Normalizing the environment recapitulates adult human immune traits in laboratory mice
Open accessAbstract
Our current understanding of immunology was largely defined in laboratory mice, partly because they are inbred and genetically homogeneous, can be genetically manipulated, allow kinetic tissue analyses to be carried out from the onset of disease, and permit the use of tractable disease models. Comparably reductionist experiments are neither technically nor ethically possible in humans. However, there is growing concern that laboratory mice do not reflect relevant aspects of the human immune system, which may account for failures to translate disease treatments from bench to bedside. Laboratory mice live in abnormally hygienic specific pathogen free (SPF) barrier facilities. Here we show that standard laboratory mouse husbandry has profound effects on the immune system and that environmental changes produce mice with immune systems closer to those of adult humans. Laboratory mice--like newborn, but not adult, humans--lack effector-differentiated and mucosally distributed memory T cells. These cell populations were present in free-living barn populations of feral mice and pet store mice with diverse microbial experience, and were induced in laboratory mice after co-housing with pet store mice, suggesting that the environment is involved in the induction of these cells. Altering the living conditions of mice profoundly affected the cellular composition of the innate and adaptive immune systems, resulted in global changes in blood cell gene expression to patterns that more closely reflected the immune signatures of adult humans rather than neonates, altered resistance to infection, and influenced T-cell differentiation in response to a de novo viral infection. These data highlight the effects of environment on the basal immune state and response to infection and suggest that restoring physiological microbial exposure in laboratory mice could provide a relevant tool for modelling immunological events in free-living organisms, including humans.
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Compared to free-living mice or laboratory animals exposed to gut flora from wild mice, SPF animals have a more limited microbial community and are also more susceptible to inflammatory diseases, with a reduced immune repertoire including deficits in memory responses.
“compared to free-living mice or laboratory animals exposed to gut flora from wild mice, SPF animals have a more limited microbial community and are also more susceptible to inflammatory diseases, with a reduced immune repertoire including deficits in memory responses”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [29]
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- Authors
- Beura, L. K., Hamilton, S. E., Bi, K., Schenkel, J. M., Odumade, O. A., Casey, K. A., Thompson, E. A., Fraser, K. A., Rosato, P. C., Filali-Mouhim, A., Sekaly, R. P., Jenkins, M. K., Vezys, V., Haining, W. N., Jameson, S. C., & Masopust, D.
- Affiliations
- University of Minnesota (US)
- Boston Children's Hospital (US)
- Corresponding author
- Jameson, Stephen C.
- Masopust, David
- ORCID
- Venue
- Nature
- Published
- 2016-04
- Volume
- 532
- Issue
- 7600
- Pages
- 512-516
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4871315
- OpenAlex
- W2337334490
- Cited by
- 1,072
- References
- 42
- Citations by year
- 2026: 83 · 2025: 80 · 2024: 94 · 2023: 76 · 2022: 92 · 2021: 139 · 2020: 114 · 2019: 118 · 2018: 111 · 2017: 119 · 2016: 45
- FWCI
- 79.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
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- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (UL1TR000114)
- National Cancer Institute (P30CA077598)
- National Institute of Allergy and Infectious Diseases (R01AI084913, R01AI075168, R01AI111671, R01AI116678, R37AI084913, T32AI007313, P01AI035296)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- environmental enrichment, cohousing, specific pathogen-free mice, immune system maturation, memory T cells, mucosal immunity, infection resistance, translational immunology, mouse husbandry, T cell differentiation, translational failure, preclinical models
- MeSH terms
- Adult, Animals, Animal Husbandry, Animals, Laboratory, Animals, Wild, Cell Differentiation, Environment, Environmental Exposure, Female, Humans, Immune System, Immunity, Immunity, Innate, Immunologic Memory, Infant, Newborn, Male, Phenotype, Specific Pathogen-Free Organisms, T-Lymphocytes, Virus Diseases, Models, Animal, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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