Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise. / Place, Nicolas; Ivarsson, Niklas; Venckunas, Tomas; Neyroud, Daria; Brazaitis, Marius; Cheng, Arthur J.; Ochala, Julien; Kamandulis, Sigitas; Girard, Sebastien; Volungevičius, Gintautas; Paužas, Henrikas; Mekideche, Abdelhafid; Kayser, Bengt; Martinez-Redondo, Vicente; Ruas, Jorge L.; Bruton, Joseph; Truffert, Andre; Lanner, Johanna T.; Skurvydas, Albertas; Westerblad, Håkan.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 50, 15.12.2015, p. 15492-15497.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Place, N, Ivarsson, N, Venckunas, T, Neyroud, D, Brazaitis, M, Cheng, AJ, Ochala, J, Kamandulis, S, Girard, S, Volungevičius, G, Paužas, H, Mekideche, A, Kayser, B, Martinez-Redondo, V, Ruas, JL, Bruton, J, Truffert, A, Lanner, JT, Skurvydas, A & Westerblad, H 2015, 'Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise', Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 50, pp. 15492-15497. https://doi.org/10.1073/pnas.1507176112

APA

Place, N., Ivarsson, N., Venckunas, T., Neyroud, D., Brazaitis, M., Cheng, A. J., Ochala, J., Kamandulis, S., Girard, S., Volungevičius, G., Paužas, H., Mekideche, A., Kayser, B., Martinez-Redondo, V., Ruas, J. L., Bruton, J., Truffert, A., Lanner, J. T., Skurvydas, A., & Westerblad, H. (2015). Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise. Proceedings of the National Academy of Sciences of the United States of America, 112(50), 15492-15497. https://doi.org/10.1073/pnas.1507176112

Vancouver

Place N, Ivarsson N, Venckunas T, Neyroud D, Brazaitis M, Cheng AJ et al. Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise. Proceedings of the National Academy of Sciences of the United States of America. 2015 Dec 15;112(50):15492-15497. https://doi.org/10.1073/pnas.1507176112

Author

Place, Nicolas ; Ivarsson, Niklas ; Venckunas, Tomas ; Neyroud, Daria ; Brazaitis, Marius ; Cheng, Arthur J. ; Ochala, Julien ; Kamandulis, Sigitas ; Girard, Sebastien ; Volungevičius, Gintautas ; Paužas, Henrikas ; Mekideche, Abdelhafid ; Kayser, Bengt ; Martinez-Redondo, Vicente ; Ruas, Jorge L. ; Bruton, Joseph ; Truffert, Andre ; Lanner, Johanna T. ; Skurvydas, Albertas ; Westerblad, Håkan. / Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 50. pp. 15492-15497.

Bibtex

@article{53da1bcc2dd9439c9ca486295c2c44ba,
title = "Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise",
abstract = "High-intensity interval training (HIIT) is a time-efficient way of improving physical performance in healthy subjects and in patients with common chronic diseases, but less so in elite endurance athletes. The mechanisms underlying the effectiveness of HIIT are uncertain. Here, recreationally active human subjects performed highly demanding HIIT consisting of 30-s bouts of all-out cycling with 4-min rest in between bouts (≤3 min total exercise time). Skeletal muscle biopsies taken 24 h after the HIIT exercise showed an extensive fragmentation of the sarcoplasmic reticulum (SR) Ca2+ release channel, the ryanodine receptor type 1 (RyR1). The HIIT exercise also caused a prolonged force depression and triggered major changes in the expression of genes related to endurance exercise. Subsequent experiments on elite endurance athletes performing the same HIIT exercise showed no RyR1 fragmentation or prolonged changes in the expression of endurance-related genes. Finally, mechanistic experiments performed on isolated mouse muscles exposed to HIIT-mimicking stimulation showed reactive oxygen/nitrogen species (ROS)-dependent RyR1 fragmentation, calpain activation, increased SR Ca2+ leak at rest, and depressed force production due to impaired SR Ca2+ release upon stimulation. In conclusion, HIIT exercise induces a ROS-dependent RyR1 fragmentation in muscles of recreationally active subjects, and the resulting changes in muscle fiber Ca2+-handling trigger muscular adaptations. However, the same HIIT exercise does not cause RyR1 fragmentation in muscles of elite endurance athletes, which may explain why HIIT is less effective in this group.",
keywords = "Ca, High-intensity exercise, Reactive oxygen species, Ryanodine receptor 1, Skeletal muscle",
author = "Nicolas Place and Niklas Ivarsson and Tomas Venckunas and Daria Neyroud and Marius Brazaitis and Cheng, {Arthur J.} and Julien Ochala and Sigitas Kamandulis and Sebastien Girard and Gintautas Volungevi{\v c}ius and Henrikas Pau{\v z}as and Abdelhafid Mekideche and Bengt Kayser and Vicente Martinez-Redondo and Ruas, {Jorge L.} and Joseph Bruton and Andre Truffert and Lanner, {Johanna T.} and Albertas Skurvydas and H{\aa}kan Westerblad",
year = "2015",
month = dec,
day = "15",
doi = "10.1073/pnas.1507176112",
language = "English",
volume = "112",
pages = "15492--15497",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "The National Academy of Sciences of the United States of America",
number = "50",

