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Blood pressure regulation VIII: resistance vessel tone and implications for a pro-atherogenic conduit artery endothelial cell phenotype

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Abstract

Dysfunction of the endothelium is proposed as the primary initiator of atherosclerotic peripheral artery disease, which occurs mainly in medium- to large-sized conduit arteries of the lower extremities (e.g., iliac, femoral, popliteal arteries). In this review article, we propose the novel concept that conduit artery endothelial cell phenotype is determined, in part, by microvascular tone in skeletal muscle resistance arteries through both changes in arterial blood pressure as well as upstream conduit artery shear stress patterns. First, we summarize the literature supporting the involvement of sympathetic nerve activity (SNA) and nitric oxide (NO) in the modulation of microvascular tone and arterial blood pressure. We then focus on the role of elevated blood pressure and shear stress profiles in modulating conduit artery endothelial cell phenotype. Last, we discuss findings from classic and emerging studies indicating that increased vascular resistance, as it occurs in the context of increased SNA and/or reduced NO bioavailability, is associated with greater oscillatory shear stress (e.g., increased retrograde shear) in upstream conduit arteries. The ideas put forth in this review set the stage for a new paradigm concerning the mechanistic link between increased microvascular tone and development of conduit artery endothelial dysfunction and thus increased risk for peripheral artery disease. Indeed, a vast amount of evidence supports the notion that excessive blood pressure and oscillatory shear stress are potent pro-atherogenic signals to the endothelium.

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References

  • Alberts-Grill N, Rezvan A, Son DJ, Qiu H, Kim CW, Kemp ML, Weyand CM, Jo H (2012) Dynamic immune cell accumulation during flow-induced atherogenesis in mouse carotid artery: an expanded flow cytometry method. Arterioscler Thromb Vasc Biol 32:623–632

    CAS  PubMed Central  PubMed  Google Scholar 

  • Andrews TC, Whitney EJ, Green G, Kalenian R, Personius BE (1997) Effect of gemfibrozil ± niacin ± cholestyramine on endothelial function in patients with serum low-density lipoprotein cholesterol levels <160 mg/dl and high-density lipoprotein cholesterol levels <40 mg/dl. Am J Cardiol 80:831–835

    CAS  PubMed  Google Scholar 

  • Augustyniak RA, Victor RG, Morgan DA, Zhang W (2006) l-NAME- and ADMA-induced sympathetic neural activation in conscious rats. Am J Physiol Regul Integr Comp Physiol 290:R726–R732

    CAS  PubMed  Google Scholar 

  • Baccelli G, Pignoli P, Corbellini E, Pizzolati PL, Bassini M, Longo T, Zanchetti A (1985) Hemodynamic factors changing blood flow velocity waveform and profile in normal human brachial artery. Angiol J Vasc Dis 36:1–8

    CAS  Google Scholar 

  • Barboriak JJ, Pintar K, Korns ME (1974) Atherosclerosis in aortocoronary vein grafts. Lancet 2:621–624

    CAS  PubMed  Google Scholar 

  • Becker GJ, McClenny TE, Kovacs ME, Raabe RD, Katzen BT (2002) The importance of increasing public and physician awareness of peripheral arterial disease. J Vasc Interv Radiol 13:7–11

    PubMed  Google Scholar 

  • Bedarida GV, Bushell E, Haefeli WE, Blaschke TF, Hoffman BB (1993) Responsiveness to bradykinin in veins of hypercholesterolemic humans. Circulation 88:2754–2761

    CAS  PubMed  Google Scholar 

  • Bell DR (1993) Vascular smooth muscle responses to endothelial autacoids in rats with chronic coarctation hypertension. J Hypertens 11:65–74

    CAS  PubMed  Google Scholar 

  • Bell DR, Bohr DF (1991) Endothelium in functional aortic changes of coarctation hypertension. Am J Physiol 260:H1187–H1193

    CAS  PubMed  Google Scholar 

  • Benjamin EJ, Larson MG, Keyes MJ, Mitchell GF, Vasan RS, Keaney JF Jr, Lehman BT, Fan S, Osypiuk E, Vita JA (2004) Clinical correlates and heritability of flow-mediated dilation in the community: the Framingham Heart Study. Circulation 109:613–619

    PubMed  Google Scholar 

  • Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA (1998) Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med 338:1650–1656

    CAS  PubMed  Google Scholar 

  • Blackshear WM, Phillips DJ, Strandness DE (1979) Pulsed Doppler assessment of normal human femoral artery velocity patterns. J Surg Res 27:73–83

    PubMed  Google Scholar 

  • Boura AL, Green AF (1959) The actions of bretylium: adrenergic neurone blocking and other effects. Br J Pharmacol Chemother 14:536–548

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brooks AR, Lelkes PI, Rubanyi GM (2002) Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol Genomics 9:27–41

