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

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, Benjamin G; Brombacher, F.; Horsnell, W. G. C.

doi:10.1126/sciadv.aav3058

Article (Scientific journals)

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

Darby, M. G.; Chetty, A.; Mrjden, D. et al.

2019 • In Science Advances, 5 (5)

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/237111

DOI
10.1126/sciadv.aav3058

PubMed
31236458

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Keywords :

T-cells; CD4 T-cells; Early life; Long lasting; Maternal exposure; Maternal transfer; Nursing

Abstract :

[en] 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-4R-/- 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. © 2019 by the Authors.

Disciplines :

Immunology & infectious disease

Author, co-author :

Darby, M. G.; Institute of Infectious Disease and Molecular Medicine, Division of Immunology, University of Cape Town, Cape Town, 7925, South Africa

Chetty, A.; Institute of Infectious Disease and Molecular Medicine, Division of Immunology, University of Cape Town, Cape Town, 7925, South Africa

Mrjden, D.; Institute of Infectious Disease and Molecular Medicine, Division of Immunology, University of Cape Town, Cape Town, 7925, South Africa, Department of Pathology, Stanford Blood Center, Stanford University, 3373 Hillview Ave., Palo Alto, CA 94304, United States

Rolot, M.; Fundamental and Applied Research in Animals and Health (FARAH), Immunology-Vaccinology, Faculty of Veterinary Medicine (B43b), University of Liège, Liège, Belgium

Smith, K.; Institute of Infectious Disease and Molecular Medicine, Division of Immunology, University of Cape Town, Cape Town, 7925, South Africa, Institute of Infection and Immunity, University of Cardiff, Cardiff, United Kingdom

MacKowiak, C.; Laboratory of Molecular and Experimental Immunology and Neuro-genetics, UMR 7355, CNRS-University of Orleans, Le Studium Institute for Advanced Studies, Rue Dupanloup, Orléans, 45000, France

Sedda, D.; Laboratory of Molecular and Experimental Immunology and Neuro-genetics, UMR 7355, CNRS-University of Orleans, Le Studium Institute for Advanced Studies, Rue Dupanloup, Orléans, 45000, France

Nyangahu, D.; Institute of Infectious Disease and Molecular Medicine, Division of Immunology, University of Cape Town, Cape Town, 7925, South Africa

Jaspan, H.; Institute of Infectious Disease and Molecular Medicine, Division of Immunology, University of Cape Town, Cape Town, 7925, South Africa, Seattle Children's Research Institute, Departments of Paediatrics and Global Health, University of Washington, Seattle, WA, United States

Toellner, K.-M.; Institute of Immunology and Immunotherapy, School of Immunity and Infection, University of Birmingham, Birmingham, B15 2TT, United Kingdom

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Title :

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

Publication date :

2019

Journal title :

Science Advances

eISSN :

2375-2548

Publisher :

