Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring

Matthew G. Darby; Alisha Chetty; Dunja Mrjden; Marion Rolot; Katherine Smith; Claire MacKowiak; Delphine Sedda; Donald Nyangahu; Heather Jaspan; Kai Michael Toellner; Ari Waisman; Valerie Quesniaux; Bernhard Ryffel; Adam F. Cunningham; Benjamin G. Dewals; Frank Brombacher; William G.C. Horsnell

doi:10.1126/sciadv.aav3058

Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring

Matthew G. Darby, Alisha Chetty, Dunja Mrjden, Marion Rolot, Katherine Smith, Claire MacKowiak, Delphine Sedda, Donald Nyangahu, Heather Jaspan, Kai Michael Toellner, Ari Waisman, Valerie Quesniaux, Bernhard Ryffel, Adam F. Cunningham, Benjamin G. Dewals, Frank Brombacher, William G.C. Horsnell^*

^*Corresponding author for this work

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

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Abstract

Maternal immune transfer is the most significant source of protection from early-life infection, but whether maternal transfer of immunity by nursing permanently alters offspring immunity is poorly understood. Here, we identify maternal immune imprinting of offspring nursed by mothers who had a pre-conception helminth infection. Nursing of pups by helminth-exposed mothers transferred protective cellular immunity to these offspring against helminth infection. Enhanced control of infection was not dependent on maternal antibody. Protection associated with systemic development of protective type 2 immunity in T helper 2 (T_H2) impaired IL-4Rα ^-/- offspring. This maternally acquired immunity was maintained into maturity and required transfer (via nursing) to the offspring of maternally derived T_H2-competent CD4 T cells. Our data therefore reveal that maternal exposure to a globally prevalent source of infection before pregnancy provides long-term nursing-acquired immune benefits to offspring mediated by maternally derived pathogen-experienced lymphocytes.

Original language	English
Article number	eaav3058
Journal	Science Advances
Volume	5
Issue number	5
DOIs	https://doi.org/10.1126/sciadv.aav3058
Publication status	Published - 29 May 2019

ASJC Scopus subject areas

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Physics and Astronomy (miscellaneous)

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10.1126/sciadv.aav3058Licence: Creative Commons: Attribution-NonCommercial (CC BY-NC)

Darby_et_al_Pre-conception_maternal_helminth_Science_Advances_2019
Checked for eligibility: 24/06/2019 Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring by Matthew G. Darby, Alisha Chetty, Dunja Mrjden, Marion Rolot, Katherine Smith, Claire MacKowiak, Delphine Sedda, Donald Nyangahu, Heather Jaspan, Kai-Michael Toellner, Ari Waisman, Valerie Quesniaux, Bernhard Ryffel, Adam F. Cunningham, Benjamin G. Dewals, Frank Brombacher, William G. C. Horsnell science advances29 may 2019 : eaav3058
Final published version, 362 KBLicence: Creative Commons: Attribution-NonCommercial (CC BY-NC)

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Darby, M. G., Chetty, A., Mrjden, D., Rolot, M., Smith, K., MacKowiak, C., Sedda, D., Nyangahu, D., Jaspan, H., Toellner, K. M., Waisman, A., Quesniaux, V., Ryffel, B., Cunningham, A. F., Dewals, B. G., Brombacher, F., & Horsnell, W. G. C. (2019). Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring. Science Advances, 5(5), Article eaav3058. https://doi.org/10.1126/sciadv.aav3058

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title = "Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring",

abstract = "Maternal immune transfer is the most significant source of protection from early-life infection, but whether maternal transfer of immunity by nursing permanently alters offspring immunity is poorly understood. Here, we identify maternal immune imprinting of offspring nursed by mothers who had a pre-conception helminth infection. Nursing of pups by helminth-exposed mothers transferred protective cellular immunity to these offspring against helminth infection. Enhanced control of infection was not dependent on maternal antibody. Protection associated with systemic development of protective type 2 immunity in T helper 2 (TH2) impaired IL-4Rα -/- offspring. This maternally acquired immunity was maintained into maturity and required transfer (via nursing) to the offspring of maternally derived TH2-competent CD4 T cells. Our data therefore reveal that maternal exposure to a globally prevalent source of infection before pregnancy provides long-term nursing-acquired immune benefits to offspring mediated by maternally derived pathogen-experienced lymphocytes. ",

author = "Darby, {Matthew G.} and Alisha Chetty and Dunja Mrjden and Marion Rolot and Katherine Smith and Claire MacKowiak and Delphine Sedda and Donald Nyangahu and Heather Jaspan and Toellner, {Kai Michael} and Ari Waisman and Valerie Quesniaux and Bernhard Ryffel and Cunningham, {Adam F.} and Dewals, {Benjamin G.} and Frank Brombacher and Horsnell, {William G.C.}",

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Darby, MG, Chetty, A, Mrjden, D, Rolot, M, Smith, K, MacKowiak, C, Sedda, D, Nyangahu, D, Jaspan, H, Toellner, KM, Waisman, A, Quesniaux, V, Ryffel, B, Cunningham, AF, Dewals, BG, Brombacher, F & Horsnell, WGC 2019, 'Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring', Science Advances, vol. 5, no. 5, eaav3058. https://doi.org/10.1126/sciadv.aav3058

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AU - Darby, Matthew G.

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AU - MacKowiak, Claire

AU - Sedda, Delphine

AU - Nyangahu, Donald

AU - Jaspan, Heather

AU - Toellner, Kai Michael

AU - Waisman, Ari

AU - Quesniaux, Valerie

AU - Ryffel, Bernhard

AU - Cunningham, Adam F.

AU - Dewals, Benjamin G.

AU - Brombacher, Frank

AU - Horsnell, William G.C.

PY - 2019/5/29

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N2 - Maternal immune transfer is the most significant source of protection from early-life infection, but whether maternal transfer of immunity by nursing permanently alters offspring immunity is poorly understood. Here, we identify maternal immune imprinting of offspring nursed by mothers who had a pre-conception helminth infection. Nursing of pups by helminth-exposed mothers transferred protective cellular immunity to these offspring against helminth infection. Enhanced control of infection was not dependent on maternal antibody. Protection associated with systemic development of protective type 2 immunity in T helper 2 (TH2) impaired IL-4Rα -/- offspring. This maternally acquired immunity was maintained into maturity and required transfer (via nursing) to the offspring of maternally derived TH2-competent CD4 T cells. Our data therefore reveal that maternal exposure to a globally prevalent source of infection before pregnancy provides long-term nursing-acquired immune benefits to offspring mediated by maternally derived pathogen-experienced lymphocytes.

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Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring

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