The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes
It is widely accepted that infection and immune response incur significant metabolic demands, yet the respective demands of specific immune responses to live pathogens have not been well delineated. It is also established that upon activation, metabolic pathways undergo shifts at the cellular level....
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2020.614697/full |
| _version_ | 1818324657293492224 |
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| author | Robert M. Johnson Adesola C. Olatunde Lauren N. Woodie Michael W. Greene Elizabeth Hiltbold Schwartz |
| author_facet | Robert M. Johnson Adesola C. Olatunde Lauren N. Woodie Michael W. Greene Elizabeth Hiltbold Schwartz |
| author_sort | Robert M. Johnson |
| collection | DOAJ |
| description | It is widely accepted that infection and immune response incur significant metabolic demands, yet the respective demands of specific immune responses to live pathogens have not been well delineated. It is also established that upon activation, metabolic pathways undergo shifts at the cellular level. However, most studies exploring these issues at the systemic or cellular level have utilized pathogen associated molecular patterns (PAMPs) that model sepsis, or model antigens at isolated time points. Thus, the dynamics of pathogenesis and immune response to a live infection remain largely undocumented. To better quantitate the metabolic demands induced by infection, we utilized a live pathogenic infection model. Mice infected with Listeria monocytogenes were monitored longitudinally over the course of infection through clearance. We measured systemic metabolic phenotype, bacterial load, innate and adaptive immune responses, and cellular metabolic pathways. To further delineate the role of adaptive immunity in the metabolic phenotype, we utilized two doses of bacteria, one that induced both sickness behavior and protective (T cell mediated) immunity, and the other protective immunity alone. We determined that the greatest impact to systemic metabolism occurred during the early immune response, which coincided with the greatest shift in innate cellular metabolism. In contrast, during the time of maximal T cell expansion, systemic metabolism returned to resting state. Taken together, our findings demonstrate that the timing of maximal metabolic demand overlaps with the innate immune response and that when the adaptive response is maximal, the host has returned to relative metabolic homeostasis. |
| first_indexed | 2024-12-13T11:32:04Z |
| format | Article |
| id | doaj.art-f0f1877c07c841f88f09329c4917e385 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-13T11:32:04Z |
| publishDate | 2021-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-f0f1877c07c841f88f09329c4917e3852022-12-21T23:47:54ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-02-011110.3389/fimmu.2020.614697614697The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenesRobert M. Johnson0Adesola C. Olatunde1Lauren N. Woodie2Michael W. Greene3Elizabeth Hiltbold Schwartz4Department of Biological Sciences, Auburn University, Auburn, AL, United StatesDepartment of Biological Sciences, Auburn University, Auburn, AL, United StatesDepartment of Nutrition, Dietetics, and Hospitality Management, Auburn University, Auburn, AL, United StatesDepartment of Nutrition, Dietetics, and Hospitality Management, Auburn University, Auburn, AL, United StatesDepartment of Biological Sciences, Auburn University, Auburn, AL, United StatesIt is widely accepted that infection and immune response incur significant metabolic demands, yet the respective demands of specific immune responses to live pathogens have not been well delineated. It is also established that upon activation, metabolic pathways undergo shifts at the cellular level. However, most studies exploring these issues at the systemic or cellular level have utilized pathogen associated molecular patterns (PAMPs) that model sepsis, or model antigens at isolated time points. Thus, the dynamics of pathogenesis and immune response to a live infection remain largely undocumented. To better quantitate the metabolic demands induced by infection, we utilized a live pathogenic infection model. Mice infected with Listeria monocytogenes were monitored longitudinally over the course of infection through clearance. We measured systemic metabolic phenotype, bacterial load, innate and adaptive immune responses, and cellular metabolic pathways. To further delineate the role of adaptive immunity in the metabolic phenotype, we utilized two doses of bacteria, one that induced both sickness behavior and protective (T cell mediated) immunity, and the other protective immunity alone. We determined that the greatest impact to systemic metabolism occurred during the early immune response, which coincided with the greatest shift in innate cellular metabolism. In contrast, during the time of maximal T cell expansion, systemic metabolism returned to resting state. Taken together, our findings demonstrate that the timing of maximal metabolic demand overlaps with the innate immune response and that when the adaptive response is maximal, the host has returned to relative metabolic homeostasis.https://www.frontiersin.org/articles/10.3389/fimmu.2020.614697/fullmetabolic phenotypeListeria (L.) monocytogenessickness behaviorimmunometabolismlife history theory |
| spellingShingle | Robert M. Johnson Adesola C. Olatunde Lauren N. Woodie Michael W. Greene Elizabeth Hiltbold Schwartz The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes Frontiers in Immunology metabolic phenotype Listeria (L.) monocytogenes sickness behavior immunometabolism life history theory |
| title | The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes |
| title_full | The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes |
| title_fullStr | The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes |
| title_full_unstemmed | The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes |
| title_short | The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes |
| title_sort | systemic and cellular metabolic phenotype of infection and immune response to listeria monocytogenes |
| topic | metabolic phenotype Listeria (L.) monocytogenes sickness behavior immunometabolism life history theory |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2020.614697/full |
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