The hyperaemic response to passive leg movement is dependent on nitric oxide: A new tool to evaluate endothelial nitric oxide function

Journal of Physiology

Volumn 590, Issue 17, 2012, Pages 4391-4400

  Mortensen, Stefan P ^a   Askew, Christopher D ^b,c   Walker, Meegan ^c   Nyberg, Michael ^d   Hellsten, Ylva ^d  

^a International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c UNIVERSITY OF THE SUNSHINE COAST   (Australia)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE; NITRIC OXIDE; NITRITE;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FEMORAL ARTERY FLOW; HUMAN; HYPEREMIA; LEG BLOOD FLOW; LEG MOVEMENT; MALE; MEAN ARTERIAL PRESSURE; MUSCLE LEVEL; PASSIVE MOVEMENT; PRIORITY JOURNAL; VASODILATATION;

ACETYLCHOLINE; ADULT; AGED; BLOOD FLOW VELOCITY; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; HYPEREMIA; LEG; MALE; MIDDLE AGED; MOVEMENT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OMEGA-N-METHYLARGININE; PERIPHERAL ARTERIAL DISEASE; VASODILATION; YOUNG ADULT;

EID: 84865593362     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.235952     Document Type: Article

References (41)

1. Böger RH, Bode-Böger SM, Thiele W, Junker W, Alexander K & Frölich JC (1997). Biochemical evidence for impaired nitric oxide synthesis in patients with peripheral arterial occlusive disease. Circulation 95, 2068-2074.
2. Boushel R, Langberg H, Gemmer C, Olesen J, Crameri R, Scheede C, Sander M & Kjaer M (2002). Combined inhibition of nitric oxide and prostaglandins reduces human skeletal muscle blood flow during exercise. J Physiol 543, 691-698.
3. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK & Deanfield JE (1992). Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340, 1111-1115.
4. Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J & Deanfield JE (1994). Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24, 471-476.
5. Cheng TH, Chen JJW, Shih NL, Lin JW, Liu JC, Chen YL, Chen CH & Chen JJ (2009). Mechanical stretch induces endothelial nitric oxide synthase gene expression in neonatal rat cardiomyocytes. Clin Exp Pharmacol Physiology 36, 559-566.
6. Dai G, Tsukurov O, Chen M, Gertler JP & Kamm RD (2002). Endothelial nitric oxide production during in vitro simulation of external limb compression. Am J Physiol Heart Circ Physiol 282, H2066-H2075.
7. G-nitro-l-arginine methyl ester in humans. J Physiol 531, 257-264.
8. Fukudome Y, Fujii K, Abe I, Ohya Y, Fukuhara M, Kaseda S, Onaka U, Tsuchihashi T & Fujishima M (1997). Ultrasonographic assessment of regional differences in atherosclerotic lesions in patients with hypertension, diabetes mellitus, or both. Hypertens Res 20, 175-181.
9. Furchgott RF & Zawadzki JV (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373-376.
10. González-Alonso J, Mortensen SP, Jeppesen TD, Ali L, Barker H, Damsgaard R, Secher NH, Dawson EA & Dufour SP (2008). Haemodynamic responses to exercise, ATP infusion and thigh compression in humans: insight into the role of muscle mechanisms on cardiovascular function. J Physiol 586, 2405-2417.
11. Hellsten Y, Rufener N, Nielsen JJ, Hoier B, Krustrup P & Bangsbo J (2008). Passive leg movement enhances interstitial VEGF protein, endothelial cell proliferation, and eNOS mRNA content in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 294, R975-R982.
12. Høier B, Rufener N, Bojsen-Møller J, Bangsbo J & Hellsten Y (2010). The effect of passive movement training on angiogenic factors and capillary growth in human skeletal muscle. J Physiol 588, 3833-3845.
13. Jansson PA, Veneman T, Nurjhan N & Gerich J (1994). An improved method to calculate adipose tissue interstitial substrate recovery for microdialysis studies. Life Sci 54, 1621-1624.
14. Joannides R, Haefeli WE, Linder L, Richard V, Bakkali EH, Thuillez C & Lüscher TF (1995). Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 91, 1314-1319.
15. Kirby BS, Crecelius AR, Voyles WF & Dinenno FA (2010). Vasodilatory responsiveness to adenosine triphosphate in ageing humans. J Physiol 588, 4017-4027.
16. Kooijman M, Thijssen DHJ, de Groot PCE, Bleeker MWP, van Kuppevelt HJM, Green DJ, Rongen GA, Smits P & Hopman MTE (2008). Flow-mediated dilatation in the superficial femoral artery is nitric oxide mediated in humans. J Physiol 586, 1137-1145.
17. Krustrup P, Hellsten Y & Bangsbo J (2004). Intense interval training enhances human skeletal muscle oxygen uptake in the initial phase of dynamic exercise at high but not at low intensities. J Physiol 559, 335-345.