    CAS  PubMed  Google Scholar 

  • Burnstock G (1986) The changing face of autonomic neurotransmission. Acta Physiol Scand 126:67–91

    CAS  PubMed  Google Scholar 

  • Caro CG (2009) Discovery of the role of wall shear in atherosclerosis. Atheroscler Thrombosis Vasc Biol 29:158–161

    CAS  Google Scholar 

  • Caro CG, Fitz-Gerald JM, Schroter RC (1969) Arterial wall shear and distribution of early atheroma in man. Nature 223:1159–1161

    CAS  PubMed  Google Scholar 

  • Casey DP, Padilla J, Joyner MJ (2012) Alpha-adrenergic vasoconstriction contributes to the age-related increase in conduit artery retrograde and oscillatory shear. Hypertension 60:1016–1022

    CAS  PubMed Central  PubMed  Google Scholar 

  • Celermajer DS, Sorensen KE, Bull C, Robinson J, Deanfield JE (1994) Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction. J Am Coll Cardiol 24:1468–1474

    CAS  PubMed  Google Scholar 

  • Chen Z, Tzima E (2009) PECAM-1 is necessary for flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol 29:1067–1073

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen W, Srinivasan SR, Li S, Boerwinkle E, Berenson GS (2004) Gender-specific influence of NO synthase gene on blood pressure since childhood: the Bogalusa Heart Study. Hypertension 44:668–673

    CAS  PubMed  Google Scholar 

  • Cheng JJ, Chao YJ, Wung BS, Wang DL (1996a) Cyclic strain-induced plasminogen activator inhibitor-1 (PAI-1) release from endothelial cells involves reactive oxygen species. Biochem Biophys Res Commun 225:100–105

    CAS  PubMed  Google Scholar 

  • Cheng JJ, Wung BS, Chao YJ, Wang DL (1996b) Cyclic strain enhances adhesion of monocytes to endothelial cells by increasing intercellular adhesion molecule-1 expression. Hypertension 28:386–391

    CAS  PubMed  Google Scholar 

  • Cheng JJ, Wung BS, Chao YJ, Wang DL (1998) Cyclic strain-induced reactive oxygen species involved in ICAM-1 gene induction in endothelial cells. Hypertension 31:125–130

    CAS  PubMed  Google Scholar 

  • Chiang HY, Korshunov VA, Serour A, Shi F, Sottile J (2009) Fibronectin is an important regulator of flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol 29:1074–1079

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chironi GN, Boulanger CM, Simon A, Dignat-George F, Freyssinet JM, Tedgui A (2009) Endothelial microparticles in diseases. Cell Tissue Res 335:143–151

    PubMed  Google Scholar 

  • Civelek M, Manduchi E, Riley RJ, Stoeckert CJ, Davies PF (2011) Coronary artery endothelial transcriptome in vivo/clinical perspective. Circ Cardiovasc Genet 4:243–252

    PubMed Central  PubMed  Google Scholar 

  • Conway DE, Williams MR, Eskin SG, McIntire LV (2010) Endothelial cell responses to atheroprone flow are driven by two separate flow components, low time-average shear stress and fluid flow reversal. Am J Physiol Cell Physiol 298:H367–H374

    CAS  Google Scholar 

  • Coote JH (2007) Landmarks in understanding the central nervous control of the cardiovascular system. Exp Physiol 92:3–18

    PubMed  Google Scholar 

  • Corrado E, Muratori I, Tantillo R, Contorno F, Coppola G, Strano A, Novo S (2005) Relationship between endothelial dysfunction, intima media thickness and cardiovascular risk factors in asymptomatic subjects. Int Angiol 24:52–58

    CAS  PubMed  Google Scholar 

  • Cowley AW Jr, Liard JF, Guyton AC (1973) Role of baroreceptor reflex in daily control of arterial blood pressure and other variables in dogs. Circ Res 32:564–576

    PubMed  Google Scholar 

  • Criqui MH, Langer RD, Fronek A, Feigelson HS, Klauber MR, McCann TJ, Browner D (1992) Mortality over a period of 10 years in patients with peripheral arterial disease. N Engl J Med 326:381–386

    CAS  PubMed  Google Scholar 

  • Critser JK, Laughlin MH, Prather RS, Riley LK (2009) Proceedings of the conference on swine in biomedical research. ILAR J 50:89–94

    CAS  PubMed  Google Scholar 

  • Dai G, Kaazempur-Mofrad MR, Natarajan S, Zhang Y, Vaughn S, Blackman BR, Kamm RD, Garcia-Cardena G, Gimbrone MA (2004) Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc Natl Acad Sci 101:14871–14876

    CAS  PubMed  Google Scholar 

  • Davies PF, Remuzzi A, Gordon EJ, Dewey CF Jr, Gimbrone MA Jr (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci USA 83:2114–2117

