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Comparative Study
. 2012 Aug 15;113(4):557-65.
doi: 10.1152/japplphysiol.00151.2012. Epub 2012 Jun 7.

Exercise training and muscle microvascular oxygenation: functional role of nitric oxide

Daniel M Hirai  1 , Steven W Copp, Scott K Ferguson, Clark T Holdsworth, Danielle J McCullough, Bradley J Behnke, Timothy I Musch, David C Poole
Affiliations
Comparative Study

Exercise training and muscle microvascular oxygenation: functional role of nitric oxide

Daniel M Hirai et al. J Appl Physiol (1985). .

Abstract

Exercise training induces multiple adaptations within skeletal muscle that may improve local O(2) delivery-utilization matching (i.e., Po(2)mv). We tested the hypothesis that increased nitric oxide (NO) function is intrinsic to improved muscle Po(2)mv kinetics from rest to contractions after exercise training. Healthy young Sprague-Dawley rats were assigned to sedentary (n = 18) or progressive treadmill exercise training (n = 10; 5 days/wk, 6-8 wk, final workload of 60 min/day at 35 m/min, -14% grade) groups. Po(2)mv was measured via phosphorescence quenching in the spinotrapezius muscle at rest and during 1-Hz twitch contractions under control (Krebs-Henseleit solution), sodium nitroprusside (SNP, NO donor; 300 μM), and N(G)-nitro-L-arginine methyl ester (l-NAME, nonspecific NO synthase blockade; 1.5 mM) superfusion conditions. Exercise-trained rats had greater peak oxygen uptake (Vo(2 peak)) than their sedentary counterparts (81 ± 1 vs. 72 ± 2 ml · kg(-1) · min(-1), respectively; P < 0.05). Exercise-trained rats had significantly slower Po(2)mv fall throughout contractions (τ(1); time constant for the first component) during control (sedentary: 8.1 ± 0.6; trained: 15.2 ± 2.8 s). Compared with control, SNP slowed τ(1) to a greater extent in sedentary rats (sedentary: 38.7 ± 5.6; trained: 26.8 ± 4.1 s; P > 0.05) whereas l-NAME abolished the differences in τ(1) between sedentary and trained rats (sedentary: 12.0 ± 1.7; trained: 11.2 ± 1.4 s; P < 0.05). Our results indicate that endurance exercise training leads to greater muscle microvascular oxygenation across the metabolic transient following the onset of contractions (i.e., slower Po(2)mv kinetics) partly via increased NO-mediated function, which likely constitutes an important mechanism for training-induced metabolic adaptations.

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Figures

Fig. 1.
Fig. 1.
Results from experiments performed to examine potential cyanide-induced impairment of skeletal muscle function with the current sodium nitroprusside (SNP) superfusion protocol. Three contraction bouts were conducted in the following superfusion order: control 1 (Krebs-Henseleit), SNP (300 μM), control 2 (Krebs-Henseleit). Spinotrapezius O2 pressure within the microvasculature (muscle Po2mv) was measured at rest and throughout contractions (n = 9). Spinotrapezius muscle blood flow (Q̇m) and oxygen utilization (V̇o2) were determined at rest and during the contraction steady state via radiolabeled microspheres and direct Fick calculation, respectively (n = 4). Top panels: spinotrapezius Q̇m and V̇o2 at rest and during the contraction steady state during the first and third bouts (i.e., control 1 and 2, respectively). Bottom panel: spinotrapezius Po2mv at rest and following the onset of contractions under all 3 conditions (control 1, SNP, and control 2). Time zero denotes the onset of contractions. That resting and contracting spinotrapezius muscle V̇o2 did not differ between the first and third bouts (i.e., control 1 vs. control 2; P > 0.05) suggests preserved mitochondrial function post-SNP condition. The possibility of prolonged and/or irreversible vasodilation following the SNP condition is not supported based on similar resting and contraction steady-state Q̇m between the first and third bouts (i.e., control 1 vs. control 2; P > 0.05). Similar Po2mv profiles during the first and third bouts (i.e., control 1 vs. control 2; P > 0.05 for all kinetics parameters) are also consistent with the notion that mitochondrial and vascular control were not impaired following the SNP condition (i.e., second bout). ns, not significantly different.
Fig. 2.
Fig. 2.
Spinotrapezius muscle Po2mv response from representative sedentary and exercise-trained rats under control, SNP, and NG-nitro-l-arginine methyl ester (l-NAME) conditions. Time zero denotes the onset of contractions. Note that exercise training slowed the Po2mv fall during contractions (τ1, time constant for the first component) under the control condition. SNP slowed τ1 to a greater extent in sedentary rats, whereas l-NAME abolished the differences in τ1 between sedentary and trained rats (see text for details).
Fig. 3.
Fig. 3.
Spinotrapezius muscle Po2mv kinetics (top panel: τ1, time constant for the first component; bottom panel: Δ1Po2mv/τ1; relative rate of Po2mv fall) in sedentary and exercise-trained rats under control, SNP, and l-NAME conditions. Significantly different from *control within group; †SNP within group; ‡sedentary within superfusion condition. #P = 0.12 vs. sedentary SNP.
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