The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles
A better understanding of the cellular and molecular mechanisms that are involved in skeletal muscle adaptation to exercise is fundamentally important to take full advantage of the enormous benefits that exercise training offers in disease prevention and therapy. The aim of this study was to elucida...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2024-03-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/25/5/2881 |
| _version_ | 1797264369208262656 |
|---|---|
| author | Thomas Beiter Martina Zügel Jens Hudemann Marius Schild Annunziata Fragasso Christof Burgstahler Karsten Krüger Frank C. Mooren Jürgen M. Steinacker Andreas M. Nieß |
| author_facet | Thomas Beiter Martina Zügel Jens Hudemann Marius Schild Annunziata Fragasso Christof Burgstahler Karsten Krüger Frank C. Mooren Jürgen M. Steinacker Andreas M. Nieß |
| author_sort | Thomas Beiter |
| collection | DOAJ |
| description | A better understanding of the cellular and molecular mechanisms that are involved in skeletal muscle adaptation to exercise is fundamentally important to take full advantage of the enormous benefits that exercise training offers in disease prevention and therapy. The aim of this study was to elucidate the transcriptional signatures that distinguish the endurance-trained and untrained muscles in young adult males (24 ± 3.5 years). We characterized baseline differences as well as acute exercise-induced transcriptome responses in <i>vastus lateralis</i> biopsy specimens of endurance-trained athletes (ET; n = 8; VO<sub>2</sub>max, 67.2 ± 8.9 mL/min/kg) and sedentary healthy volunteers (SED; n = 8; VO<sub>2</sub>max, 40.3 ± 7.6 mL/min/kg) using microarray technology. A second cohort of SED volunteers (SED-T; n = 10) followed an 8-week endurance training program to assess expression changes of selected marker genes in the course of skeletal muscle adaptation. We deciphered differential baseline signatures that reflected major differences in the oxidative and metabolic capacity of the endurance-trained and untrained muscles. SED-T individuals in the training group displayed an up-regulation of nodal regulators of oxidative adaptation after 3 weeks of training and a significant shift toward the ET signature after 8 weeks. Transcriptome changes provoked by 1 h of intense cycling exercise only poorly overlapped with the genes that constituted the differential baseline signature of ETs and SEDs. Overall, acute exercise-induced transcriptional responses were connected to pathways of contractile, oxidative, and inflammatory stress and revealed a complex and highly regulated framework of interwoven signaling cascades to cope with exercise-provoked homeostatic challenges. While temporal transcriptional programs that were activated in SEDs and ETs were quite similar, the quantitative divergence in the acute response transcriptomes implicated divergent kinetics of gene induction and repression following an acute bout of exercise. Together, our results provide an extensive examination of the transcriptional framework that underlies skeletal muscle plasticity. |
| first_indexed | 2024-04-25T00:27:48Z |
| format | Article |
| id | doaj.art-827d780a9e434040962210f607b4ed32 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-04-25T00:27:48Z |
| publishDate | 2024-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-827d780a9e434040962210f607b4ed322024-03-12T16:46:41ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-03-01255288110.3390/ijms25052881The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome ProfilesThomas Beiter0Martina Zügel1Jens Hudemann2Marius Schild3Annunziata Fragasso4Christof Burgstahler5Karsten Krüger6Frank C. Mooren7Jürgen M. Steinacker8Andreas M. Nieß9Department of Sports Medicine, Medical Clinic, Eberhard-Karls-University of Tübingen, 72076 Tübingen, GermanyDepartment of Sport and Rehabilitation Medicine, University of Ulm, 89075 Ulm, GermanyDepartment of Sports Medicine, Medical Clinic, Eberhard-Karls-University of Tübingen, 72076 Tübingen, GermanyDepartment of Exercise Physiology and Sports Therapy, University of Gießen, 35394 Gießen, GermanyDepartment of Sports Medicine, Medical Clinic, Eberhard-Karls-University of Tübingen, 72076 Tübingen, GermanyDepartment of Sports Medicine, Medical Clinic, Eberhard-Karls-University of Tübingen, 72076 Tübingen, GermanyDepartment of Exercise Physiology and Sports Therapy, University of Gießen, 35394 Gießen, GermanyDepartment of Medicine, Faculty of Health, University of Witten/Herdecke, 58455 Witten, GermanyDepartment of Sport and Rehabilitation Medicine, University of Ulm, 89075 Ulm, GermanyDepartment of Sports Medicine, Medical Clinic, Eberhard-Karls-University of Tübingen, 72076 Tübingen, GermanyA better understanding of the cellular and molecular mechanisms that are involved in skeletal muscle