Endothelium-independent flow-induced dilation in the mouse carotid artery

Journal of Vascular Research

Volumn 43, Issue 4, 2006, Pages 383-391

  Quan, Adrian ^a,b,c   Ward, Michael E ^b,c,d   Kulandavelu, Shathiyah ^d,e   Adamson, S Lee ^c,d,e   Langille, B Lowell ^a,c,d  

^a TORONTO GENERAL HOSPITAL   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Blood flow autoregulation; eNOS knockout mice; Shear stress; Vascular remodeling; Vascular smooth muscle

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ADENYLATE CYCLASE INHIBITOR; GUANYLATE CYCLASE INHIBITOR; INDOMETACIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE INHIBITOR; PHENYLEPHRINE; PROSTAGLANDIN SYNTHASE INHIBITOR;

ANIMAL CELL; ARTERY ENDOTHELIUM; ARTICLE; BLOOD FLOW; BLOOD VESSEL TONE; BRONCHODILATATION; CAROTID ARTERY; CONTROLLED STUDY; HEART PERFUSION; HYPOXIA; LEISURE; MALE; MOUSE; MYOGRAPHY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; VASCULAR SMOOTH MUSCLE; VASODILATATION;

ACETYLCHOLINE; ANIMALS; BLOOD FLOW VELOCITY; CAROTID ARTERIES; CYCLOOXYGENASE INHIBITORS; ENDOTHELIUM, VASCULAR; GUANYLATE CYCLASE; INDOMETHACIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE II; OXADIAZOLES; QUINOXALINES; VASODILATION; VASODILATOR AGENTS;

EID: 33746731668     PISSN: 10181172     EISSN: None     Source Type: Journal    
DOI: 10.1159/000094414     Document Type: Article

References (62)

