Normalizing the environment recapitulates adult human immune traits in laboratory mice
The immune system of laboratory mice raised in an ultra-hygienic environment resembles that ofnewborn humans, but can be induced to resemble the immune system of adult humans or 'dirty' mice by co-housing with pet store-bought mice. Do 'dirty' mice make better immunological model...
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| Vydáno v: | Nature (London) Ročník 532; číslo 7600; s. 512 - 516 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
28.04.2016
Nature Publishing Group |
| Témata: | |
| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| On-line přístup: | Získat plný text |
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| Abstract | The immune system of laboratory mice raised in an ultra-hygienic environment resembles that ofnewborn humans, but can be induced to resemble the immune system of adult humans or 'dirty' mice by co-housing with pet store-bought mice.
Do 'dirty' mice make better immunological models?
The laboratory mouse is by far the dominant model organism for
in vivo
immunological research which — particularly in the light of disappointing results obtained with some recent transfers of disease treatments from laboratory to clinic — raises the question of how accurately the model reflects the human immune system. These authors compare the immune status of laboratory mice with that of feral mice and with mice bought commercially as pets. They find that the immune system of the ubiquitous laboratory 'specific pathogen free' mouse approximates that of human neonates, rather than human adults. Co-housing laboratory mice with 'pet store' mice leads to maturation of the immune system, making it more similar to that of the human adult, and resulting in increased resistance in several models of infection. The use of such 'dirty' mice could supplement current models to either increase translational potential to human disease or to better inform the efficacy of preclinical prophylactic and therapeutic modalities.
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
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. 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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| AbstractList | The immune system of laboratory mice raised in an ultra-hygienic environment resembles that ofnewborn humans, but can be induced to resemble the immune system of adult humans or 'dirty' mice by co-housing with pet store-bought mice.
Do 'dirty' mice make better immunological models?
The laboratory mouse is by far the dominant model organism for
in vivo
immunological research which — particularly in the light of disappointing results obtained with some recent transfers of disease treatments from laboratory to clinic — raises the question of how accurately the model reflects the human immune system. These authors compare the immune status of laboratory mice with that of feral mice and with mice bought commercially as pets. They find that the immune system of the ubiquitous laboratory 'specific pathogen free' mouse approximates that of human neonates, rather than human adults. Co-housing laboratory mice with 'pet store' mice leads to maturation of the immune system, making it more similar to that of the human adult, and resulting in increased resistance in several models of infection. The use of such 'dirty' mice could supplement current models to either increase translational potential to human disease or to better inform the efficacy of preclinical prophylactic and therapeutic modalities.
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
1
,
2
,
3
,
4
,
5
,
6
,
7
,
8
. 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. 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.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. 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 (1-8). 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. 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. 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 bedside1-8. 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. |
| Audience | Academic |
| Author | Masopust, David Hamilton, Sara E. Casey, Kerry A. Rosato, Pamela C. Filali-Mouhim, Ali Vezys, Vaiva Odumade, Oludare A. Thompson, Emily A. Fraser, Kathryn A. Beura, Lalit K. Schenkel, Jason M. Jameson, Stephen C. Sekaly, Rafick P. Haining, W. Nicholas Jenkins, Marc K. Bi, Kevin |
| Author_xml | – sequence: 1 givenname: Lalit K. surname: Beura fullname: Beura, Lalit K. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 2 givenname: Sara E. surname: Hamilton fullname: Hamilton, Sara E. organization: Department of Laboratory Medicine and Pathology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 3 givenname: Kevin surname: Bi fullname: Bi, Kevin organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, and Pediatric Hematology and Oncology, Children's Hospital – sequence: 4 givenname: Jason M. surname: Schenkel fullname: Schenkel, Jason M. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 5 givenname: Oludare A. surname: Odumade fullname: Odumade, Oludare A. organization: Department of Laboratory Medicine and Pathology, Center for Immunology, University of Minnesota, Minneapolis, † Present addresses: Department of Pediatrics, University of California San Diego, Rady Children’s Hospital, San Diego, California 92123, USA (O.A.O.); Department of Respiratory, Inflammation and Autoimmunity, MedImmune LLC, Gaithersburg, Maryland 20878, USA (K.A.C.) – sequence: 6 givenname: Kerry A. surname: Casey fullname: Casey, Kerry A. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis, † Present addresses: Department of Pediatrics, University of California San Diego, Rady Children’s Hospital, San Diego, California 92123, USA (O.A.O.); Department of Respiratory, Inflammation and Autoimmunity, MedImmune LLC, Gaithersburg, Maryland 20878, USA (K.A.C.) – sequence: 7 givenname: Emily A. surname: Thompson fullname: Thompson, Emily A. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 8 givenname: Kathryn A. surname: Fraser fullname: Fraser, Kathryn A. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 9 givenname: Pamela C. surname: Rosato fullname: Rosato, Pamela C. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 10 givenname: Ali surname: Filali-Mouhim fullname: Filali-Mouhim, Ali organization: Department of Pathology, Case Western Reserve University – sequence: 11 givenname: Rafick P. surname: Sekaly fullname: Sekaly, Rafick P. organization: Department of Pathology, Case Western Reserve University – sequence: 12 givenname: Marc K. surname: Jenkins fullname: Jenkins, Marc K. organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 13 givenname: Vaiva surname: Vezys fullname: Vezys, Vaiva organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 14 givenname: W. Nicholas surname: Haining fullname: Haining, W. Nicholas organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, and Pediatric Hematology and Oncology, Children's Hospital – sequence: 15 givenname: Stephen C. surname: Jameson fullname: Jameson, Stephen C. email: masopust@umn.edu organization: Department of Laboratory Medicine and Pathology, Center for Immunology, University of Minnesota, Minneapolis – sequence: 16 givenname: David surname: Masopust fullname: Masopust, David email: james024@umn.edu organization: Department of Microbiology and Immunology, Center for Immunology, University of Minnesota, Minneapolis |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27096360$$D View this record in MEDLINE/PubMed |
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| Snippet | The immune system of laboratory mice raised in an ultra-hygienic environment resembles that ofnewborn humans, but can be induced to resemble the immune system... Our current understanding of immunology was largely defined in laboratory mice, partly because they are inbred and genetically homogeneous, can be genetically... |
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| SubjectTerms | 13/31 14/63 38/61 631/250/2520 631/250/254 Adult Animal Husbandry - methods Animals Animals, Laboratory - immunology Animals, Wild - immunology Antigens Biomedical research Cell Differentiation Disease Environment Environmental changes Environmental effects Environmental Exposure Female Gene expression Humanities and Social Sciences Humans Immune system Immune System - immunology Immunity Immunity - immunology Immunity, Innate - immunology Immunologic Memory Immunology Infant, Newborn Infections Laboratory animals letter Living conditions Lymphocytes Male Medical treatment Mice Models, Animal multidisciplinary Neonates Pathogens Phenotype Physiological aspects Physiological research Rodents Science Specific Pathogen-Free Organisms T cells T-Lymphocytes - cytology T-Lymphocytes - immunology Tissue analysis Virus Diseases - immunology Virus Diseases - virology |
| Title | Normalizing the environment recapitulates adult human immune traits in laboratory mice |
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