American Association for the Advancement of Science

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

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since 20 June 2019

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Bibliography

K. M. Neuzil, B. G. Mellen, P. F. Wright, E. F. Mitchel Jr., M. R. Griffin, The effect of influenza on hospitalizations, outpatient visits, and courses of antibiotics in children. N. Engl. J. Med. 342, 225-231 (2000)
E. A. F. Simoes, E. A. F. Simoes, T. Cherian, J. Chow, S. A. Shahid-Salles, R. Laxminarayan, T. J. John, Acute respiratory infections in children, in Disease Control Priorities in Developing Countries, D. T. Jamison, J. G. Breman, A. R. Measham, G. Alleyne, M. Claeson, D. B. Evans, P. Jha, A. Mills, P. Musgrove, Eds. (Oxford Univ. Press, 2006)
G. Jones, R. W. Steketee, R. E. Black, Z. A. Bhutta, S. S. Morris; Bellagio Child Survival Study Group, How many child deaths can we prevent this year? Lancet 362, 65-71 (2003)
J. H. Wolf, Low breastfeeding rates and public health in the United States. Am. J. Public Health 93, 2000-2010 (2003)
P. T. Heath, F. J. Culley, C. E. Jones, B. Kampmann, K. le Doare, M. C. Nunes, M. Sadarangani, Z. Chaudhry, C. J. Baker, P. J. M. Openshaw, Group B streptococcus and respiratory syncytial virus immunisation during pregnancy: A landscape analysis. Lancet Infect. Dis. 17, e223-e234 (2017)
A. Marchant, M. Sadarangani, M. Garand, N. Dauby, V. Verhasselt, L. Pereira, G. Bjornson, C. E. Jones, S. A. Halperin, K. M. Edwards, P. Heath, P. J. Openshaw, D. W. Scheifele, T. R. Kollmann, Maternal immunisation: Collaborating with mother nature. Lancet Infect. Dis. 17, e197-e208 (2017)
V. Verhasselt, Is infant immunization by breastfeeding possible? Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 1-6 (2015)
M. K. Ghosh, V. Nguyen, H. K. Muller, A. M. Walker, Maternal milk T cells drive development of transgenerational Th1 immunity in offspring thymus. J. Immunol. 197, 2290-2296 (2016)
B. G. Dewals, L. E. Layland, C. Prazeres da Costa, W. G. Horsnell, Maternal helminth infections and the shaping of offspring immunity. Parasite Immunol. 41, e12599 (2019)
W. G. Horsnell, M. G. Darby, J. C. Hoving, N. Nieuwenhuizen, H. J. McSorley, H. Ndlovu, S. Bobat, M. Kimberg, F. Kirstein, A. J. Cutler, B. DeWals, A. F. Cunningham, F. Brombacher, IL-4R-associated antigen processing by B cells promotes immunity in Nippostrongylus brasiliensis infection. PLOS Pathog. 9, e1003662 (2013)
W. C. Gause, R. M. Maizels, Macrobiota-Helminths as active participants and partners of the microbiota in host intestinal homeostasis. Curr. Opin. Microbiol. 32, 14-18 (2016)
R. M. Maizels, Parasitic helminth infections and the control of human allergic and autoimmune disorders. Clin. Microbiol. Infect. 22, 481-486 (2016)
N. L. Harris, I. Spoerri, J. F. Schopfer, C. Nembrini, P. Merky, J. Massacand, J. F. Urban Jr., A. Lamarre, K. Burki, B. Odermatt, R. M. Zinkernagel, A. J. Macpherson, Mechanisms of neonatal mucosal antibody protection. J. Immunol. 177, 6256-6262 (2006)
K. Straubinger, S. Paul, O. Prazeres da Costa, M. Ritter, T. Buch, D. H. Busch, L. E. Layland, C. U. Prazeres da Costa, Maternal immune response to helminth infection during pregnancy determines offspring susceptibility to allergic airway inflammation. J. Allergy Clin. Immunol. 134, 1271-1279.e10 (2014)
I. Guadalupe, E. Mitre, S. Benitez, M. E. Chico, T. B. Nutman, P. J. Cooper, Evidence for in utero sensitization to Ascaris lumbricoides in newborns of mothers with ascariasis. J. Infect. Dis. 199, 1846-1850 (2009)
H. Mpairwe, J. Ndibazza, E. L. Webb, M. Nampijja, L. Muhangi, B. Apule, S. Lule, H. Akurut, D. Kizito, M. Kakande, F. M. Jones, C. M. Fitzsimmons, M. Muwanga, L. C. Rodrigues, D. W. Dunne, A. M. Elliott, Maternal hookworm modifies risk factors for childhood eczema: Results from a birth cohort in Uganda. Pediatr. Allergy Immunol. 25, 481-488 (2014)
S. G. Thawer, W. G. C. Horsnell, M. Darby, J. C. Hoving, B. Dewals, A. J. Cutler, D. Lang, F. Brombacher, Lung-resident CD4+ T cells are sufficient for IL-4R-dependent recall immunity to Nippostrongylus brasiliensis infection. Mucosal Immunol. 7, 239-248 (2014)
L. A. Hanson, M. Korotkova, S. Lundin, L. Håversen, S. A. Silfverdal, I. Mattsby-Baltzer, B. Strandvik, E. Telemo, The transfer of immunity from mother to child. Ann. N. Y. Acad. Sci. 987, 199-206 (2003)
Q. Liu, T. Kreider, S. Bowdridge, Z. Liu, Y. Song, A. G. Gaydo, J. F. Urban Jr., W. C. Gause, B cells have distinct roles in host protection against different nematode parasites. J. Immunol. 184, 5213-5223 (2010)
