Patrick J Ferrara1,2,3, Anthony R P Verkerke1,2,3, Jeffrey J Brault4,5,6, Katsuhiko Funai1,2,3,4,5,6,7. 1. Diabetes & Metabolism Research Center, University of Utah, Salt Lake City, UT. 2. Department of Physical Therapy & Athletic Training, University of Utah, Salt Lake City, UT. 3. Department of Nutrition & Integrative Physiology, University of Utah, Salt Lake City, UT. 4. Department of Kinesiology, East Carolina University, Greenville, NC. 5. Department of Physiology, East Carolina University, Greenville, NC. 6. East Carolina Diabetes & Obesity Institute, East Carolina University, Greenville, NC. 7. Molecular Medicine Program, University of Utah, Salt Lake City, UT.
Abstract
INTRODUCTION: Evidence suggests that the energy efficiency of key ATPases involved in skeletal muscle contractile activity is improved in a hypothermic condition. However, it is unclear how a decrease in temperature affects skeletal muscle O2 consumption (mVO2) induced by muscle contraction. METHODS: Isolated mouse extensor digitorum longus (EDL) muscles were incubated in a temperature-controlled (37°C or 25°C) bath that included an O2 probe. EDL muscles from one limb were subjected to the measurement of resting mVO2, and the contralateral EDL muscles were used for the measurement of mVO2 with electrically stimulated contraction. For the resting protocol, muscles were suspended at resting tension for 15 min with continuous O2 recordings. For the contraction protocol, EDL muscles underwent 10 electrically stimulated isometric contractions with continuous O2 recordings for 15 min. The rate of O2 disappearance was quantified as micromoles of O2 per minute and normalized to the wet weight of the muscle. RESULTS: Resting mVO2 was greater at 37°C than at 25°C, consistent with the idea that lower temperature reduces basal metabolic rate. Electrically stimulated contraction robustly increased mVO2 at both 37°C and 25°C, which was sustained for ~3 min postcontraction. During that period, mVO2 was elevated approximately fivefold at both 37°C and 25°C. Greater contraction-induced mVO2 at 37°C compared with 25°C occurred despite lower force generated at 37°C than at 25°C. CONCLUSIONS: Together, O2 cost for muscle contraction (force-time integral per O2 consumed) was greater at 37°C than at 25°C. Levels of high-energy phosphates were consistent with greater energy demand at 37°C compared with 25°C. In conclusion, these results indicate that muscle contraction that occurs at subnormal temperature requires less O2 than at 37°C.
INTRODUCTION: Evidence suggests that the energy efficiency of key ATPases involved in skeletal muscle contractile activity is improved in a hypothermic condition. However, it is unclear how a decrease in temperature affects skeletal muscle O2 consumption (mVO2) induced by muscle contraction. METHODS: Isolated mouse extensor digitorum longus (EDL) muscles were incubated in a temperature-controlled (37°C or 25°C) bath that included an O2 probe. EDL muscles from one limb were subjected to the measurement of resting mVO2, and the contralateral EDL muscles were used for the measurement of mVO2 with electrically stimulated contraction. For the resting protocol, muscles were suspended at resting tension for 15 min with continuous O2 recordings. For the contraction protocol, EDL muscles underwent 10 electrically stimulated isometric contractions with continuous O2 recordings for 15 min. The rate of O2 disappearance was quantified as micromoles of O2 per minute and normalized to the wet weight of the muscle. RESULTS: Resting mVO2 was greater at 37°C than at 25°C, consistent with the idea that lower temperature reduces basal metabolic rate. Electrically stimulated contraction robustly increased mVO2 at both 37°C and 25°C, which was sustained for ~3 min postcontraction. During that period, mVO2 was elevated approximately fivefold at both 37°C and 25°C. Greater contraction-induced mVO2 at 37°C compared with 25°C occurred despite lower force generated at 37°C than at 25°C. CONCLUSIONS: Together, O2 cost for muscle contraction (force-time integral per O2 consumed) was greater at 37°C than at 25°C. Levels of high-energy phosphates were consistent with greater energy demand at 37°C compared with 25°C. In conclusion, these results indicate that muscle contraction that occurs at subnormal temperature requires less O2 than at 37°C.
Authors: Catherine L Ward; Benjamin T Corona; James J Yoo; Benjamin S Harrison; George J Christ Journal: PLoS One Date: 2013-08-26 Impact factor: 3.240
Authors: Hiroaki Eshima; Piyarat Siripoksup; Ziad S Mahmassani; Jordan M Johnson; Patrick J Ferrara; Anthony R P Verkerke; Anahy Salcedo; Micah J Drummond; Katsuhiko Funai Journal: J Appl Physiol (1985) Date: 2020-06-18
Authors: Patrick J Ferrara; Anthony R P Verkerke; J Alan Maschek; Justin L Shahtout; Piyarat Siripoksup; Hiroaki Eshima; Jordan M Johnson; Jonathan J Petrocelli; Ziad S Mahmassani; Thomas D Green; Joseph M McClung; James E Cox; Micah J Drummond; Katsuhiko Funai Journal: FASEB J Date: 2021-10 Impact factor: 5.834
Authors: Jonathan J Petrocelli; Ziad S Mahmassani; Dennis K Fix; Jessie A Montgomery; Paul T Reidy; Alec I McKenzie; Naomi M de Hart; Patrick J Ferrara; Joshua J Kelley; Hiroaki Eshima; Katsuhiko Funai; Micah J Drummond Journal: FASEB J Date: 2021-09 Impact factor: 5.834
Authors: Patrick J Ferrara; Xin Rong; J Alan Maschek; Anthony Rp Verkerke; Piyarat Siripoksup; Haowei Song; Thomas D Green; Karthickeyan C Krishnan; Jordan M Johnson; John Turk; Joseph A Houmard; Aldons J Lusis; Micah J Drummond; Joseph M McClung; James E Cox; Saame Raza Shaikh; Peter Tontonoz; William L Holland; Katsuhiko Funai Journal: J Clin Invest Date: 2021-04-15 Impact factor: 19.456
Authors: Anthony R P Verkerke; Patrick J Ferrara; Chien-Te Lin; Jordan M Johnson; Terence E Ryan; J Alan Maschek; Hiroaki Eshima; Christopher W Paran; Brenton T Laing; Piyarat Siripoksup; Trevor S Tippetts; Edward J Wentzler; Hu Huang; Espen E Spangenburg; Jeffrey J Brault; Claudio J Villanueva; Scott A Summers; William L Holland; James E Cox; Dennis E Vance; P Darrell Neufer; Katsuhiko Funai Journal: Nat Metab Date: 2019-09-16
Authors: Timothy D Heden; Jordan M Johnson; Patrick J Ferrara; Hiroaki Eshima; Anthony R P Verkerke; Edward J Wentzler; Piyarat Siripoksup; Tara M Narowski; Chanel B Coleman; Chien-Te Lin; Terence E Ryan; Paul T Reidy; Lisandra E de Castro Brás; Courtney M Karner; Charles F Burant; J Alan Maschek; James E Cox; Douglas G Mashek; Gabrielle Kardon; Sihem Boudina; Tonya N Zeczycki; Jared Rutter; Saame Raza Shaikh; Jean E Vance; Micah J Drummond; P Darrell Neufer; Katsuhiko Funai Journal: Sci Adv Date: 2019-09-11 Impact factor: 14.136