Angie Mena, Evelyn Medawar, Barbara A.S. Lima, Justin Doritchamou, Jahanara Rajwani, Albert Jin, Kenneth Gavina, Francis Ntumngia, Patrick Duffy, David Narum, Nicaise Tuikue Ndam, Morten A. Nielsen, Ali Salanti, Flora S. Kano, Luzia H. Carvalho, John H. AdamsAmanda Maestre, Michael F. Good, Stephanie K. Yanow

VAR2CSA team

8 Citations (Scopus)

Abstract

Background: In pregnancy, Plasmodium falciparum parasites express the surface antigen VAR2CSA, which mediates adherence of red blood cells to chondroitin sulfate A (CSA) in the placenta. VAR2CSA antibodies are generally acquired during infection in pregnancy and are associated with protection from placental malaria. We observed previously that men and children in Colombia also had antibodies to VAR2CSA, but the origin of these antibodies was unknown. Here, we tested whether infection with Plasmodium vivax is an alternative mechanism of acquisition of VAR2CSA antibodies. Methods: We analyzed sera from nonpregnant Colombians and Brazilians exposed to P. vivax and monoclonal antibodies raised against P. vivax Duffy binding protein (PvDBP). Cross-reactivity to VAR2CSA was characterized by enzyme-linked immunosorbent assay, immunofluorescence assay, and flow cytometry, and antibodies were tested for inhibition of parasite binding to CSA. Results: Over 50% of individuals had antibodies that recognized VAR2CSA. Affinity-purified PvDBP human antibodies and a PvDBP monoclonal antibody recognized VAR2CSA, showing that PvDBP can give rise to cross-reactive antibodies. Importantly, the monoclonal antibody inhibited parasite binding to CSA, which is the primary in vitro correlate of protection from placental malaria. Conclusions: These data suggest that PvDBP induces antibodies that functionally recognize VAR2CSA, revealing a novel mechanism of cross-species immune recognition to falciparum malaria.

Original language	English
Journal	The Journal of Infectious Diseases
Volume	219
Issue number	1
Pages (from-to)	110-120
Number of pages	11
ISSN	0022-1899
DOIs	https://doi.org/10.1093/infdis/jiy467
Publication status	Published - 2019

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Gnidehou, S., Mitran, C. J., Arango, E., Banman, S., Mena, A., Medawar, E., Lima, B. A. S., Doritchamou, J., Rajwani, J., Jin, A., Gavina, K., Ntumngia, F., Duffy, P., Narum, D., Ndam, N. T., Nielsen, M. A., Salanti, A., Kano, F. S., Carvalho, L. H., ... Yanow, S. K. (2019). Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA. The Journal of Infectious Diseases, 219(1), 110-120. https://doi.org/10.1093/infdis/jiy467

Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA. / Gnidehou, Sédami; Mitran, Catherine J.; Arango, Eliana et al.

In: The Journal of Infectious Diseases, Vol. 219, No. 1, 2019, p. 110-120.

Research output: Contribution to journal › Journal article › Research › peer-review

Gnidehou, S, Mitran, CJ, Arango, E, Banman, S, Mena, A, Medawar, E, Lima, BAS, Doritchamou, J, Rajwani, J, Jin, A, Gavina, K, Ntumngia, F, Duffy, P, Narum, D, Ndam, NT, Nielsen, MA , Salanti, A, Kano, FS, Carvalho, LH, Adams, JH, Maestre, A, Good, MF & Yanow, SK 2019, 'Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA', The Journal of Infectious Diseases, vol. 219, no. 1, pp. 110-120. https://doi.org/10.1093/infdis/jiy467

@article{78096df6e3b64334a96839a8522928a1,

title = "Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA",

abstract = "Background: In pregnancy, Plasmodium falciparum parasites express the surface antigen VAR2CSA, which mediates adherence of red blood cells to chondroitin sulfate A (CSA) in the placenta. VAR2CSA antibodies are generally acquired during infection in pregnancy and are associated with protection from placental malaria. We observed previously that men and children in Colombia also had antibodies to VAR2CSA, but the origin of these antibodies was unknown. Here, we tested whether infection with Plasmodium vivax is an alternative mechanism of acquisition of VAR2CSA antibodies. Methods: We analyzed sera from nonpregnant Colombians and Brazilians exposed to P. vivax and monoclonal antibodies raised against P. vivax Duffy binding protein (PvDBP). Cross-reactivity to VAR2CSA was characterized by enzyme-linked immunosorbent assay, immunofluorescence assay, and flow cytometry, and antibodies were tested for inhibition of parasite binding to CSA. Results: Over 50% of individuals had antibodies that recognized VAR2CSA. Affinity-purified PvDBP human antibodies and a PvDBP monoclonal antibody recognized VAR2CSA, showing that PvDBP can give rise to cross-reactive antibodies. Importantly, the monoclonal antibody inhibited parasite binding to CSA, which is the primary in vitro correlate of protection from placental malaria. Conclusions: These data suggest that PvDBP induces antibodies that functionally recognize VAR2CSA, revealing a novel mechanism of cross-species immune recognition to falciparum malaria.",

