Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle

We recently reported that the greatest distinguishing feature between eccentric (ECC) and concentric (CON) muscle loading lays in architectural adaptations: ECC favors increases in fascicle length (Lf), associated with distal vastus lateralis muscle (VL) hypertrophy, and CON increases in pennation a...

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Main Authors: Franchi, Martino V., Wilkinson, Daniel J., Quinlan, Jonathan I., Mitchell, William K., Lund, Jonathan N., Williams, John P., Reeves, Neil D., Smith, Kenneth, Atherton, Philip J., Narici, Marco V.
Format: Article
Published: Wiley 2015
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Online Access:https://eprints.nottingham.ac.uk/44533/
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author Franchi, Martino V.
Wilkinson, Daniel J.
Quinlan, Jonathan I.
Mitchell, William K.
Lund, Jonathan N.
Williams, John P.
Reeves, Neil D.
Smith, Kenneth
Atherton, Philip J.
Narici, Marco V.
author_facet Franchi, Martino V.
Wilkinson, Daniel J.
Quinlan, Jonathan I.
Mitchell, William K.
Lund, Jonathan N.
Williams, John P.
Reeves, Neil D.
Smith, Kenneth
Atherton, Philip J.
Narici, Marco V.
author_sort Franchi, Martino V.
building Nottingham Research Data Repository
collection Online Access
description We recently reported that the greatest distinguishing feature between eccentric (ECC) and concentric (CON) muscle loading lays in architectural adaptations: ECC favors increases in fascicle length (Lf), associated with distal vastus lateralis muscle (VL) hypertrophy, and CON increases in pennation angle (PA). Here, we explored the interactions between structural and morphological remodeling, assessed by ultrasound and dual x‐ray absorptiometry (DXA), and long‐term muscle protein synthesis (MPS), evaluated by deuterium oxide (D2O) tracing technique. Ten young males (23 ± 4 years) performed unilateral resistance exercise training (RET) three times/week for 4 weeks; thus, one‐leg trained concentrically while the contralateral performed ECC exercise only at 80% of either CON or ECC one repetition maximum (1RM). Subjects consumed an initial bolus of D2O (150 mL), while a 25‐mL dose was thereafter provided every 8 days. Muscle biopsies from VL midbelly (MID) and distal myotendinous junction (MTJ) were collected at 0 and 4‐weeks. MPS was then quantified via GC–pyrolysis–IRMS over the 4‐week training period. Expectedly, ECC and CON RET resulted in similar increases in VL muscle thickness (MT) (7.5% vs. 8.4%, respectively) and thigh lean mass (DXA) (2.3% vs. 3%, respectively), albeit through distinct remodeling: Lf increasing more after ECC (5%) versus CON (2%) and PA increasing after CON (7% vs. 3%). MPS did not differ between contractile modes or biopsy sites (MID‐ECC: 1.42 vs. MID‐CON: 1.4% day−1; MTJ‐ECC: 1.38 vs. MTJ‐CON: 1.39% day−1). Muscle thickness at MID site increased similarly following ECC and CON RET, reflecting a tendency for a contractile mode‐independent correlation between MPS and MT (P = 0.07; R2 = 0.18). We conclude that, unlike MT, distinct structural remodeling responses to ECC or CON are not reflected in MPS; the molecular mechanisms of distinct protein deposition, and/or the role of protein breakdown in mediating these responses remain to be defined.
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spelling nottingham-445332020-05-04T17:23:37Z https://eprints.nottingham.ac.uk/44533/ Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle Franchi, Martino V. Wilkinson, Daniel J. Quinlan, Jonathan I. Mitchell, William K. Lund, Jonathan N. Williams, John P. Reeves, Neil D. Smith, Kenneth Atherton, Philip J. Narici, Marco V. We recently reported that the greatest distinguishing feature between eccentric (ECC) and concentric (CON) muscle loading lays in architectural adaptations: ECC favors increases in fascicle length (Lf), associated with distal vastus lateralis muscle (VL) hypertrophy, and CON increases in pennation angle (PA). Here, we explored the interactions between structural and morphological remodeling, assessed by ultrasound and dual x‐ray absorptiometry (DXA), and long‐term muscle protein synthesis (MPS), evaluated by deuterium oxide (D2O) tracing technique. Ten young males (23 ± 4 years) performed unilateral resistance exercise training (RET) three times/week for 4 weeks; thus, one‐leg trained concentrically while the contralateral performed ECC exercise only at 80% of either CON or ECC one repetition maximum (1RM). Subjects consumed an initial bolus of D2O (150 mL), while a 25‐mL dose was thereafter provided every 8 days. Muscle biopsies from VL midbelly (MID) and distal myotendinous junction (MTJ) were collected at 0 and 4‐weeks. MPS was then quantified via GC–pyrolysis–IRMS over the 4‐week training period. Expectedly, ECC and CON RET resulted in similar increases in VL muscle thickness (MT) (7.5% vs. 8.4%, respectively) and thigh lean mass (DXA) (2.3% vs. 3%, respectively), albeit through distinct remodeling: Lf increasing more after ECC (5%) versus CON (2%) and PA increasing after CON (7% vs. 3%). MPS did not differ between contractile modes or biopsy sites (MID‐ECC: 1.42 vs. MID‐CON: 1.4% day−1; MTJ‐ECC: 1.38 vs. MTJ‐CON: 1.39% day−1). Muscle thickness at MID site increased similarly following ECC and CON RET, reflecting a tendency for a contractile mode‐independent correlation between MPS and MT (P = 0.07; R2 = 0.18). We conclude that, unlike MT, distinct structural remodeling responses to ECC or CON are not reflected in MPS; the molecular mechanisms of distinct protein deposition, and/or the role of protein breakdown in mediating these responses remain to be defined. Wiley 2015-11-12 Article PeerReviewed Franchi, Martino V., Wilkinson, Daniel J., Quinlan, Jonathan I., Mitchell, William K., Lund, Jonathan N., Williams, John P., Reeves, Neil D., Smith, Kenneth, Atherton, Philip J. and Narici, Marco V. (2015) Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle. Physiological Reports, 3 (11). e12593/1-e12593/11. ISSN 2051-817X Exercise; hypertrophy; metabolism; muscle architecture; protein synthesis https://doi.org/10.14814/phy2.12593 doi:10.14814/phy2.12593 doi:10.14814/phy2.12593
spellingShingle Exercise; hypertrophy; metabolism; muscle architecture; protein synthesis
Franchi, Martino V.
Wilkinson, Daniel J.
Quinlan, Jonathan I.
Mitchell, William K.
Lund, Jonathan N.
Williams, John P.
Reeves, Neil D.
Smith, Kenneth
Atherton, Philip J.
Narici, Marco V.
Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
title Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
title_full Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
title_fullStr Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
title_full_unstemmed Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
title_short Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
title_sort early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle
topic Exercise; hypertrophy; metabolism; muscle architecture; protein synthesis
url https://eprints.nottingham.ac.uk/44533/
https://eprints.nottingham.ac.uk/44533/
https://eprints.nottingham.ac.uk/44533/