Microvascular Function Is Impaired after Short-Term Immobilization in Healthy Men.
6-Ketoprostaglandin F1 alpha
/ blood
Endothelium, Vascular
/ physiology
Epoprostenol
/ blood
Humans
Immobilization
/ adverse effects
Leg
/ blood supply
Male
Microcirculation
/ physiology
Muscle Proteins
/ metabolism
Muscle, Smooth, Vascular
/ physiology
Norepinephrine
/ blood
Physical Conditioning, Human
/ physiology
Regional Blood Flow
Time Factors
Vasoconstriction
/ physiology
Vasodilation
/ physiology
Young Adult
Journal
Medicine and science in sports and exercise
ISSN: 1530-0315
Titre abrégé: Med Sci Sports Exerc
Pays: United States
ID NLM: 8005433
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
pubmed:
5
6
2020
medline:
9
3
2021
entrez:
5
6
2020
Statut:
ppublish
Résumé
We examined whether 2 wk of one-leg immobilization would impair leg microvascular function and to what extent a subsequent period of intense aerobic cycle training could restore function. Study participants were healthy young men (n = 12; 20-24 yr of age). Leg microvascular function was determined before the intervention, after the immobilization period, and after a 4-wk exercise training period. Microvascular function was assessed as the vasodilator response to intra-arterial infusion of acetylcholine and sodium nitroprusside and as the vasoconstrictor response to endogenous noradrenaline release induced by tyramine infusion. Vasodilator enzymes as well as prooxidant and antioxidant enzymes were assessed by protein analysis in skeletal muscle samples: endothelial nitric oxide synthase, NADPH oxidase (NOX p67 and NOX gp91), and superoxide dismutase 2 (SOD2). The acetylcholine-induced change in vascular conductance was reduced after the 2 wk of immobilization (P = 0.003), tended to increase (P = 0.061), and was back to baseline levels after the subsequent 4 wk of exercise training. Plasma prostacyclin levels in response to acetylcholine infusion were lower after immobilization than before (P = 0.041). The changes in vascular conductance with sodium nitroprusside and tyramine were similar during all conditions. Skeletal muscle protein levels of endothelial nitric oxide synthase in the experimental leg were unchanged with immobilization and subsequent training but increased 47% in the control leg with training (P = 0.002). NOX p67, NOX gp91, and SOD2 in the experimental leg remained unaltered with immobilization, and SOD2 was higher than preimmobilization after 4 wk of training (P < 0.001). The study shows that 2 wk of immobilization impairs leg microvascular endothelial function and prostacyclin formation but that 4 wk of intense aerobic exercise training restores the function. The underlying mechanism may reside in the prostacyclin system.
Identifiants
pubmed: 32496738
doi: 10.1249/MSS.0000000000002369
pii: 00005768-202010000-00006
doi:
Substances chimiques
Muscle Proteins
0
6-Ketoprostaglandin F1 alpha
58962-34-8
Epoprostenol
DCR9Z582X0
Norepinephrine
X4W3ENH1CV
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2107-2116Références
Wall BT, Dirks ML, van Loon LJH. Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia. Ageing Res Rev. 2013;12(4):898–906.
Hvid L, Aagaard P, Justesen L, et al. Effects of aging on muscle mechanical function and muscle fiber morphology during short-term immobilization and subsequent retraining. J Appl Physiol. 2010;109(6):1628–34.
Hvid LG, Suetta C, Nielsen JH, et al. Aging impairs the recovery in mechanical muscle function following 4 days of disuse. Exp Gerontol. 2014;52:1–8.
Hesse C, Siedler H, Luntz SP, et al. Modulation of endothelial and smooth muscle function by bed rest and hypoenergetic, low-fat nutrition. J Appl Physiol. 2005;99(6):2196–203.
Birk GK, Dawson EA, Timothy Cable N, Green DJ, Thijssen DH. Effect of unilateral forearm inactivity on endothelium-dependent vasodilator function in humans. Eur J Appl Physiol. 2013;113(4):933–40.
Hamburg NM, McMackin CJ, Huang AL, et al. Physical inactivity rapidly induces insulin resistance and microvascular dysfunction in healthy volunteers. Arterioscler Thromb Vasc Biol. 2007;27(12):2650–6.
Rakobowchuk M, Crozier J, Glover EI, et al. Short-term unilateral leg immobilization alters peripheral but not central arterial structure and function in healthy young humans. Eur J Appl Physiol. 2011;111(2):203–10.
Bleeker MW, De Groot PC, Poelkens F, Rongen GA, Smits P, Hopman MT. Vascular adaptation to 4 wk of deconditioning by unilateral lower limb suspension. Am J Physiol Heart Circ Physiol. 2005;288(4):H1747–55.
Marshall JJ, Kontos HA. Endothelium-derived relaxing factors. A perspective from in vivo data. Hypertension. 1990;16(4):371–86.
Boushel R. Metabolic control of muscle blood flow during exercise in humans. Can J Appl Physiol. 2003;28(5):754–73.
