Arteriolar endothelial dysfunction is restored in ischaemic muscles by chronic electrical stimulation

Journal of Vascular Research

Volumn 41, Issue 3, 2004, Pages 241-251

  Kelsall, C J ^a   Brown, M D ^a   Kent, J ^a   Kloehn, M ^a   Hudlicka, O ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Arterial ligation; Arterioles; Capillaries; Nitric oxide synthase inhibition; Skeletal muscle

Indexed keywords

ACETYLCHOLINE; ALPHA ACTIN; BRADYKININ; N(G) NITROARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLAR ENDOTHELIAL DYSFUNCTION; ARTERY DISEASE; ARTERY LIGATION; ARTICLE; CAPILLARY; CONTROLLED STUDY; ELECTROSTIMULATION; EXERCISE; IMMUNOHISTOCHEMISTRY; MALE; MICROVASCULATURE; MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; RAT; VASOCONSTRICTION; VASODILATATION;

ACTINS; ANIMALS; ARTERIOLES; BLOOD PRESSURE; BLOOD VESSELS; ELECTRIC STIMULATION THERAPY; ENDOTHELIUM, VASCULAR; HINDLIMB; ISCHEMIA; MALE; MICROCIRCULATION; MUSCLE, SKELETAL; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY;

EID: 2942716834     PISSN: 10181172     EISSN: None     Source Type: Journal    
DOI: 10.1159/000078301     Document Type: Article

References (69)

