Cold acclimation affects immune composition in skeletal muscle of healthy lean subjects
Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigat...
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| Published in | Physiological reports Vol. 3; no. 7; pp. e12394 - n/a |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
John Wiley & Sons, Inc
01.07.2015
John Wiley & Sons, Ltd |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2051-817X 2051-817X |
| DOI | 10.14814/phy2.12394 |
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| Abstract | Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15°C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation (P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (−28%, P < 0.01) and NEDD4L (−15%, P < 0.05), as well as the regulatory T‐cell marker FOXP3 (−13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (−50%, P < 0.05), CXCL13 (−17%, P < 0.05) and CD209 (−15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined.
10 days of cold acclimation not only results in enhanced nonshivering thermogenesis, but also induces marked changes in immune cell markers in skeletal muscle of healthy lean subjects. Markers involved in Th17 response and M2 macrophage markers were downregulated, and markers for M1 macrophages were upregulated. Furthermore, immune markers related to IFN signaling were upregulated. |
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| AbstractList | Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15°C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation (P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (−28%, P < 0.01) and NEDD4L (−15%, P < 0.05), as well as the regulatory T‐cell marker FOXP3 (−13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (−50%, P < 0.05), CXCL13 (−17%, P < 0.05) and CD209 (−15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined. Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15 °: C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation (P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (-28%, P < 0.01) and NEDD4L (-15%, P < 0.05), as well as the regulatory T-cell marker FOXP3 (-13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (-50%, P < 0.05), CXCL13 (-17%, P < 0.05) and CD209 (-15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined.Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15 °: C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation (P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (-28%, P < 0.01) and NEDD4L (-15%, P < 0.05), as well as the regulatory T-cell marker FOXP3 (-13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (-50%, P < 0.05), CXCL13 (-17%, P < 0.05) and CD209 (-15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined. Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15 °: C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation (P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (-28%, P < 0.01) and NEDD4L (-15%, P < 0.05), as well as the regulatory T-cell marker FOXP3 (-13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (-50%, P < 0.05), CXCL13 (-17%, P < 0.05) and CD209 (-15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined. Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15 ° C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation ( P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (−28%, P < 0.01) and NEDD4L (−15%, P < 0.05), as well as the regulatory T-cell marker FOXP3 (−13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (−50%, P < 0.05), CXCL13 (−17%, P < 0.05) and CD209 (−15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined. Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal changes, which may directly or indirectly alter the immune system, even in the skeletal muscle. The aim of the present study was to investigate the effect of cold acclimation on immune composition in skeletal muscle. Skeletal muscle biopsies were obtained from 17 healthy lean subjects before and after 10 days of mild cold exposure (15°C, 6 h/day). Nonshivering thermogenesis was calculated by indirect calorimetry. We found that cold acclimation increased nonshivering thermogenesis from 10.8 ± 7.5 before to 17.8 ± 11.1% after cold acclimation (P < 0.01), but did not affect plasma catecholamine nor cytokine levels. In contrast, cold acclimation affected mRNA expression of several immune cell markers in skeletal muscle. It downregulated expression of the Th17 markers RORC (−28%, P < 0.01) and NEDD4L (−15%, P < 0.05), as well as the regulatory T‐cell marker FOXP3 (−13%, P < 0.05). Furthermore, cold acclimation downregulated expression of the M2 macrophage markers CCL22 (−50%, P < 0.05), CXCL13 (−17%, P < 0.05) and CD209 (−15%, P < 0.05), while the M1 macrophage marker IL12B was upregulated (+141%, P < 0.05). Cold acclimation also enhanced several markers related to interferon (IFN) signaling, including TAP1 (+12%, P < 0.01), IFITM1/3 (+11%, P < 0.05), CD274 (+36%, P < 0.05) and STAT 2 (+10%, P < 0.05). In conclusion, 10 days of intermittent cold exposure induces marked changes in the expression of immune cell markers in skeletal muscle of healthy lean subjects. The physiological consequences and therapeutic relevance of these changes remain to be determined. 10 days of cold acclimation not only results in enhanced nonshivering thermogenesis, but also induces marked changes in immune cell markers in skeletal muscle of healthy lean subjects. Markers involved in Th17 response and M2 macrophage markers were downregulated, and markers for M1 macrophages were upregulated. Furthermore, immune markers related to IFN signaling were upregulated. |
| Author | Marken Lichtenbelt, Wouter D. Haks, Mariëlle C. Quinten, Edwin Boon, Mariëtte R. Schaart, Gert Lans, Anouk A. J. J. Ottenhoff, Tom H. |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26149277$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1186_s12915_024_02041_6 crossref_primary_10_7717_peerj_9578 crossref_primary_10_1080_09613218_2017_1307647 crossref_primary_10_1016_j_ajpath_2016_03_019 crossref_primary_10_1016_j_jtherbio_2021_102875 crossref_primary_10_1002_ajhb_23175 crossref_primary_10_1016_j_jbiosc_2018_09_014 crossref_primary_10_1002_ajhb_23723 crossref_primary_10_1080_08958378_2018_1508258 crossref_primary_10_3390_ijms25010046 |
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| Copyright | 2015 The Authors. published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society. 2015 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society. 2015. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2015 The Authors. published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society. 2015 |
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| Keywords | macrophages thermogenesis skeletal muscle Cold acclimation Th17 cells |
| Language | English |
| License | Attribution http://creativecommons.org/licenses/by/4.0 http://doi.wiley.com/10.1002/tdm_license_1.1 2015 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Notes | This work is financed by the Netherlands Organization for Scientific Research (TOP 91209037 to W.D. van Marken Lichtenbelt) and by the EU FP7 projects DIABAT (HEALTH‐F2‐2011‐278373 to W.D. van Marken Lichtenbelt) and TANDEM (305279). Furthermore, M.R. Boon is supported by an NWO Rubicon Grant (#825.13.021). Funding Information ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Funding Information This work is financed by the Netherlands Organization for Scientific Research (TOP 91209037 to W.D. van Marken Lichtenbelt) and by the EU FP7 projects DIABAT (HEALTH-F2-2011-278373 to W.D. van Marken Lichtenbelt) and TANDEM (305279). Furthermore, M.R. Boon is supported by an NWO Rubicon Grant (#825.13.021). Both authors contributed equally. |
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| Snippet | Low environmental temperatures have a profound effect on biological processes in the body, including the immune system. Cold exposure coincides with hormonal... |
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| SubjectTerms | Catecholamines Cold acclimation Lymphocytes T Macrophages Original Research Physiology skeletal muscle Th17 cells thermogenesis |
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| Title | Cold acclimation affects immune composition in skeletal muscle of healthy lean subjects |
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