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Elucidating regulatory processes of intense physical activity by multi-omics analysis
BACKGROUND: Physiological and biochemical processes across tissues of the body are regulated in response to the high demands of intense physical activity in several occupations, such as firefighting, law enforcement, military, and sports. A better understanding of such processes can ultimately help...
Autores principales: | , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10583322/ https://www.ncbi.nlm.nih.gov/pubmed/37853489 http://dx.doi.org/10.1186/s40779-023-00477-5 |
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author | Nakayasu, Ernesto S. Gritsenko, Marina A. Kim, Young-Mo Kyle, Jennifer E. Stratton, Kelly G. Nicora, Carrie D. Munoz, Nathalie Navarro, Kathleen M. Claborne, Daniel Gao, Yuqian Weitz, Karl K. Paurus, Vanessa L. Bloodsworth, Kent J. Allen, Kelsey A. Bramer, Lisa M. Montes, Fernando Clark, Kathleen A. Tietje, Grant Teeguarden, Justin Burnum-Johnson, Kristin E. |
author_facet | Nakayasu, Ernesto S. Gritsenko, Marina A. Kim, Young-Mo Kyle, Jennifer E. Stratton, Kelly G. Nicora, Carrie D. Munoz, Nathalie Navarro, Kathleen M. Claborne, Daniel Gao, Yuqian Weitz, Karl K. Paurus, Vanessa L. Bloodsworth, Kent J. Allen, Kelsey A. Bramer, Lisa M. Montes, Fernando Clark, Kathleen A. Tietje, Grant Teeguarden, Justin Burnum-Johnson, Kristin E. |
author_sort | Nakayasu, Ernesto S. |
collection | PubMed |
description | BACKGROUND: Physiological and biochemical processes across tissues of the body are regulated in response to the high demands of intense physical activity in several occupations, such as firefighting, law enforcement, military, and sports. A better understanding of such processes can ultimately help improve human performance and prevent illnesses in the work environment. METHODS: To study regulatory processes in intense physical activity simulating real-life conditions, we performed a multi-omics analysis of three biofluids (blood plasma, urine, and saliva) collected from 11 wildland firefighters before and after a 45 min, intense exercise regimen. Omics profiles post- versus pre-exercise were compared by Student’s t-test followed by pathway analysis and comparison between the different omics modalities. RESULTS: Our multi-omics analysis identified and quantified 3835 proteins, 730 lipids and 182 metabolites combining the 3 different types of samples. The blood plasma analysis revealed signatures of tissue damage and acute repair response accompanied by enhanced carbon metabolism to meet energy demands. The urine analysis showed a strong, concomitant regulation of 6 out of 8 identified proteins from the renin-angiotensin system supporting increased excretion of catabolites, reabsorption of nutrients and maintenance of fluid balance. In saliva, we observed a decrease in 3 pro-inflammatory cytokines and an increase in 8 antimicrobial peptides. A systematic literature review identified 6 papers that support an altered susceptibility to respiratory infection. CONCLUSION: This study shows simultaneous regulatory signatures in biofluids indicative of homeostatic maintenance during intense physical activity with possible effects on increased infection susceptibility, suggesting that caution against respiratory diseases could benefit workers on highly physical demanding jobs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40779-023-00477-5. |
format | Online Article Text |
id | pubmed-10583322 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-105833222023-10-19 Elucidating regulatory processes of intense physical activity by multi-omics analysis Nakayasu, Ernesto S. Gritsenko, Marina A. Kim, Young-Mo Kyle, Jennifer E. Stratton, Kelly G. Nicora, Carrie D. Munoz, Nathalie Navarro, Kathleen M. Claborne, Daniel Gao, Yuqian Weitz, Karl K. Paurus, Vanessa L. Bloodsworth, Kent J. Allen, Kelsey A. Bramer, Lisa M. Montes, Fernando Clark, Kathleen A. Tietje, Grant Teeguarden, Justin Burnum-Johnson, Kristin E. Mil Med Res Research BACKGROUND: Physiological and biochemical processes across tissues of the body are regulated in response to the high demands of intense physical activity in several occupations, such as firefighting, law enforcement, military, and sports. A better understanding of such processes can ultimately help improve human performance and prevent illnesses in the work environment. METHODS: To study regulatory processes in intense physical activity simulating real-life conditions, we performed a multi-omics analysis of three biofluids (blood plasma, urine, and saliva) collected from 11 wildland firefighters before and after a 45 min, intense exercise regimen. Omics profiles post- versus pre-exercise were compared by Student’s t-test followed by pathway analysis and comparison between the different omics modalities. RESULTS: Our multi-omics analysis identified and quantified 3835 proteins, 730 lipids and 182 metabolites combining the 3 different types of samples. The blood plasma analysis revealed signatures of tissue damage and acute repair response accompanied by enhanced carbon metabolism to meet energy demands. The urine analysis showed a strong, concomitant regulation of 6 out of 8 identified proteins from the renin-angiotensin system supporting increased excretion of catabolites, reabsorption of nutrients and maintenance of fluid balance. In saliva, we observed a decrease in 3 pro-inflammatory cytokines and an increase in 8 antimicrobial peptides. A systematic literature review identified 6 papers that support an altered susceptibility to respiratory infection. CONCLUSION: This study shows simultaneous regulatory signatures in biofluids indicative of homeostatic maintenance during intense physical activity with possible effects on increased infection susceptibility, suggesting that caution against respiratory diseases could benefit workers on highly physical demanding jobs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40779-023-00477-5. BioMed Central 2023-10-18 /pmc/articles/PMC10583322/ /pubmed/37853489 http://dx.doi.org/10.1186/s40779-023-00477-5 Text en © © Battelle Memorial Institute 2023 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Nakayasu, Ernesto S. Gritsenko, Marina A. Kim, Young-Mo Kyle, Jennifer E. Stratton, Kelly G. Nicora, Carrie D. Munoz, Nathalie Navarro, Kathleen M. Claborne, Daniel Gao, Yuqian Weitz, Karl K. Paurus, Vanessa L. Bloodsworth, Kent J. Allen, Kelsey A. Bramer, Lisa M. Montes, Fernando Clark, Kathleen A. Tietje, Grant Teeguarden, Justin Burnum-Johnson, Kristin E. Elucidating regulatory processes of intense physical activity by multi-omics analysis |
title | Elucidating regulatory processes of intense physical activity by multi-omics analysis |
title_full | Elucidating regulatory processes of intense physical activity by multi-omics analysis |
title_fullStr | Elucidating regulatory processes of intense physical activity by multi-omics analysis |
title_full_unstemmed | Elucidating regulatory processes of intense physical activity by multi-omics analysis |
title_short | Elucidating regulatory processes of intense physical activity by multi-omics analysis |
title_sort | elucidating regulatory processes of intense physical activity by multi-omics analysis |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10583322/ https://www.ncbi.nlm.nih.gov/pubmed/37853489 http://dx.doi.org/10.1186/s40779-023-00477-5 |
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