Effect of Resistance Training on Microvascular Density and eNOS Content in Skeletal Muscle of Sedentary Men

Microcirculation

Volumn 21, Issue 8, 2014, Pages 738-746

  Cocks, Matthew ^a   Shaw, Christopher S ^b   Shepherd, Sam O ^a   Fisher, James P ^c   Ranasinghe, Aaron M ^c   Barker, Thomas A ^c   Tipton, Kevin D ^d   Wagenmakers, Anton J M ^a  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b VICTORIA UNIVERSITY   (Australia)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Insulin sensitivity; Muscle microvascular endothelial function; NAD(P)Hoxidase; Nitric oxide

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INSULIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; NOS3 PROTEIN, HUMAN;

ADULT; ARTERIAL STIFFNESS; ARTICLE; BIOAVAILABILITY; BLOOD PRESSURE; CAPILLARY DENSITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; INSULIN SENSITIVITY; MALE; MICROVASCULATURE; MUSCLE BIOPSY; QUANTITATIVE ANALYSIS; RESISTANCE TRAINING; SEDENTARY LIFESTYLE; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; BIOSYNTHESIS; CLINICAL TRIAL; ENZYMOLOGY; FITNESS; MICROCIRCULATION; MULTICENTER STUDY; PHOSPHORYLATION; PHYSIOLOGY; VASCULARIZATION;

ADULT; HUMANS; MALE; MICROCIRCULATION; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PHYSICAL FITNESS;

EID: 84910671170     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12155     Document Type: Article

References (45)

