Effects of exercise-induced intracellular
acidosis on the phosphocreatine recovery
kinetics: a
31
P MRS study in three muscle
groups in humans
Gwenael Layec
a,b,c
, Emil Malucelli
d
, Y. Le Fur
a
, David Manners
e
,
Kazuya Yashiro
a
, Claudia Testa
e
, Patrick J. Cozzone
a
, Stefano Iotti
d,f
and David Bendahan
a
*
Little is known about the metabolic differences that exist among different muscle groups within the same subjects.
Therefore, we used
31
P-magnetic resonance spectroscopy (
31
P-MRS) to investigate muscle oxidative capacity and the
potential effects of pH on PCr recovery kinetics between muscles of different phenotypes (quadriceps (Q), finger (FF)
and plantar flexors (PF)) in the same cohort of 16 untrained adults. The estimated muscle oxidative capacity was
lower in Q (29 12 mM min
-1
, CV
inter-subject
= 42%) as compared with PF (46 20 mM min
-1
, CV
inter-subject
= 44%)
and tended to be higher in FF (43 35 mM min
-1
, CV
inter-subject
= 80%). The coefficient of variation (CV) of oxidative
capacity between muscles within the group was 59 24%. PCr recovery time constant was correlated with
end-exercise pH in Q (p < 0.01), FF ( p < 0.05) and PF ( p <0.05) as well as proton efflux rate in FF ( p < 0.01),
PF ( p < 0.01) and Q ( p = 0.12). We also observed a steeper slope of the relationship between end-exercise acidosis
and PCr recovery kinetics in FF compared with either PF or Q muscles. Overall, this study supports the concept of
skeletal muscle heterogeneity by revealing a comparable inter- and intra-individual variability in oxidative capacity
across three skeletal muscles in untrained individuals. These findings also indicate that the sensitivity of mitochondrial
respiration to the inhibition associated with cytosolic acidosis is greater in the finger flexor muscles compared with
locomotor muscles, which might be related to differences in permeability in the mitochondrial membrane and, to some
extent, to proton efflux rates. Copyright © 2013 John Wiley & Sons, Ltd.
Keywords: mitochondrial function; muscle oxidative capacity; magnetic resonance spectroscopy; exercise; skeletal muscle;
muscle acidosis
INTRODUCTION
It has been largely acknowledged that muscle oxidative capacity
can vary according to daily-level physical activity (1). Among the
corresponding changes, a variety of metabolic and cardiovascular
changes including reduced utilization of muscle glycogen and
exercise-induced lactate production at a given exercise intensity,
increased capillary and mitochondrial densities as well as mito-
chondrial enzymatic activities has been reported (1). However,
while differences in muscle oxidative capacity have been related
to variations in physical fitness (2–4), little is known about the po-
tential differences among muscles exposed to different chronic
load for a given subject (5,6). Likewise, the effects of exercise-
induced acidosis on measured oxidative capacity have been
addressed for a given muscle, but the corresponding effects on dif-
ferent muscles of a given subject remain to be clearly documented.
* Correspondence to: D. Bendahan, Centre de Resonance Magnetique
Biologique et Medicale, UMR CNRS 6612, Faculté de Médecine de Marseille,
Marseille, France.
E-mail: david.bendahan@univmed.fr
a G. Layec, Y. Le Fur, K. Yashiro, P. J. Cozzone, D. Bendahan
Centre de Resonance Magnetique Biologique et Medicale, UMR CNRS 6612,
Faculté de Médecine de Marseille, Marseille, France
b G. Layec
Department of Medicine, Division of Geriatrics, University of Utah, Salt Lake
City, UT, USA
c G. Layec
Geriatric Research, Education, and Clinical Center, George E. Whalen VA
Medical Center, Salt Lake City, UT, USA
d E. Malucelli, S. Iotti
Dipartimento di Farmacia e Biotecnologie dell’Invecchiamento e Malattie
Nefrologiche, Università di Bologna, Italy
e D. Manners, C. Testa
Dipartimento di Scienze Biomediche e Neuromotorie dell’Invecchiamento e
Malattie Nefrologiche, Università di Bologna, Italy
f S. Iotti
Istituto Nazionale Biostrutture e Biosistemi, Rome, Italy
Abbreviations used:
31
P-MRS,
31
P magnetic resonance spectroscopy; PCr,
phosphocreatine; Pi, inorganic phosphate; ADP, adenosine diphosphate;
MVC, maximum isometric force; Τc, time constant of PCr resynthesis kinetics;
Q
max
, oxidative capacity; Q
b
, basal rate of ATP synthesis; K
m
, affinity
constant.
Research article
Received: 17 August 2012, Revised: 22 March 2013, Accepted: 25 March 2013, Published online in Wiley Online Library: 2013
(wileyonlinelibrary.com) DOI: 10.1002/nbm.2966
NMR Biomed. (2013) Copyright © 2013 John Wiley & Sons, Ltd.