Genetic and environmental interactions contribute to immune variation in rewilded mice

Oyebola Oyesola; Alexander E. Downie; Nina Howard; Ramya S. Barre; Kasalina Kiwanuka; Kimberly Zaldana; Ying Han Chen; Arthur Menezes; Soo Ching Lee; Joseph Devlin; Octavio Mondragón-Palomino; Camila Oliveira Silva Souza; Christin Herrmann; Sergei B. Koralov; Ken Cadwell; Andrea L. Graham; P’ng Loke

doi:10.1038/s41590-024-01862-5

Genetic and environmental interactions contribute to immune variation in rewilded mice

Oyebola Oyesola, Alexander E. Downie, Nina Howard, Ramya S. Barre, Kasalina Kiwanuka, Kimberly Zaldana, Ying Han Chen, Arthur Menezes, Soo Ching Lee, Joseph Devlin, Octavio Mondragón-Palomino, Camila Oliveira Silva Souza, Christin Herrmann, Sergei B. Koralov, Ken Cadwell, Andrea L. Graham, P’ng Loke

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3 Scopus citations

Abstract

The relative and synergistic contributions of genetics and environment to interindividual immune response variation remain unclear, despite implications in evolutionary biology and medicine. Here we quantify interactive effects of genotype and environment on immune traits by investigating C57BL/6, 129S1 and PWK/PhJ inbred mice, rewilded in an outdoor enclosure and infected with the parasite Trichuris muris. Whereas cellular composition was shaped by interactions between genotype and environment, cytokine response heterogeneity including IFNγ concentrations was primarily driven by genotype with consequence on worm burden. In addition, we show that other traits, such as expression of CD44, were explained mostly by genetics on T cells, whereas expression of CD44 on B cells was explained more by environment across all strains. Notably, genetic differences under laboratory conditions were decreased following rewilding. These results indicate that nonheritable influences interact with genetic factors to shape immune variation and parasite burden.

Original language	English (US)
Pages (from-to)	1270-1282
Number of pages	13
Journal	Nature Immunology
Volume	25
Issue number	7
DOIs	https://doi.org/10.1038/s41590-024-01862-5
State	Published - Jul 2024

All Science Journal Classification (ASJC) codes

Immunology and Allergy
Immunology

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10.1038/s41590-024-01862-5

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Oyesola, O., Downie, A. E., Howard, N., Barre, R. S., Kiwanuka, K., Zaldana, K., Chen, Y. H., Menezes, A., Lee, S. C., Devlin, J., Mondragón-Palomino, O., Souza, C. O. S., Herrmann, C., Koralov, S. B., Cadwell, K., Graham, A. L., & Loke, P. (2024). Genetic and environmental interactions contribute to immune variation in rewilded mice. Nature Immunology, 25(7), 1270-1282. https://doi.org/10.1038/s41590-024-01862-5

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title = "Genetic and environmental interactions contribute to immune variation in rewilded mice",

abstract = "The relative and synergistic contributions of genetics and environment to interindividual immune response variation remain unclear, despite implications in evolutionary biology and medicine. Here we quantify interactive effects of genotype and environment on immune traits by investigating C57BL/6, 129S1 and PWK/PhJ inbred mice, rewilded in an outdoor enclosure and infected with the parasite Trichuris muris. Whereas cellular composition was shaped by interactions between genotype and environment, cytokine response heterogeneity including IFNγ concentrations was primarily driven by genotype with consequence on worm burden. In addition, we show that other traits, such as expression of CD44, were explained mostly by genetics on T cells, whereas expression of CD44 on B cells was explained more by environment across all strains. Notably, genetic differences under laboratory conditions were decreased following rewilding. These results indicate that nonheritable influences interact with genetic factors to shape immune variation and parasite burden.",

author = "Oyebola Oyesola and Downie, {Alexander E.} and Nina Howard and Barre, {Ramya S.} and Kasalina Kiwanuka and Kimberly Zaldana and Chen, {Ying Han} and Arthur Menezes and Lee, {Soo Ching} and Joseph Devlin and Octavio Mondrag{\'o}n-Palomino and Souza, {Camila Oliveira Silva} and Christin Herrmann and Koralov, {Sergei B.} and Ken Cadwell and Graham, {Andrea L.} and P{\textquoteright}ng Loke",

note = "Publisher Copyright: {\textcopyright} This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2024.",

year = "2024",

month = jul,

doi = "10.1038/s41590-024-01862-5",

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Oyesola, O, Downie, AE, Howard, N, Barre, RS, Kiwanuka, K, Zaldana, K, Chen, YH, Menezes, A, Lee, SC, Devlin, J, Mondragón-Palomino, O, Souza, COS, Herrmann, C, Koralov, SB, Cadwell, K, Graham, AL & Loke, P 2024, 'Genetic and environmental interactions contribute to immune variation in rewilded mice', Nature Immunology, vol. 25, no. 7, pp. 1270-1282. https://doi.org/10.1038/s41590-024-01862-5

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AU - Oyesola, Oyebola

AU - Downie, Alexander E.

AU - Howard, Nina

AU - Barre, Ramya S.

AU - Kiwanuka, Kasalina

AU - Zaldana, Kimberly

AU - Chen, Ying Han

AU - Menezes, Arthur

AU - Lee, Soo Ching

AU - Devlin, Joseph

AU - Mondragón-Palomino, Octavio

AU - Souza, Camila Oliveira Silva

AU - Herrmann, Christin

AU - Koralov, Sergei B.

AU - Cadwell, Ken

AU - Graham, Andrea L.

AU - Loke, P’ng

PY - 2024/7

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AB - The relative and synergistic contributions of genetics and environment to interindividual immune response variation remain unclear, despite implications in evolutionary biology and medicine. Here we quantify interactive effects of genotype and environment on immune traits by investigating C57BL/6, 129S1 and PWK/PhJ inbred mice, rewilded in an outdoor enclosure and infected with the parasite Trichuris muris. Whereas cellular composition was shaped by interactions between genotype and environment, cytokine response heterogeneity including IFNγ concentrations was primarily driven by genotype with consequence on worm burden. In addition, we show that other traits, such as expression of CD44, were explained mostly by genetics on T cells, whereas expression of CD44 on B cells was explained more by environment across all strains. Notably, genetic differences under laboratory conditions were decreased following rewilding. These results indicate that nonheritable influences interact with genetic factors to shape immune variation and parasite burden.

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Genetic and environmental interactions contribute to immune variation in rewilded mice

Abstract

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