1. Barrett EJ, Wang H, Upchurch CT, Liu Z. Insulin regulates its own delivery to skeletal muscle by feed-forward actions on the vasculature. Am J Physiol Endocrinol Metab 301: E252-E263, 2011.
2. Bell GJ, Syrotuik D, Martin TP, Burnham R, Quinney HA. Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentrations in humans. Eur J Appl Physiol 81: 418-427, 2000.
3. Bradley EA, Richards SM, Keske MA, Rattigan S. Local NOS inhibition impairs vascular and metabolic actions of insulin in rat hindleg muscle in vivo. Am J Physiol Endocrinol Metab 305: E745-E750, 2013.
4. Brandes RP, Kreuzer J. Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65: 16-27, 2005.
5. Casey DP, Beck DT, Braith RW. Progressive resistance training without volume increases does not alter arterial stiffness and aortic wave reflection. Exp Biol Med 232: 1228-1235, 2007.
6. Charles M, Charifi N, Verney J, Pichot V, Feasson L, Costes F, Denis C. Effect of endurance training on muscle microvascular filtration capacity and vascular bed morphometry in the elderly. Acta Physiol 187: 399-406, 2006.
7. Chilibeck PD, Syrotuik DG, Bell GJ. The effect of strength training on estimates of mitochondrial density and distribution throughout muscle fibres. Eur J Appl Physiol 80: 604-609, 1999.
8. Cocks M, Shaw CS, Shepherd SO, Fisher J, Ranasinghe AM, Barker TA, Tipton KD, Wagenmakers AJM. High intensity interval and endurance training are equally effective in increasing muscle microvascular density and eNOS content in sedentary males. J Physiol 2012.
9. Cocks M, Shaw CS, Shepherd SO, Fisher JP, Ranasinghe AM, Barker TA, Tipton KD, Wagenmakers AJM. Sprint interval and endurance training are equally effective in increasing muscle microvascular density and eNOS content in sedentary males. J Physiol 591: 641-656, 2013.
10. Cocks M, Shepherd SO, Shaw CS, Achten J, Costa ML, Wagenmakers AJM. Immunofluorescence microscopy to assess enzymes controlling nitric oxide availability and microvascular blood flow in muscle. Microcirculation 19: 642-651, 2012.
11. Cohen J. A power primer. Psychol Bulletin 112: 155-159, 1992.
12. Crecelius AR, Kirby BS, Voyles WF, Dinenno FA. Nitric oxide, but not vasodilating prostaglandins, contributes to the improvement of exercise hyperemia via ascorbic acid in healthy older adults. Am J Physiol Heart Circ Physiol 299: H1633-H1641, 2010.
13. Dube JJ, Amati F, Toledo FGS, Stefanovic-Racic M, Rossi A, Coen P, Goodpaster BH. Effects of weight loss and exercise on insulin resistance, and intramyocellular triacylglycerol, diacylglycerol and ceramide. Diabetologia 54: 1147-1156, 2011.
14. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15, 2011.
15. Frisbee JC. Reduced nitric oxide bioavailability contributes to skeletal muscle microvessel rarefaction in the metabolic syndrome. Am J Physiol Regul Integr Comp Physiol 289: R307-R316, 2005.
16. Gamble J, Gartside IB, Christ F. A reassement of mercury in silastic strain-gauge plethysmography for microvascular permeability assessment in man. J Physiol 464: 407-422, 1993.
17. Green H, Goreham C, Ouyang J, Ball-Burnett M, Ranney D. Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol Regul Integr Comp Physiol 276: R591-R596, 1999.
18. Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, Macera CA, Heath GW, Thompson PD, Bauman A. Physical activity and public health - Updated recommendation for adults from the American college of sports medicine and the American heart association. Circulation 116: 1081-1093, 2007.
19. Heffernan KS, Fahs CA, Iwamoto GA, Jae SY, Wilund KR, Woods JA, Fernhall B. Resistance exercise training reduces central blood pressure and improves microvascular function in African American and white men. Atherosclerosis 207: 220-226, 2009.
20. Hepple RT. A new measurement of tissue capillarity: the capillary-to-fibre perimeter exchange index. Can J Appl Physiol 22: 11-22, 1997.
21. Hepple RT, Mackinnon SLM, Thomas SG, Goodman JM, Plyley MJ. Quantitating the capillary supply and the response to resistance training in older men. Pflugers Arch 433: 238-244, 1997.
22. Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JFP, Dela F. Strength training increases insulin-mediated glucose uptake, GLUT4 content, and insulin signaling in skeletal muscle in patients with type 2 diabetes. Diabetes 53: 294-305, 2004.
23. Hood JD, Meininger CJ, Ziche M, Granger HJ. VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am J Physiol Heart Circ Physiol 274: H1054-H1058, 1998.
24. Hudlicka O, Brown MD, May S, Zakrzewicz A, Pries AR. Changes in capillary shear stress in skeletal muscles exposed to long-term activity: role of nitric oxide. Microcirculation 13: 249-259, 2006.
25. Kraemer WJ, Fry AC. Strength Testing: Development and Evaluation of Methodology. Physiological Assessment of Human Fitness. Champaign, IL: Human Kinetics, 1995.
26. Krisan AD, Collins DE, Crain AM, Kwong CC, Singh MK, Bernard JR, Yaspelkis BB. Resistance training enhances components of the insulin signaling cascade in normal and high-fat-fed rodent skeletal muscle. J Appl Physiol 96: 1691-1700, 2004.
27. Macdougall JD, Sale DG, Moroz JR, Elder GCB, Sutton JR, Howald H. Mitochondrial volume density in human skeletal-muscle following heavy resistance training. Med Sci Sports Exerc 11: 164-166, 1979.
28. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing - Comparison with the euglycemic insulin clamp. Diabetes Care 22: 1462-1470, 1999.
29. McCall GE, Byrnes WC, Dickinson A, Pattany PM, Fleck SJ. Muscle fiber hypertrophy: hyperplasia, and capillary density in college men after resistance training. J Appl Physiol 81: 2004-2012, 1996.
30. Mitchell WK, Phillips BE, Williams JP, Rankin D, Smith K, Lund JN, Atherton PJ. Development of a new Sonovue contrast-enhanced ultrasound approach reveals temporal and age-related features of muscle microvascular responses to feeding. Physiol Rep 1: e00119, 2013.
31. Miyachi M. Effects of resistance training on arterial stiffness: a meta-analysis. Br J Sports Med 47: 393-396, 2012.
32. Okamoto T, Masuhara M, Ikuta K. Effects of muscle contraction timing during resistance training on vascular function. J Hum Hypertens 23: 470-478, 2009.
33. Premilovac D, Bradley EA, Ng HLH, Richards SM, Rattigan S, Keske MA. Muscle insulin resistance resulting from impaired microvascular insulin sensitivity in Sprague Dawley rats. Cardiovasc Res 98: 28-36, 2013.
34. Rakobowchuk M, McGowan CL, de Groot PC, Bruinsma D, Hartman JW, Phillips SM, MacDonald MJ. Effect of whole body resistance training on arterial compliance in young men. Exp Physiol 90: 645-651, 2005.
35. Schrage WG, Wilkins BW, Johnson CP, Eisenach JH, Limberg JK, Dietz NM, Curry TB, Joyner MJ. Roles of nitric oxide synthase and cyclooxygenase in leg vasodilation and oxygen consumption during prolonged low-intensity exercise in untrained humans. J Appl Physiol 109: 768-777, 2007.
36. Shepherd SO, Cocks M, Tipton CM, Witard OC, Ranasinghe AM, Barker TA, Wagenmakers AJM, Shaw CS. Resistance training increases skeletal muscle oxidative capacity and net intramuscular triglyceride breakdown in type I and II fibres of sedentary males. Exp Physiol 99: 894-908, 2014.
37. Silver AE, Beske SD, Christou DD, Donato AJ, Moreau KL, Eskurza I, Gates PE, Seals DR. Overweight and obese humans demonstrate increased vascular endothelial NAD(P)H oxidase-p47(phox) expression and evidence of endothelial oxidative stress. Circulation 115: 627-637, 2007.
38. Spier SA, Delp MD, Stallone JN, Dominguez JM, Muller-Delp JM. Exercise training enhances flow-induced vasodilation in skeletal muscle resistance arteries of aged rats: role of PGI(2) and nitric oxide. Am J Physiol Heart Circ Physiol 292: H3119-H3127, 2007.
39. Tarnopolsky MA, Pearce E, Smith K, Lach B. Suction-modified Bergstrom muscle biopsy technique: experience with 13, 500 procedures. Muscle Nerve 43: 717-725, 2011.
40. Tesch PA, Thorsson A, Colliander EB. Effects of eccentric and concentric resistance training on skeletal-muscle substrates, enzyme-activities and capillary supply. Acta Physiol Scand 140: 575-580, 1990.
41. Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S, Barrett EJ. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53: 1418-1423, 2004.
42. Wagenmakers AJM, van Riel NAW, Frenneaux MP, Stewart PM. Integration of the metabolic and cardiovascular effects of exercise. Essays Biochem 42: 193-210, 2006.
43. Wilkinson IB, MacCallum H, Flint L, Cockcroft JR, Newby DE, Webb DJ. The influence of heart rate on augmentation index and central arterial pressure in humans. J Physiol 525: 263-270, 2000.
44. Wilkinson IB, Prasad K, Hall IR, Thomas A, MacCallum H, Webb DJ, Frenneaux MP, Cockcroft JR. Increased central pulse pressure and augmentation index in subjects with hypercholesterolemia. J Am Coll Cardiol 39: 1005-1011, 2002.
45. Yaspelkis BB, Singh MK, Trevino B, Krisan AD, Collins DE. Resistance training increases glucose uptake and transport in rat skeletal muscle. Acta Physiol Scand 175: 315-323, 2002.