1. Bendeck MP, Keeley FW, Langille BL: Perinatal accumulation of arterial wall constituents: relation to hemodynamic changes at birth. Am J Physiol 1994;267:H2268-H2279.
2. Bendeck MP, Langille BL: Changes in blood flow distribution during the perinatal period in fetal sheep and lambs. Can J Physiol Pharmacol 1992;70:1576-1582.
3. Koller A, Sun D, Huang A, Kaley G: Corelease of nitric oxide and prostaglandins mediates flow-dependent dilation of rat gracilis muscle arterioles. Am J Physiol 1994;267:H326-H332.
4. Nadaud S, Philippe M, Arnal JF, Michel JB, Soubrier F: Sustained increase in aortic endothelial nitric oxide synthase expression in vivo in a model of chronic high blood flow. Circ Res 1996;79:857-863.
5. Huang A, Wu Y, Sun D, Koller A, Kaley G: Effect of estrogen on flow-induced dilation in NO deficiency: role of prostaglandins and EDHF. J Appl Physiol 2001;91:2561-2566.
6. Huang A, Sun D, Shesely EG, Levee EM, Koller A, Kaley G: Neuronal NOS-dependent dilation to flow in coronary arteries of male eNOS-KO mice. Am J Physiol 2002;282:H429-H436.
7. New DI, Chesser AM, Thuraisingham RC, Yaqoob MM: Cerebral artery responses to pressure and flow in uremic hypertensive and spontaneously hypertensive rats. Am J Physiol 2003;284:H1212-H1216.
8. Garcia-Roldan JL, Bevan JA: Augmentation of endothelium-independent flow constriction in pial arteries at high intravascular pressures. Hypertension 1991;17:870-874.
9. Gaw AJ, Bevan JA: Flow-induced relaxation of the rabbit middle cerebral artery is composed of both endothelium-dependent and -independent components. Stroke 1993;24:105-110.
10. Lamping KG, Faraci FM: Role of sex differences and effects of endothelial NO synthase deficiency in responses of carotid arteries to serotonin. Arterioscler Thromb Vasc Biol 2001;21:523-528.
11. Loufrani L, Matrougui K, Li Z, Levy BI, Lacolley P, Paulin D, Henrion D, Gorny D, Duriez M, Blanc I: Selective microvascular dysfunction in mice lacking the gene encoding for desmin. FASEB J 2002;16:117-119.
12. Quinlan TR, Li D, Laubach VE, Shesely EG, Zhou N, Johns RA: eNOS-deficient mice show reduced pulmonary vascular proliferation and remodeling to chronic hypoxia. Am J Physiol 2000;279:L641-L650.
13. Wadsworth RM: Vasoconstrictor and vasodilator effects of hypoxia. Trends Pharmacol Sci 1994;15:47-53.
14. Ward ME: Dilation of rat diaphragmatic arterioles by flow and hypoxia: roles of nitric oxide and prostaglandins. J Appl Physiol 1999;86:1644-1650.
15. Vedernikov YP, Graser T, Leisner H, Tierdt N: Effect of hypoxia on endothelium-dependent relaxation of porcine coronary arteries and veins. Biomed Biochim Acta 1991;50:257-263.
16. Kuo L, Davis MJ, Chilian WM: Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol 1990;259:H1063-H1070.
17. 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.
18. Denninger JW, Marietta MA: Guanylate cyclase and the NO/cGMP signaling pathway. Biochim Biophys Acta 1999;1411:334-350.
19. Botelho LH, Rothermel JD, Coombs RV, Jastorff B: cAMP analog antagonists of cAMP action. Methods Enzymol 1988;159:159-172.
20. Muller JM, Chilian WM, Davis MJ: Integrin signaling transduces shear stress-dependent vasodilation of coronary arterioles. Circ Res 1997;80:320-326.
21. Auer G, Ward ME: Impaired reactivity of rat aorta to phenylephrine and KCl after prolonged hypoxia: role of the endothelium. J Appl Physiol 1998;85:411-417.
22. Ryan MJ, Didion SP, Davis DR, Faraci FM, Sigmund CD: Endothelial dysfunction and blood pressure variability in selected inbred mouse strains. Arterioscler Thromb Vasc Biol 2002;22:42-48.
23. Wong AY, Kulandavelu S, Whiteley KJ, Qu D, Langille BL, Adamson SL: Maternal cardiovascular changes during pregnancy and postpartum in mice. Am J Physiol 2002;282:H918-H925.
24. Moncada S, Vane JR: Pharmacology and endogenous roles of prostaglandin endoperoxides, thromboxane A2, and prostacyclin. Pharmacol Rev 1978;30:293-331.
25. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B: Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 1995;48:184-188.
26. Teoh H, Man RY: Enhanced relaxation of porcine coronary arteries after acute exposure to a physiological level of 17beta-estradiol involves non-genomic mechanisms and the cyclic AMP cascade. Br J Pharmacol 2000;129:1739-1747.
27. 2+]i induced by RGD-containing peptide. Am J Physiol 1997;272:H2065-H2070.
28. Eitzman DT, Bodary PF, Shen Y, Khairallah CG, Wild SR, Abe A, Shaffer-Hartman J, Shayman JA: Fabry disease in mice is associated with age-dependent susceptibility to vascular thrombosis. J Am Soc Nephrol 2003;14:298-302.
29. Korshunov VA, Berk BC: Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler Thromb Vasc Biol 2003;23:2185-2191.
30. Hajra L, Evans AI, Chen M, Hyduk SJ, Collins T, Cybulsky MI: The NF-kappa B signal transduction pathway in aortic endothelial cells is primed for activation in regions predisposed to atherosclerotic lesion formation. Proc Natl Acad Sci USA 2000;97:9052-9057.