1. Tan KH, DeCossart L, Edwards PR: Exercise training and peripheral vascular disease. Br J Surg 2000;87:553-562.
2. Delp MD, Laughlin MH: Time course of enhanced endothelium-mediated dilation in aorta or trained rats. Med Sci Sports Exerc 1997;29:1454-1461.
3. Sun D, Huang A, Koller A, Kaley G: Enhanced NO-mediated dilation in skeletal muscle arterioles of chronically exercised rats. Microvasc Res 2002;64:491-496.
4. Koller A, Huang A, Sun D, Kaley G: Exercise training augments flow-dependent dilatation in rat skeletal muscle arterioles. Role of endothelial nitric oxide and prostaglandins. Circ Res 1995;76:544-550.
5. Laughlin MH, Pollock JS, Amann JF, Hollis ML, Woodman CR, Price EM: Training induces nonuniform increases in eNOS content along the coronary arterial tree. J Appl Physiol 2001;90:501-510.
6. Brendle DC, Joseph LJ, Corretti MC, Gardner AW, Katzel LI: Effects of exercise rehabilitation on endothelial reactivity in older patients with peripheral arterial disease. Am J Cardiol 2001;87:324-329.
7. Hambrecht R, Fiehn E, Weigl C, Gielen S, Hamann C, Kaiser R, Yu J, Adams V, Niebauer J, Schuler G: Regular physical exercise corrects endothelial dysfunction and improves exercise capacity in patients with chronic heart failure. Circulation 1998;98:2709-2715.
8. Green DJ, Walsh JH, Maiorana A, Best MJ, Taylor RR, O'Driscoll JG: Exercise-induced improvement in endothelial dysfunction is not mediated by changes in CV risk factors: Pooled analysis of diverse patient populations. Am J Physiol 2003;285:H2679-H2687.
9. Lloyd PG, Yang HT, Terjung RL: Arteriogenesis and angiogenesis in ischemic hind-limb: Role of nitric oxide. Am J Physiol 2001;281:H2528-2538.
10. Kelsall CJ, Brown MD, Hudlicka O: Alterations of small arterioles in rat skeletal muscles as a result of chronic ischaemia. J Vasc Res 2001;38:212-218.
11. Brown MD, Kent J, Kelsall CJ, Milkiewicz M, Hudlicka O: Remodeling in the microcirculation of rat skeletal muscle during chronic ischemia. Microcirculation 2003;10:179-191.
12. Anderson SI, Whatling P, Hudlicka O, Gosling P, Simms M, Brown MD: Chronic transcutaneous electrical stimulation of calf muscles improves functional capacity without inducing systemic inflammation in claudicants. Eur J Vasc Endovasc Surg 2004;27:201-209.
13. Hudlicka O, Brown MD, Egginton S, Dawson JM: Effect of long-term electrical stimulation on vascular supply and fatigue in chronically ischemic muscles. J Appl Physiol 1994;77:1317-1324.
14. Balon TW, Nadler JL: Nitric oxide release is present from incubated skeletal muscle preparations. J Appl Physiol 1994;77:2519-2521.
15. Reiser PJ, Kline WO, Vaghy PL: Induction of neuronal type nitric oxide synthase in skeletal muscle by chronic electrical stimulation in vivo. J Appl Physiol 1997;82:1250-1255.
16. Linderman JR, Kloehn MR, Greene AS: Development of an implantable muscle stimulator: Measurement of stimulated angiogenesis and poststimulus vessel regression. Microcirculation 2000;7:119-128.
17. Anderson SI, Hudlicka O, Brown MD: Capillary red blood cell flow and activation of white blood cells in chronic muscle ischaemia in the rat. Am J Physiol 1997;272:H2757-H2764.
18. ATP channels and nitric oxide. J Physiol 2002;539:547-555.
19. Borsch DM, Cilento EV, Reilly FD: Role for nitric oxide but not prostaglandins in acetylcholine induced relaxation of rat cremaster third-order arterioles in 5-hour ischemia-reperfusion control rats. Chin J Physiol 1999;41:9-16.
20. Koller A, Messina EJ, Wolin MS, Kaley G: Effects of endothelial impairment on arteriolar dilator responses in vivo. Am J Physiol 1989; 257:H1485-H1489.
21. Carter RW, Begaye M, Kanagy NL: Acute and chronic NOS inhibition enhances alpha2-adrenoceptor-stimulated RhoA and Rho kinase in rat aorta. Am J Physiol 2002;283:H1361-H1369.
22. Librizzi L, Folco G, de Curtis M: Nitric oxide synthase inhibitors unmask acetylcholine-mediated constriction of cerebral vessels in the in vitro isolated guinea-pig brain. Neuroscience 2000;101:283-287.
23. Miller FJ Jr, Dellsperger KC, Gutterman DD: Pharmacologic activation of the human coronary microcirculation in vitro: Endotheliumdependent dilation and differential responses to acetylcholine. Cardiovasc Res 2998:38:744-750.