adaptation to exercise is fundamentally important to take full advantage of the enormous benefits that exercise training offers in disease prevention and therapy. The aim of this study was to elucidate the transcriptional signatures that distinguish the endurance-trained and untrained muscles in young adult males (24 ± 3.5 years). We characterized baseline differences as well as acute exercise-induced transcriptome responses in <i>vastus lateralis</i> biopsy specimens of endurance-trained athletes (ET; n = 8; VO<sub>2</sub>max, 67.2 ± 8.9 mL/min/kg) and sedentary healthy volunteers (SED; n = 8; VO<sub>2</sub>max, 40.3 ± 7.6 mL/min/kg) using microarray technology. A second cohort of SED volunteers (SED-T; n = 10) followed an 8-week endurance training program to assess expression changes of selected marker genes in the course of skeletal muscle adaptation. We deciphered differential baseline signatures that reflected major differences in the oxidative and metabolic capacity of the endurance-trained and untrained muscles. SED-T individuals in the training group displayed an up-regulation of nodal regulators of oxidative adaptation after 3 weeks of training and a significant shift toward the ET signature after 8 weeks. Transcriptome changes provoked by 1 h of intense cycling exercise only poorly overlapped with the genes that constituted the differential baseline signature of ETs and SEDs. Overall, acute exercise-induced transcriptional responses were connected to pathways of contractile, oxidative, and inflammatory stress and revealed a complex and highly regulated framework of interwoven signaling cascades to cope with exercise-provoked homeostatic challenges. While temporal transcriptional programs that were activated in SEDs and ETs were quite similar, the quantitative divergence in the acute response transcriptomes implicated divergent kinetics of gene induction and repression following an acute bout of exercise. Together, our results provide an extensive examination of the transcriptional framework that underlies skeletal muscle plasticity.https://www.mdpi.com/1422-0067/25/5/2881skeletal muscle transcriptomicsgene expressionexercise physiologyskeletal muscleendurance trainingacute exercise |
| spellingShingle | Thomas Beiter Martina Zügel Jens Hudemann Marius Schild Annunziata Fragasso Christof Burgstahler Karsten Krüger Frank C. Mooren Jürgen M. Steinacker Andreas M. Nieß The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles International Journal of Molecular Sciences skeletal muscle transcriptomics gene expression exercise physiology skeletal muscle endurance training acute exercise |
| title | The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles |
| title_full | The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles |
| title_fullStr | The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles |
| title_full_unstemmed | The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles |
| title_short | The Acute, Short-, and Long-Term Effects of Endurance Exercise on Skeletal Muscle Transcriptome Profiles |
| title_sort | acute short and long term effects of endurance exercise on skeletal muscle transcriptome profiles |
| topic | skeletal muscle transcriptomics gene expression exercise physiology skeletal muscle endurance training acute exercise |
| url | https://www.mdpi.com/1422-0067/25/5/2881 |
| work_keys_str_mv | AT thomasbeiter theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT martinazugel theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT jenshudemann theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT mariusschild theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT annunziatafragasso theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT christofburgstahler theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT karstenkruger theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT frankcmooren theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT jurgenmsteinacker theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT andreasmnieß theacuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT thomasbeiter acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT martinazugel acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT jenshudemann acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT mariusschild acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT annunziatafragasso acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT christofburgstahler acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT karstenkruger acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT frankcmooren acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT jurgenmsteinacker acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles AT andreasmnieß acuteshortandlongtermeffectsofenduranceexerciseonskeletalmuscletranscriptomeprofiles |