Elucidating regulatory processes of intense physical activity by multi-omics analysis
Abstract 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 ultimate...
| Main Authors: | , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-10-01
|
| Series: | Military Medical Research |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40779-023-00477-5 |
| _version_ | 1797577311846924288 |
|---|---|
| author | Ernesto S. Nakayasu Marina A. Gritsenko Young-Mo Kim Jennifer E. Kyle Kelly G. Stratton Carrie D. Nicora Nathalie Munoz Kathleen M. Navarro Daniel Claborne Yuqian Gao Karl K. Weitz Vanessa L. Paurus Kent J. Bloodsworth Kelsey A. Allen Lisa M. Bramer Fernando Montes Kathleen A. Clark Grant Tietje Justin Teeguarden Kristin E. Burnum-Johnson |
| author_facet | Ernesto S. Nakayasu Marina A. Gritsenko Young-Mo Kim Jennifer E. Kyle Kelly G. Stratton Carrie D. Nicora Nathalie Munoz Kathleen M. Navarro Daniel Claborne Yuqian Gao Karl K. Weitz Vanessa L. Paurus Kent J. Bloodsworth Kelsey A. Allen Lisa M. Bramer Fernando Montes Kathleen A. Clark Grant Tietje Justin Teeguarden Kristin E. Burnum-Johnson |
| author_sort | Ernesto S. Nakayasu |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-03-10T22:07:29Z |
| format | Article |
| id | doaj.art-8d95b24435db469bbedea100bc80ed20 |
| institution | Directory Open Access Journal |
| issn | 2054-9369 |
| language | English |
| last_indexed | 2024-03-10T22:07:29Z |
| publishDate | 2023-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Military Medical Research |
| spelling | doaj.art-8d95b24435db469bbedea100bc80ed202023-11-19T12:45:55ZengBMCMilitary Medical Research2054-93692023-10-0110112110.1186/s40779-023-00477-5Elucidating regulatory processes of intense physical activity by multi-omics analysisErnesto S. Nakayasu0Marina A. Gritsenko1Young-Mo Kim2Jennifer E. Kyle3Kelly G. Stratton4Carrie D. Nicora5Nathalie Munoz6Kathleen M. Navarro7Daniel Claborne8Yuqian Gao9Karl K. Weitz10Vanessa L. Paurus11Kent J. Bloodsworth12Kelsey A. Allen13Lisa M. Bramer14Fernando Montes15Kathleen A. Clark16Grant Tietje17Justin Teeguarden18Kristin E. Burnum-Johnson19Biological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryEnvironmental and Molecular Sciences Division, Pacific Northwest National LaboratoryCenters for Disease Control and Prevention, National Institute for Occupational Safety and HealthComputational Analytics Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryNational Security Directorate, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryLos Angeles County Fire DepartmentCenters for Disease Control and Prevention, National Institute for Occupational Safety and Health, Respiratory Health DivisionNational Security Directorate, Pacific Northwest National LaboratoryEnvironmental and Molecular Sciences Division, Pacific Northwest National LaboratoryEnvironmental and Molecular Sciences Division, Pacific Northwest National LaboratoryAbstract 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.https://doi.org/10.1186/s40779-023-00477-5Multi-omics analysisIntense exerciseHuman performanceBiofluidsMetabolismImmunity |
| spellingShingle | Ernesto S. Nakayasu Marina A. Gritsenko Young-Mo Kim Jennifer E. Kyle Kelly G. Stratton Carrie D. Nicora Nathalie Munoz Kathleen M. Navarro Daniel Claborne Yuqian Gao Karl K. Weitz Vanessa L. Paurus Kent J. Bloodsworth Kelsey A. Allen Lisa M. Bramer Fernando Montes Kathleen A. Clark Grant Tietje Justin Teeguarden Kristin E. Burnum-Johnson Elucidating regulatory processes of intense physical activity by multi-omics analysis Military Medical Research Multi-omics analysis Intense exercise Human performance Biofluids Metabolism Immunity |
| 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 | Multi-omics analysis Intense exercise Human performance Biofluids Metabolism Immunity |
| url | https://doi.org/10.1186/s40779-023-00477-5 |
| work_keys_str_mv | AT ernestosnakayasu elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT marinaagritsenko elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT youngmokim elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT jenniferekyle elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT kellygstratton elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT carriednicora elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT nathaliemunoz elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT kathleenmnavarro elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT danielclaborne elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT yuqiangao elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT karlkweitz elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT vanessalpaurus elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT kentjbloodsworth elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT kelseyaallen elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT lisambramer elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT fernandomontes elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT kathleenaclark elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT granttietje elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT justinteeguarden elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis AT kristineburnumjohnson elucidatingregulatoryprocessesofintensephysicalactivitybymultiomicsanalysis |