24. Lau KS, Grange RW, Chang W-J, Kamm KE, Sarelius I, Stull JT: Skeletal muscle contractions stimulate cGMP formation and attenuate vascular smooth muscle myosin phosphorylation via nitric oxide. FEBS Lett 1998;431:71-74.
25. Lau KS, Grange RW, Isotani E, Sarelius IH, Kamm KE, Huang PL, Stull JT: nNOS and eNOS modulate cGMP formation and vascular response in contracting fast-twitch skeletal muscle. Physiol Genomics 2000;2:21-27.
26. Roberts CK, Barnard RJ, Jasman A, Balon TW: Acute exercise increases nitric oxide synthase activity in skeletal muscle. Am J Physiol 1999;277:E390-E394.
27. Laughlin MH: Endothelium-mediated control of coronary vascular tone after chronic exercise training. Med Sci Sports Exerc 1995;27:1135-1144.
28. Pearce SC, Hudlicka O, Brown MD: Effect of indomethacin on capillary growth and microvasculature in chronically stimulated rat skeletal muscle. J Physiol 2000;526.2:435-443.
29. Hansen-Smith FM, Egginton S, Hudlicka O: Growth of arterioles in chronically stimulated adult skeletal muscle. Microcirculation 1998;5:49-59.
30. Dananberg J, Sideer RS, Grekin RJ: Sustained hypertension induced by orally administrated nitro-L-arginine. Hypertension 1993;21:359-363.
31. Yang AL, Tsai SJ, Jiang MJ, Jen CJ, Chen HI: Chronic exercise increases both inducible and endothelial nitric oxide synthase gene expression in endothelial cells of rat aorta. J Biomed Sci 2002;9:149-155.
32. Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, et al: Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 2003;107:3152-3158.
33. Angus JA, Lew MJ: Interpretation of the acetylcholine test of endothelial cell dysfunction in hypertension. J Hypertens 1992;10(suppl 7):S179-S186.
34. Huk I, Nanobashvili J, Neumayer C, Puntz A, Meuller M, Afkthampour K, Mittlboeck M, Losert U, Polterauer P, Roth E, Patton S, Malinksi T: L-Arginine treatment alters the kinetics of nitric oxide and superoxide release and reduces ischemia/reperfusion injury in skeletal muscle. Circ Res 2001;96:667-675.
35. Bouloumie A, Bauersachs J, Linz W, Scholkens BA, Wiemer G, Fleming I, Busse R: Endothelial dysfunction coincides with an enhanced nitric oxide expression and superoxide anion production. Hypertension 1997;30:934-941.
36. Matoba T, Shimokawa H, Nakashima M, Hirakawa Y, Mukai Y, Hirano K, et al: Hydrogen peroxide in an endothelium-dependent hyperpolarizing factor in mice. J Clin Invest 2000;106:1521-1530.
37. Garnham A, Hudlicka O: Effect of allopurinol and vitamin E on leukocyte rolling and adhesion in venules in chronically ischaemic muscles (abstract). Int J Microcirc 1995;15:202-203.
38. McArdle A, Pattwell D, Vasilaki A, Griffiths RD, Jackson MJ: Contractile activity-induced oxidative stress: Cellular origin and adaptive responses. Am J Physiol 2001;280:C621-C627.
39. Hollander J, Fiebig R, Gore M, Ookawara T, Ohno H, Ji LL: Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflügers Arch 2001;442:426-434.
40. Rush JWE, Laughlin MH, Woodman CR, Price EM: SOD-1 expression in pig coronary arterioles is increased by exercise training. Am J Physiol 2000;279:2068-2076.
41. Husain K: Exercise conditioning attenuates the hypertensive effects of nitric oxide synthase inhibitor in rat. Mol Cell Biochem 2002;231:129-137.
42. Chang HY, Chen CW, Hsiue TR: Comparative effects of L-NOARG and L-NAME on basal flow and Ach-induced vasodilatation in diaphragmatic microcirculation. Br J Pharmacol 1997;129:326-332.
43. Lamping KG, Nuno DW, Shesely EG, Maeda N, Faraci FM: Vasodilator mechanisms in the coronary circulation of endothelial nitric oxide synthase-deficient mice. Am J Physiol 2000;279:H1906-H1912.
44. Milkiewicz M, Brown MD, Egginton S, Hudlicka O: Shear modulation of angiogenesis and VEGF in skeletal muscles in vivo. Microcirculation 2000;8:229-241.
45. Myrhage R, Hudlicka O: Capillary growth in chronically stimulated adult skeletal muscle as studied by intravital microscopy and histological methods in rabbits and rats. Microvasc Res 1978;16:73-90.
46. Messina A, Knight KR, Dowsing BJ, Zhang B, Phan LH, Hurley JV, Morrison WA, Stewarts AG: Localization of inducible nitric oxide synthase to mast cells during ischemia/reperfusion injury of skeletal muscle. Lab Invest 2000;80:423-431.
47. Kaley G, Koller A, Rodenburg JM, Messina EJ, Wolin MS: Regulation of arteriolar tone and responses via L-arginine pathway in skeletal muscle. Am J Physiol 1992;262:H987-H992.