31. Ward ME, Yan L, Kelly S, Angle MR: Flow modulation of pressure-sensitive tone in rat pial arterioles: role of the endothelium. Anesthesiology 2000;93:1456-1464.
32. Ziegler T, Silacci P, Harrison VJ, Hayoz D: Nitric oxide synthase expression in endothelial cells exposed to mechanical forces. Hypertension 1998;32:351-355.
33. Papadaki M, Tilton RG, Eskin SG, Mclntire LV: Nitric oxide production by cultured human aortic smooth muscle cells: stimulation by fluid flow. Am J Physiol 1998;274:H616-H626.
34. Alshihabi SN, Chang YS, Frangos JA, Tarbell JM: Shear stress-induced release of PGE2 and PGI2 by vascular smooth muscle cells. Biochem Biophys Res Commun 1996;224:808-814.
35. Xie H, Bevan JA: Barium and 4-aminopyridine inhibit flow-initiated endothelium-independent relaxation. J Vase Res 1998;35:428-436.
36. Bergaya S, Meneton P, Bloch-Faure M, Mathieu E, Alhenc-Gelas F, Levy BI, Boulanger CM: Decreased flow-dependent dilation in carotid arteries of tissue kallikrein-knockout mice. Circ Res 2001;88:593-599.
37. Loufrani L, Matrougui K, Gorny D, Duriez M, Blanc I, Levy BI, Henrion D: Flow (shear stress)-induced endothelium-dependent dilation is altered in mice lacking the gene encoding for dystrophin. Circulation 2001;103:864-870.
38. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA: A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005;437:426-431.
39. Jalali S, del Pozo MA, Chen K, Miao H, Li Y, Schwartz MA, Shyy JY, Chien S: Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc Natl Acad Sci USA 2001;98:1042-1046.
40. Urbich C, Walter DH, Zeiher AM, Dimmeler S: Laminar shear stress upregulates integrin expression: role in endothelial cell adhesion and apoptosis. Circ Res 2000;87:683-689.
41. Liu SQ, Goldman J: Role of blood shear stress in the regulation of vascular smooth muscle cell migration. IEEE Trans Biomed Eng 2001;48:474-483.
42. Rhoads DN, Eskin SG, McIntire LV: Fluid flow releases fibroblast growth factor-2 from human aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 2000;20:416-421.
43. Wang S, Tarbell JM: Effect of fluid flow on smooth muscle cells in a 3-dimensional collagen gel model. Arterioscler Thromb Vasc Biol 2000;20:2220-2225.
44. Tada S, Tarbell JM: Flow through internal elastic lamina affects shear stress on smooth muscle cells (3D simulations). Am J Physiol 2002;282:H576-H584.
45. Bevan JA, Joyce EH: Flow-induced resistance artery tone: balance between constrictor and dilator mechanisms. Am J Physiol 1990;258:H663-H668.
46. Wang DM, Tarbell JM: Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J Biomech Eng 1995;117:358-363.
47. + current in vascular endothelial cells. Nature 1988;331:168-170.
48. Schwarz G, Callewaert G, Droogmans G, Nilius B: Shear stress-induced calcium transients in endothelial cells from human umbilical cord veins. J Physiol 1992;458:527-538.
49. Gudi SR, Clark CB, Frangos JA: Fluid flow rapidly activates G proteins in human endothelial cells. Involvement of G proteins in mechanochemical signal transduction. Circ Res 1996;79:834-839.
50. Berthiaume F, Frangos JA: Flow-induced prostacyclin production is mediated by a pertussis toxin-sensitive G protein. FEBS Lett 1992;308:277-279.
51. Maniotis AJ, Chen CS, Ingber DE: Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 1997;94:849-854.
52. Langille BL, O'Donnell F: Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 1986;231:405-407.
53. Spagnoli LG, Villaschi S, Neri L, Palmieri G: Gap junctions in myo-endothelial bridges of rabbit carotid arteries. Experientia 1982;38:124-125.
54. Shay-Salit A, Shushy M, Wolfovitz E, Yahav H, Breviario F, Dejana E, Resnick N: VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc Natl Acad Sci USA 2002;99:9462-9467.
55. Ko KS, Arora PD, McCulloch CA: Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium-permeable channels. J Biol Chem 2001;276:35967-35977.
56. Messina EJ, Sun D, Koller A, Wolin MS, Kaley G: Role of endothelium-derived prostaglandins in hypoxia-elicited arteriolar dilation in rat skeletal muscle. Circ Res 1992;71:790-796.
57. Price RJ, Skalak TC: Arteriolar remodeling in skeletal muscle of rats exposed to chronic hypoxia. J Vasc Res 1998;35:238-244.
58. Toporsian M, Govindaraju K, Nagi M, Eidelman D, Thibault G, Ward ME: Downregulation of endothelial nitric oxide synthase in rat aorta after prolonged hypoxia in vivo. Circ Res 2000;86:671-675.
59. Langille BL: Blood flow-induced remodeling of the artery wall; in Bevan JA, Kaley G, Rubanyi GM (eds): Flow-Dependent Regulation of Vascular Function. Oxford University Press, New York, 1995.
60. Bendeck MP, Langille BL: Rapid accumulation of elastin and collagen in the aortas of sheep in the immediate perinatal period. Circ Res 1991;69:1165-1169.
61. Huang PL: Neuronal and endothelial nitric oxide synthase gene knockout mice. Braz J Med Biol Res 1999;32:1353-1359.
62. Thorin-Trescases N, Bevan JA: High levels of myogenic tone antagonize the dilator response to flow of small rabbit cerebral arteries. Stroke 1998;29:1194-1201.