author = "S{\'e}dami Gnidehou and Mitran, {Catherine J.} and Eliana Arango and Shanna Banman and Angie Mena and Evelyn Medawar and Lima, {Barbara A.S.} and Justin Doritchamou and Jahanara Rajwani and Albert Jin and Kenneth Gavina and Francis Ntumngia and Patrick Duffy and David Narum and Ndam, {Nicaise Tuikue} and Nielsen, {Morten A.} and Ali Salanti and Kano, {Flora S.} and Carvalho, {Luzia H.} and Adams, {John H.} and Amanda Maestre and Good, {Michael F.} and Yanow, {Stephanie K.}",

year = "2019",

doi = "10.1093/infdis/jiy467",

language = "English",

volume = "219",

pages = "110--120",

journal = "Journal of Infectious Diseases",

issn = "0022-1899",

publisher = "Oxford University Press",

number = "1",

}

TY - JOUR

T1 - Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA

AU - Gnidehou, Sédami

AU - Mitran, Catherine J.

AU - Arango, Eliana

AU - Banman, Shanna

AU - Mena, Angie

AU - Medawar, Evelyn

AU - Lima, Barbara A.S.

AU - Doritchamou, Justin

AU - Rajwani, Jahanara

AU - Jin, Albert

AU - Gavina, Kenneth

AU - Ntumngia, Francis

AU - Duffy, Patrick

AU - Narum, David

AU - Ndam, Nicaise Tuikue

AU - Nielsen, Morten A.

AU - Salanti, Ali

AU - Kano, Flora S.

AU - Carvalho, Luzia H.

AU - Adams, John H.

AU - Maestre, Amanda

AU - Good, Michael F.

AU - Yanow, Stephanie K.

PY - 2019

Y1 - 2019

N2 - Background: In pregnancy, Plasmodium falciparum parasites express the surface antigen VAR2CSA, which mediates adherence of red blood cells to chondroitin sulfate A (CSA) in the placenta. VAR2CSA antibodies are generally acquired during infection in pregnancy and are associated with protection from placental malaria. We observed previously that men and children in Colombia also had antibodies to VAR2CSA, but the origin of these antibodies was unknown. Here, we tested whether infection with Plasmodium vivax is an alternative mechanism of acquisition of VAR2CSA antibodies. Methods: We analyzed sera from nonpregnant Colombians and Brazilians exposed to P. vivax and monoclonal antibodies raised against P. vivax Duffy binding protein (PvDBP). Cross-reactivity to VAR2CSA was characterized by enzyme-linked immunosorbent assay, immunofluorescence assay, and flow cytometry, and antibodies were tested for inhibition of parasite binding to CSA. Results: Over 50% of individuals had antibodies that recognized VAR2CSA. Affinity-purified PvDBP human antibodies and a PvDBP monoclonal antibody recognized VAR2CSA, showing that PvDBP can give rise to cross-reactive antibodies. Importantly, the monoclonal antibody inhibited parasite binding to CSA, which is the primary in vitro correlate of protection from placental malaria. Conclusions: These data suggest that PvDBP induces antibodies that functionally recognize VAR2CSA, revealing a novel mechanism of cross-species immune recognition to falciparum malaria.

AB - Background: In pregnancy, Plasmodium falciparum parasites express the surface antigen VAR2CSA, which mediates adherence of red blood cells to chondroitin sulfate A (CSA) in the placenta. VAR2CSA antibodies are generally acquired during infection in pregnancy and are associated with protection from placental malaria. We observed previously that men and children in Colombia also had antibodies to VAR2CSA, but the origin of these antibodies was unknown. Here, we tested whether infection with Plasmodium vivax is an alternative mechanism of acquisition of VAR2CSA antibodies. Methods: We analyzed sera from nonpregnant Colombians and Brazilians exposed to P. vivax and monoclonal antibodies raised against P. vivax Duffy binding protein (PvDBP). Cross-reactivity to VAR2CSA was characterized by enzyme-linked immunosorbent assay, immunofluorescence assay, and flow cytometry, and antibodies were tested for inhibition of parasite binding to CSA. Results: Over 50% of individuals had antibodies that recognized VAR2CSA. Affinity-purified PvDBP human antibodies and a PvDBP monoclonal antibody recognized VAR2CSA, showing that PvDBP can give rise to cross-reactive antibodies. Importantly, the monoclonal antibody inhibited parasite binding to CSA, which is the primary in vitro correlate of protection from placental malaria. Conclusions: These data suggest that PvDBP induces antibodies that functionally recognize VAR2CSA, revealing a novel mechanism of cross-species immune recognition to falciparum malaria.

U2 - 10.1093/infdis/jiy467

DO - 10.1093/infdis/jiy467

M3 - Journal article

C2 - 30534974

AN - SCOPUS:85058594914

SN - 0022-1899

VL - 219

SP - 110

EP - 120

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 1

ER -

Cross-species immune recognition between Plasmodium vivax Duffy binding protein antibodies and the Plasmodium falciparum surface antigen VAR2CSA

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