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Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss
Exercise and exercise-induced weight loss have a beneficial effect on overall health, including positive effects on molecular pathways associated with immune function, especially in overweight individuals. The main aim of our study was to assess how energy deprivation (i.e., “semi-starvation”) leadi...
Autores principales: | , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6511813/ https://www.ncbi.nlm.nih.gov/pubmed/31134054 http://dx.doi.org/10.3389/fimmu.2019.00907 |
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author | Sarin, Heikki V. Gudelj, Ivan Honkanen, Jarno Ihalainen, Johanna K. Vuorela, Arja Lee, Joseph H. Jin, Zhenzhen Terwilliger, Joseph D. Isola, Ville Ahtiainen, Juha P. Häkkinen, Keijo Jurić, Julija Lauc, Gordan Kristiansson, Kati Hulmi, Juha J. Perola, Markus |
author_facet | Sarin, Heikki V. Gudelj, Ivan Honkanen, Jarno Ihalainen, Johanna K. Vuorela, Arja Lee, Joseph H. Jin, Zhenzhen Terwilliger, Joseph D. Isola, Ville Ahtiainen, Juha P. Häkkinen, Keijo Jurić, Julija Lauc, Gordan Kristiansson, Kati Hulmi, Juha J. Perola, Markus |
author_sort | Sarin, Heikki V. |
collection | PubMed |
description | Exercise and exercise-induced weight loss have a beneficial effect on overall health, including positive effects on molecular pathways associated with immune function, especially in overweight individuals. The main aim of our study was to assess how energy deprivation (i.e., “semi-starvation”) leading to substantial fat mass loss affects the immune system and immunosuppression in previously normal weight individuals. Thus, to address this hypothesis, we applied a high-throughput systems biology approach to better characterize potential key pathways associated with immune system modulation during intensive weight loss and subsequent weight regain. We examined 42 healthy female physique athletes (age 27.5 ± 4.0 years, body mass index 23.4 ± 1.7 kg/m(2)) volunteered into either a diet group (n = 25) or a control group (n = 17). For the diet group, the energy intake was reduced and exercise levels were increased to induce loss of fat mass that was subsequently regained during a recovery period. The control group was instructed to maintain their typical lifestyle, exercise levels, and energy intake at a constant level. For quantification of systems biology markers, fasting blood samples were drawn at three time points: baseline (PRE), at the end of the weight loss period (MID 21.1 ± 3.1 weeks after PRE), and at the end of the weight regain period (POST 18.4 ± 2.9 weeks after MID). In contrast to the control group, the diet group showed significant (false discovery rate <0.05) alteration of all measured immune function parameters—white blood cells (WBCs), immunoglobulin G glycome, leukocyte transcriptome, and cytokine profile. Integrative omics suggested effects on multiple levels of immune system as dysregulated hematopoiesis, suppressed immune cell proliferation, attenuated systemic inflammation, and loss of immune cell function by reduced antibody and chemokine secretion was implied after intense weight loss. During the weight regain period, the majority of the measured immune system parameters returned back to the baseline. In summary, this study elucidated a number of molecular pathways presumably explaining immunosuppression in individuals going through prolonged periods of intense training with low-energy availability. Our findings also reinforce the perception that the way in which weight loss is achieved (i.e., dietary restriction, exercise, or both) has a distinct effect on how the immune system is modulated. |
format | Online Article Text |
id | pubmed-6511813 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-65118132019-05-27 Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss Sarin, Heikki V. Gudelj, Ivan Honkanen, Jarno Ihalainen, Johanna K. Vuorela, Arja Lee, Joseph H. Jin, Zhenzhen Terwilliger, Joseph D. Isola, Ville Ahtiainen, Juha P. Häkkinen, Keijo Jurić, Julija Lauc, Gordan Kristiansson, Kati Hulmi, Juha J. Perola, Markus Front Immunol Immunology Exercise and exercise-induced weight loss have a beneficial effect on overall health, including positive effects on molecular pathways associated with immune function, especially in overweight individuals. The main aim of our study was to assess how energy deprivation (i.e., “semi-starvation”) leading to substantial fat mass loss affects the immune system and immunosuppression in previously normal weight individuals. Thus, to address this hypothesis, we applied a high-throughput systems biology approach to better characterize potential key pathways associated with immune system modulation during intensive weight loss and subsequent weight regain. We examined 42 healthy female physique athletes (age 27.5 ± 4.0 years, body mass index 23.4 ± 1.7 kg/m(2)) volunteered into either a diet group (n = 25) or a control group (n = 17). For the diet group, the energy intake was reduced and exercise levels were increased to induce loss of fat mass that was subsequently regained during a recovery period. The control group was instructed to maintain their typical lifestyle, exercise levels, and energy intake at a constant level. For quantification of systems biology markers, fasting blood samples were drawn at three time points: baseline (PRE), at the end of the weight loss period (MID 21.1 ± 3.1 weeks after PRE), and at the end of the weight regain period (POST 18.4 ± 2.9 weeks after MID). In contrast to the control group, the diet group showed significant (false discovery rate <0.05) alteration of all measured immune function parameters—white blood cells (WBCs), immunoglobulin G glycome, leukocyte transcriptome, and cytokine profile. Integrative omics suggested effects on multiple levels of immune system as dysregulated hematopoiesis, suppressed immune cell proliferation, attenuated systemic inflammation, and loss of immune cell function by reduced antibody and chemokine secretion was implied after intense weight loss. During the weight regain period, the majority of the measured immune system parameters returned back to the baseline. In summary, this study elucidated a number of molecular pathways presumably explaining immunosuppression in individuals going through prolonged periods of intense training with low-energy availability. Our findings also reinforce the perception that the way in which weight loss is achieved (i.e., dietary restriction, exercise, or both) has a distinct effect on how the immune system is modulated. Frontiers Media S.A. 2019-05-03 /pmc/articles/PMC6511813/ /pubmed/31134054 http://dx.doi.org/10.3389/fimmu.2019.00907 Text en Copyright © 2019 Sarin, Gudelj, Honkanen, Ihalainen, Vuorela, Lee, Jin, Terwilliger, Isola, Ahtiainen, Häkkinen, Jurić, Lauc, Kristiansson, Hulmi and Perola. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Immunology Sarin, Heikki V. Gudelj, Ivan Honkanen, Jarno Ihalainen, Johanna K. Vuorela, Arja Lee, Joseph H. Jin, Zhenzhen Terwilliger, Joseph D. Isola, Ville Ahtiainen, Juha P. Häkkinen, Keijo Jurić, Julija Lauc, Gordan Kristiansson, Kati Hulmi, Juha J. Perola, Markus Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss |
title | Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss |
title_full | Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss |
title_fullStr | Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss |
title_full_unstemmed | Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss |
title_short | Molecular Pathways Mediating Immunosuppression in Response to Prolonged Intensive Physical Training, Low-Energy Availability, and Intensive Weight Loss |
title_sort | molecular pathways mediating immunosuppression in response to prolonged intensive physical training, low-energy availability, and intensive weight loss |
topic | Immunology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6511813/ https://www.ncbi.nlm.nih.gov/pubmed/31134054 http://dx.doi.org/10.3389/fimmu.2019.00907 |
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