48. Osanai T, Fujita N, Fujiwara N, Nakano T, Takahashi K, Guan W, Okumura K: Cross talk of shear-induced production of prostacyclin and nitric oxide in endothelial cells. Am J Physiol 2000;278:H233-H238.
49. Sun D, Huang A, Smith CJ, Stackpole CJ, Connetta JA, Shesely EG, Koller A, Kaley G: Enhanced release of prostaglandins contributes to flow-induced arteriolar dilation in eNOS knockout mice. Circ Res 1999;85:288-293.
50. Honing MLH, Smits P, Morrison PJ, Rabelink TJ: Bradykinin-induced vasodilation of human forearm resistance vessels is primarily mediated by endothelial-dependent hyperpolarization. Hypertension 2000;35:1314-1318.
51. De Wit C, Esser N, Lehr HA, Bolz SS, Pohl U: Pentobarbital-sensitive EDHF comediates ACh-induced arteriolar dilation in the hamster microcirculation. Am J Physiol 1999;276:H1527-H1534.
52. Hudlicka O, Brown M, Cotter M, Smith M, Vrbova G: The effect of long-term stimulation of fast muscles on their blood flow, metabolism and ability to withstand fatigue. Pflügers Arch 1977;369:141-149.
53. Egginton S, Hudlicka O: Early changes in performance, blood flow and capillary fine structure in rat fast muscles induced by indirect electrical stimulation. J Physiol 1999;515:265-275.
54. Brown MD, Cotter M, Hudlicka O, Vrbova G: The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflügers Arch 1976;361:241-250.
55. Brown MD, Walter H, Hansen-Smith FM, Hudlicka O, Egginton S: Lack of involvement of basic fibroblast growth factor (FGF-2) in capillary growth in skeletal muscles exposed to long-term contractile activity. Angiogenesis 1998;2:81-91.
56. Gute D, Fraga C, Laughlin MH, Amann JF: Regional changes in capillary supply in skeletal muscle of high-intensity endurance-trained rats. J Appl Physiol 1996;81:619-626.
57. Laughlin MH, Korthuis RJ, Sexton WL, Armstrong RB: Regional muscle blood flow capacity and exercise hyperemia in high-intensity trained rats. J Appl Physiol 1988;64:2420-2427.
58. Ziche M, Morbidelli L, Choudhuri R, Zhang H-T, Donnini S, Granger HJ, Bicknell R: Nitric oxide synthase lies downstream from vascular endothelium growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 1997;99:2625-2634.
59. Milkiewicz M, Hudlicka O, Verhaeg J, Egginton S, Brown MD: Differential expression of Flk-1 and Flt-1 in rat skeletal muscle in response to chronic ischaemia: Favourable effect of muscle activity. Clin Sci 2003;105:1-10.
60. Murrant CL, Sarelius IH: Coupling of muscle metabolism and muscle blood flow in capillary units during contraction. Acta Physiol Scand 2000;168:531-541.
61. Skalak TC, Price RJ, Zeller PJ: Where do new arterioles come from? Mechanical forces and microvessel adaptation. Microcirculation 1998;5:91-100.
62. Segal SS, Brett SE, Sessa WC: Codistribution of NOS and caveolin throughout peripheral vasculature and skeletal muscle in hamsters. Am J Physiol 1999;277:H1167-H1177.
63. Price RJ, Skalak TC: Arterial remodelling in skeletal muscle of rats exposed to chronic hypoxia. J Vasc Res 1998;35:238-244.
64. Hudlicka O: What makes blood vessels grow? J Physiol 1991;444:1-24.
65. Hester RL, Eraslan A, Saito Y: Differences in EDNO contribution to arteriolar diameters at rest and during functional dilation in striated muscle. Am J Physiol 1993;265:H146-H151.
66. Kubis N, Besnard S, Silvestre JS, Feletou M, Huang PL, Levy BI, Tedgui A: Decreased arteriolar density in endothelial nitric oxide synthase knockout mice is due to hypertension, not to the constitutive defect in endothelial nitric oxide synthase enzyme. J Hypertens 2002;20:273-280.
67. Kiefer FN, Misteli H, Kalak N, Tschudin K, Fingerle J, Van der Kooij M, Stumm M, Sumanovski LT, Sieber CC, Battegay EJ: Inhibition of NO biosynthesis, but not elevated pressure, reduces angiogenesis in rat models of secondary hypertension. Blood Press 2002;11:116-124.
68. Amaral SL, Zorn TM, Michelini LC: Exercise training normalizes wall-to-lumen ratio of the gracilis muscle arterioles and reduces pressure in spontaneously hypertensive rats. J Hypertens 2000;18:1563-1572.
69. Goto D, Fujii S, Zaman AKMT, Sakuma I, Gao M, Koyama T, Mitchell J, Woodcock-Mitchell J, Sobel BE, Kitabatake A: Long-term blockade of nitric oxide synthase in rats modulates coronary capillary network remodeling. Angiogenesis 1999;3:137-146.