Jasperse JL, Woodman CR, Price EM, Hasser EM, Laughlin MH. Hindlimb unweighting decreases ecNOS gene expression and endothelium-dependent dilation in rat soleus feed arteries. J Appl Physiol. 1999;87(4):1476–82.
Suvorava T, Lauer N, Harm PD, Kojda G, Harm PD. Physical inactivity causes endothelial dysfunction in healthy young mice. J Am Coll Cardiol. 2004;44(6):1320–7.
Lawler JM, Song W, Demaree SR. Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med. 2003;35(1):9–16.
Gram M, Vigelsø A, Yokota T, Helge JW, Dela F, Hey-Mogensen M. Skeletal muscle mitochondrial H2 O2 emission increases with immobilization and decreases after aerobic training in young and older men. J Physiol. 2015;593(17):4011–27.
Schulz E, Jansen T, Wenzel P, Daiber A, Münzel T. Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension. Antioxid Redox Signal. 2008;10(6):1115–26.
Gluais P, Lonchampt M, Morrow JD, Vanhoutte PM, Feletou M. Acetylcholine-induced endothelium-dependent contractions in the SHR aorta: the Janus face of prostacyclin. Br J Pharmacol. 2005;146(6):834–45.
Li H, Horke S, Förstermann U. Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis. 2014;237(1):208–19.
Wiegman DL, Harris PD, Joshua IG, Miller FN. Decreased vascular sensitivity to norepinephrine following exercise training. J Appl Physiol. 1981;51(2):282–7.
Mortensen SP, Nyberg M, Gliemann L, Thaning P, Saltin B, Hellsten Y. Exercise training modulates functional sympatholysis and α-adrenergic vasoconstrictor responsiveness in hypertensive and normotensive individuals. J Physiol. 2014;592(14):3063–73.
Mortensen SP, Morkeberg J, Thaning P, Hellsten Y, Saltin B. Two weeks of muscle immobilization impairs functional sympatholysis but increases exercise hyperemia and the vasodilatory responsiveness to infused ATP. Am J Physiol Heart Circ Physiol. 2012;302(10):H2074–82.
Francis AA, Pierce GN. An integrated approach for the mechanisms responsible for atherosclerotic plaque regression. Exp Clin Cardiol. 2011;16(3):77–86.
Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest. 1975;35(7):609–16.
Altman D. How large a sample? BMJ. 1980;281(6251):1336–8.
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4 [Internet]. J Stat Softw. 2015;67(1). Available from: http://arxiv.org/abs/1406.5823. doi:10.18637/jss.v067.i01.
doi: 10.18637/jss.v067.i01
Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50(3):346–63.
Nyberg M, Egelund J, Mandrup CM, et al. Early postmenopausal phase is associated with reduced prostacyclin-induced vasodilation that is reversed by exercise training. Hypertension. 2016;68(4):1011–20.
Gliemann L, Rytter N, Tamariz-Ellemann A, et al. Lifelong physical activity determines vascular function in late postmenopausal women. Med Sci Sports Exerc. 2020;52(3):627–36.
Gabriella Doni M, Whittle BJ, Palmer RM, Moncada S. Actions of nitric oxide on the release of prostacyclin from bovine endothelial cells in culture. Eur J Pharmacol. 1988;151(1):19–25.
Gryglewski RJ, Palmer RM, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature. 1986;320(6061):454–6.
Donato AJ, Eskurza I, Silver AE, et al. Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-kappaB. Circ Res. 2007;100(11):1659–66.
Hoier B, Nordsborg N, Andersen S, et al. Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol. 2012;590(3):595–606.
Cocks M, Shaw CS, Shepherd SO, et al. Sprint interval and moderate-intensity continuous training have equal benefits on aerobic capacity, insulin sensitivity, muscle capillarisation and endothelial eNOS/NAD(P)Hoxidase protein ratio in obese men. J Physiol. 2016;594(8):2307–21.
Gliemann L, Schmidt JF, Olesen J, et al. Resveratrol blunts the positive effects of exercise training on cardiovascular health in aged men. J Physiol. 2013;591(20):5047–59.
Hellsten Y, Jensen L, Thaning P, Nyberg M, Mortensen S. Impaired formation of vasodilators in peripheral tissue in essential hypertension is normalized by exercise training: role of adenosine and prostacyclin. J Hypertens. 2012;30(10):2007–14.
Mortensen SP, Nyberg M, Winding K, Saltin B. Lifelong physical activity preserves functional sympatholysis and purinergic signalling in the ageing human leg. J Physiol. 2012;590(23):6227–36.
Limberg JK, Casey DP, Trinity JD, et al. Assessment of resistance vessel function in human skeletal muscle: guidelines for experimental design, Doppler ultrasound, and pharmacology. Am J Physiol Heart Circ Physiol. 2020;318(2):H301–25.
Hellsten Y, Gliemann L. Limb vascular function in women-effects of female sex hormones and physical activity. Transl Sports Med. 2018;1(1):14–24.