18. McDaniel J, Hayman MA, Ives S, Fjeldstad AS, Trinity JD, Wray DW & Richardson RS (2010). Attenuated exercise induced hyperaemia with age: mechanistic insight from passive limb movement. J Physiol 588, 4507-4517.
19. Mortensen SP, González-Alonso J, Damsgaard R, Saltin B & Hellsten Y (2007). Inhibition of nitric oxide and prostaglandins, but not endothelial-derived hyperpolarizing factors, reduces blood flow and aerobic energy turnover in the exercising human leg. J Physiol 581, 853-861.
20. Mortensen SP, Gonzalez-Alonso J, Bune LT, Saltin B, Pilegaard H & Hellsten Y (2009a). ATP-induced vasodilation and purinergic receptors in the human leg: roles of nitric oxide, prostaglandins, and adenosine. Am J Physiol Regul Integr Comp Physiol 296, R1140-R1148.
21. Mortensen SP, Nyberg M, Thaning P, Saltin B & Hellsten Y (2009b). Adenosine contributes to blood flow regulation in the exercising human leg by increasing prostaglandin and nitric oxide formation. Hypertension 53, 993-999.
22. Newcomer SC, Leuenberger UA, Hogeman CS, Handly BD & Proctor DN (2004). Different vasodilator responses of human arms and legs. J Physiol 556, 1001-1011.
23. Pohl U, Holtz J, Busse R & Bassenge E (1986). Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension 8, 37-44.
24. Pyke KE, Dwyer EM & Tschakovsky ME (2004). Impact of controlling shear rate on flow-mediated dilation responses in the brachial artery of humans. J Appl Physiol 97, 499-508.
25. Rådegran G & Saltin B (1998). Muscle blood flow at onset of dynamic exercise in humans. Am J Physiol Heart Circ Physiol 274, H314-H322.
26. Rådegran G & Saltin B (1999). Nitric oxide in the regulation of vasomotor tone in human skeletal muscle. Am J Physiol Heart Circ Physiol 276, H1951-H1960.
27. Ross R (1999). Atherosclerosis - an inflammatory disease. N Engl J Med 340, 115-126.
28. Rowell LB (1993). Human Cardiovascular Control. Ann Intern Med 119, 1234-123b.
29. Scheller D & Kolb J (1991). The internal reference technique in microdialysis: a practical approach to monitoring dialysis efficiency and to calculating tissue concentration from dialysate samples. J Neurosci Methods 40, 31-38.
30. Shipley RD, Kim SJ & Muller-Delp JM (2005). Time course of flow-induced vasodilation in skeletal muscle: contributions of dilator and constrictor mechanisms. Am J Physiol Heart Circ Physiol 288, H1499-H1507.
31. Taddei S, Virdis A, Mattei P, Ghiadoni L, Fasolo CB, Sudano I & Salvetti A (1997). Hypertension causes premature aging of endothelial function in humans. Hypertension 29, 736-743.
32. Taddei S, Virdis A, Mattei P, Ghiadoni L, Gennari A, Fasolo CB, Sudano I & Salvetti A (1995). Aging and endothelial function in normotensive subjects and patients with essential hypertension. Circulation 91, 1981-1987.
33. Tendera M, Aboyans V, Bartelink ML, Baumgartner I, Clément D, Collet JP, Cremonesi A, De Carlo M, Erbel R, Fowkes FG, Heras M, Kownator S, Minar E, Ostergren J, Poldermans D, Riambau V, Roffi M, Röther J, Sievert H, van Sambeek M & Zeller T (2011). ESC Guidelines on the diagnosis and treatment of peripheral artery diseases. Eur Heart J 32, 2851-2906.
34. Thijssen DHJ, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, Parker B, Widlansky ME, Tschakovsky ME & Green DJ (2011a). Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 300, H2-H12.
35. Thijssen DHJ, Rowley N, Padilla J, Simmons GH, Laughlin MH, Whyte G, Cable NT & Green DJ (2011b). Relationship between upper and lower limb conduit artery vasodilator function in humans. J Appl Physiol 111, 244-250.
36. Tooke JE (1995). Microvascular function in human diabetes. A physiological perspective. Diabetes 44, 721-726.
37. Trinity JD, Amann M, McDaniel J, Fjeldstad AS, Barrett-O'Keefe Z, Runnels S, Morgan DE, Wray DW & Richardson RS (2010). Limb movement-induced hyperemia has a central hemodynamic component: evidence from a neural blockade study. Am J Physiol Heart Circ Physiol 299, H1693-H1700.
38. Tschakovsky ME & Pyke KE (2005). Counterpoint: Flow-mediated dilation does not reflect nitric oxide-mediated endothelial function. J Appl Physiol 99, 1235-1237.
39. Venturelli M, Amann MK, McDaniel J, Trinity JD, Fjeldstad AS & Richardson RS (2011). Central and peripheral hemodynamic responses to passive-limb movement: the role of arousal. Am J Physiol Heart Circ Physiol 302, H333-339.
40. Widlansky ME, Gokce N, Keaney JF Jr & Vita JA (2003). The clinical implications of endothelial dysfunction. J Am Coll Cardiol 42, 1149-1160.
41. Wray DW, Donato AJ, Uberoi A, Merlone JP & Richardson RS (2005). Onset exercise hyperaemia in humans: partitioning the contributors. J Physiol 565, 1053-1060.