}

RIS

TY - JOUR

T1 - Ryanodine receptor fragmentation and sarcoplasmic reticulum Ca2+ leak after one session of High-intensity interval exercise

AU - Place, Nicolas

AU - Ivarsson, Niklas

AU - Venckunas, Tomas

AU - Neyroud, Daria

AU - Brazaitis, Marius

AU - Cheng, Arthur J.

AU - Ochala, Julien

AU - Kamandulis, Sigitas

AU - Girard, Sebastien

AU - Volungevičius, Gintautas

AU - Paužas, Henrikas

AU - Mekideche, Abdelhafid

AU - Kayser, Bengt

AU - Martinez-Redondo, Vicente

AU - Ruas, Jorge L.

AU - Bruton, Joseph

AU - Truffert, Andre

AU - Lanner, Johanna T.

AU - Skurvydas, Albertas

AU - Westerblad, Håkan

PY - 2015/12/15

Y1 - 2015/12/15

N2 - High-intensity interval training (HIIT) is a time-efficient way of improving physical performance in healthy subjects and in patients with common chronic diseases, but less so in elite endurance athletes. The mechanisms underlying the effectiveness of HIIT are uncertain. Here, recreationally active human subjects performed highly demanding HIIT consisting of 30-s bouts of all-out cycling with 4-min rest in between bouts (≤3 min total exercise time). Skeletal muscle biopsies taken 24 h after the HIIT exercise showed an extensive fragmentation of the sarcoplasmic reticulum (SR) Ca2+ release channel, the ryanodine receptor type 1 (RyR1). The HIIT exercise also caused a prolonged force depression and triggered major changes in the expression of genes related to endurance exercise. Subsequent experiments on elite endurance athletes performing the same HIIT exercise showed no RyR1 fragmentation or prolonged changes in the expression of endurance-related genes. Finally, mechanistic experiments performed on isolated mouse muscles exposed to HIIT-mimicking stimulation showed reactive oxygen/nitrogen species (ROS)-dependent RyR1 fragmentation, calpain activation, increased SR Ca2+ leak at rest, and depressed force production due to impaired SR Ca2+ release upon stimulation. In conclusion, HIIT exercise induces a ROS-dependent RyR1 fragmentation in muscles of recreationally active subjects, and the resulting changes in muscle fiber Ca2+-handling trigger muscular adaptations. However, the same HIIT exercise does not cause RyR1 fragmentation in muscles of elite endurance athletes, which may explain why HIIT is less effective in this group.

AB - High-intensity interval training (HIIT) is a time-efficient way of improving physical performance in healthy subjects and in patients with common chronic diseases, but less so in elite endurance athletes. The mechanisms underlying the effectiveness of HIIT are uncertain. Here, recreationally active human subjects performed highly demanding HIIT consisting of 30-s bouts of all-out cycling with 4-min rest in between bouts (≤3 min total exercise time). Skeletal muscle biopsies taken 24 h after the HIIT exercise showed an extensive fragmentation of the sarcoplasmic reticulum (SR) Ca2+ release channel, the ryanodine receptor type 1 (RyR1). The HIIT exercise also caused a prolonged force depression and triggered major changes in the expression of genes related to endurance exercise. Subsequent experiments on elite endurance athletes performing the same HIIT exercise showed no RyR1 fragmentation or prolonged changes in the expression of endurance-related genes. Finally, mechanistic experiments performed on isolated mouse muscles exposed to HIIT-mimicking stimulation showed reactive oxygen/nitrogen species (ROS)-dependent RyR1 fragmentation, calpain activation, increased SR Ca2+ leak at rest, and depressed force production due to impaired SR Ca2+ release upon stimulation. In conclusion, HIIT exercise induces a ROS-dependent RyR1 fragmentation in muscles of recreationally active subjects, and the resulting changes in muscle fiber Ca2+-handling trigger muscular adaptations. However, the same HIIT exercise does not cause RyR1 fragmentation in muscles of elite endurance athletes, which may explain why HIIT is less effective in this group.

KW - Ca

KW - High-intensity exercise

KW - Reactive oxygen species

KW - Ryanodine receptor 1

KW - Skeletal muscle

UR - http://www.scopus.com/inward/record.url?scp=84950341491&partnerID=8YFLogxK

U2 - 10.1073/pnas.1507176112

DO - 10.1073/pnas.1507176112

M3 - Journal article

C2 - 26575622

AN - SCOPUS:84950341491

VL - 112

SP - 15492

EP - 15497

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 50

ER -

ID: 245662634