A. Waisman, M. Kraus, J. Seagal, S. Ghosh, D. Melamed, J. Song, Y. Sasaki, S. Classen, C. Lutz, F. Brombacher, L. Nitschke, K. Rajewsky, IgG1 B cell receptor signaling is inhibited by CD22 and promotes the development of B cells whose survival is less dependent on Ig/. J. Exp. Med. 204, 747-758 (2007)
P. Vieira, K. Rajewsky, The half-lives of serum immunoglobulins in adult mice. Eur. J. Immunol. 18, 313-316 (1988)
F. Chen, W. Wu, A. Millman, J. F. Craft, E. Chen, N. Patel, J. L. Boucher, J. F. Urban Jr., C. C. Kim, W. C. Gause, Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat. Immunol. 15, 938-946 (2014)
M. Harvie, M. Camberis, S. C. Tang, B. Delahunt, W. Paul, G. Le Gros, The lung is an important site for priming CD4 T-cell-mediated protective immunity against gastrointestinal helminth parasites. Infect. Immun. 78, 3753-3762 (2010)
T. Bouchery, R. Kyle, M. Camberis, A. Shepherd, K. Filbey, A. Smith, M. Harvie, G. Painter, K. Johnston, P. Ferguson, R. Jain, B. Roediger, B. Delahunt, W. Weninger, E. Forbes-Blom, G. Le Gros, ILC2s and T cells cooperate to ensure maintenance of M2 macrophages for lung immunity against hookworms. Nat. Commun. 6, 6970 (2015)
K. Urso, D. Alvarez, V. Cremasco, K. Tsang, A. Grauel, R. Lafyatis, U. H. von Andrian, J. Ermann, A. O. Aliprantis, IL4RA on lymphatic endothelial cells promotes T cell egress during sclerodermatous graft versus host disease. JCI Insight 1, e88057 (2016)
J. J. Letterio, A. G. Geiser, A. B. Kulkarni, N. S. Roche, M. B. Sporn, A. B. Roberts, Maternal rescue of transforming growth factor-beta 1 null mice. Science 264, 1936-1938 (1994)
J. Esser-von Bieren, I. Mosconi, R. Guiet, A. Piersgilli, B. Volpe, F. Chen, W. C. Gause, A. Seitz, J. S. Verbeek, N. L. Harris, Antibodies trap tissue migrating helminth larvae and prevent tissue damage by driving IL-4R-independent alternative differentiation of macrophages. PLOS Pathog. 9, e1003771 (2013)
K. D. McCoy, M. Stoel, R. Stettler, P. Merky, K. Fink, B. M. Senn, C. Schaer, J. Massacand, B. Odermatt, H. C. Oettgen, R. M. Zinkernagel, N. A. Bos, H. Hengartner, A. J. Macpherson, N. L. Harris, Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4, 362-373 (2008)
M. Barner, M. Mohrs, F. Brombacher, M. Kopf, Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr. Biol. 8, 669-672 (1998)
A. Cabinian, D. Sinsimer, M. Tang, O. Zumba, H. Mehta, A. Toma, D. Sant'Angelo, Y. Laouar, A. Laouar, Transfer of maternal immune cells by breastfeeding: Maternal cytotoxic T lymphocytes present in breast milk localize in the Peyer's patches of the nursed infant. PLOS ONE 11, e0156762 (2016)
T. Sornasse, P. V. Larenas, K. A. Davis, J. E. de Vries, H. Yssel, Differentiation and stability of T helper 1 and 2 cells derived from naive human neonatal CD4+ T cells, analyzed at the single-cell level. J. Exp. Med. 184, 473-483 (1996)
L. Li, H. H. Lee, J. J. Bell, R. K. Gregg, J. S. Ellis, A. Gessner, H. Zaghouani, IL-4 utilizes an alternative receptor to drive apoptosis of Th1 cells and skews neonatal immunity toward Th2. Immunity 20, 429-440 (2004)
H. Sefrioui, J. Donahue, E. A. Gilpin, A. S. Srivastava, E. Carrier, Tolerance and immunity following in utero transplantation of allogeneic fetal liver cells: The cytokine shift. Cell Transplant. 12, 75-82 (2003)
C. V. Jones, T. M. Williams, K. A. Walker, H. Dickinson, S. Sakkal, B. A. Rumballe, M. H. Little, G. Jenkin, S. D. Ricardo, M2 macrophage polarisation is associated with alveolar formation during postnatal lung development. Respir. Res. 14, 41 (2013)
I. M. de Kleer, M. Kool, M. J. W. de Bruijn, M. Willart, J. van Moorleghem, M. J. Schuijs, M. Plantinga, R. Beyaert, E. Hams, P. G. Fallon, H. Hammad, R. W. Hendriks, B. N. Lambrecht, Perinatal activation of the interleukin-33 pathway promotes type 2 immunity in the developing lung. Immunity 45, 1285-1298 (2016)
J. C. Hoving, F. Kirstein, N. E. Nieuwenhuizen, L. C. E. Fick, E. Hobeika, M. Reth, F. Brombacher, B cells that produce immunoglobulin E mediate colitis in BALB/c mice. Gastroenterology 142, 96-108 (2012)
M. Radwanska, A. J. Cutler, J. C. Hoving, S. Magez, C. Holscher, A. Bohms, B. Arendse, R. Kirsch, T. Hunig, J. Alexander, P. Kaye, F. Brombacher, Deletion of IL-4R on CD4 T cells renders BALB/c mice resistant to Leishmania major infection. PLOS Pathog. 3, e68 (2007)
M. Darby, C. Schnoeller, A. Vira, F. Culley, S. Bobat, E. Logan, F. Kirstein, J. Wess, A. F. Cunningham, F. Brombacher, M. E. Selkirk, W. G. C. Horsnell, The M3 muscarinic receptor is required for optimal adaptive immunity to helminth and bacterial infection. PLOS Pathog. 11, e1004636 (2015).