    CAS  PubMed  Google Scholar 

  • Davies PF, Civelek M, Fang Y, Guerraty MA, Passerini AG (2010) Endothelial heterogeneity associated with regional athero-susceptibility and adaptation to disturbed blood flow in vivo. Semin Thromb Hemost 36:265–275

    CAS  PubMed  Google Scholar 

  • Davy KP, Seals DR, Tanaka H (1998) Augmented cardiopulmonary and integrative sympathetic baroreflexes but attenuated peripheral vasoconstriction with age. Hypertension 32:298–304

    CAS  PubMed  Google Scholar 

  • Dignat-George F, Boulanger CM (2011) The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31:27–33

    CAS  PubMed  Google Scholar 

  • el Karib AO, Sheng J, Betz AL, Malvin RL (1993) The central effects of a nitric oxide synthase inhibitor (N omega-nitro-l-arginine) on blood pressure and plasma renin. Clin Exp Hypertens 15:819–832

    PubMed  Google Scholar 

  • Fairfax ST, Holwerda SW, Credeur DP, Zuidema MY, Medley JH, Dyke PC, Wray DW, Davis MJ, Fadel PJ (2013a) The role of α-adrenergic receptors in mediating beat-by-beat sympathetic vascular transduction in the forearm of resting man. J Physiol (in press)

  • Fairfax ST, Padilla J, Vianna LC, Davis MJ, Fadel PJ (2013b) Spontaneous bursts of muscle sympathetic nerve activity decrease leg vascular conductance in resting humans. Am J Physiol Heart Circ Physiol 304:H759–H766

    CAS  PubMed  Google Scholar 

  • Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–376

    CAS  PubMed  Google Scholar 

  • Gambillara V, Chambaz C, Montorzi G, Roy S, Stergiopulos N, Silacci P (2006) Plaque-prone hemodynamics impair endothelial function in pig carotid arteries. Am J Physiol Heart Circ Physiol 290:H2320–H2328

    CAS  PubMed  Google Scholar 

  • Godbole AS, Lu X, Guo X, Kassab GS (2009) NADPH oxidase has a directional response to shear stress. Am J Physiol Heart Circ Physiol 296:H152–H158

    CAS  PubMed  Google Scholar 

  • Gokce N, Holbrook M, Duffy SJ, Demissie S, Cupples LA, Biegelsen E, Keaney JF Jr, Loscalzo J, Vita JA (2001) Effects of race and hypertension on flow-mediated and nitroglycerin-mediated dilation of the brachial artery. Hypertension 38:1349–1354

    CAS  PubMed  Google Scholar 

  • Greer SA, Hays VW, Speer VC, McCall JT (1966) Effect of dietary fat, protein and cholesterol on atherosclerosis in swine. J Nutr 90:183–190

    CAS  PubMed  Google Scholar 

  • Hansen J, Jacobsen TN, Victor RG (1994) Is nitric oxide involved in the tonic inhibition of central sympathetic outflow in humans? Hypertension 24:439–444

    CAS  PubMed  Google Scholar 

  • Harada S, Tokunaga S, Momohara M, Masaki H, Tagawa T, Imaizumi T, Takeshita A (1993) Inhibition of nitric oxide formation in the nucleus tractus solitarius increases renal sympathetic nerve activity in rabbits. Circ Res 72:511–516

    CAS  PubMed  Google Scholar 

  • Hart EC, Wallin BG, Curry TB, Joyner MJ, Karlsson T, Charkoudian N (2011) Hysteresis in the sympathetic baroreflex: role of baseline nerve activity. J Physiol 589:3395–3404

    CAS  PubMed  Google Scholar 

  • Hastings NE, Simmers MB, McDonald OG, Wamhoff BR, Blackman BR (2007) Atherosclerosis-prone hemodynamics differentially regulates endothelial and smooth muscle cell phenotypes and promotes pro-inflammatory priming. Am J Physiol Cell Physiol 293:C1824–C1833

    CAS  PubMed  Google Scholar 

  • Hijmering ML, Stroes ES, Olijhoek J, Hutten BA, Blankestijn PJ, Rabelink TJ (2002) Sympathetic activation markedly reduces endothelium-dependent, flow-mediated vasodilation. J Am College Cardiol 39:683–688

    Google Scholar 

  • Hirsch AT, Criqui MH, Treat-Jacobson D, Regensteiner JG, Creager MA, Olin JW, Krook SH, Hunninghake DB, Comerota AJ, Walsh ME, McDermott MM, Hiatt WR (2001) Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA 19:1317–1324

    Google Scholar 

  • Hirst GD, Choate JK, Cousins HM, Edwards FR, Klemm MF (1996) Transmission by post-ganglionic axons of the autonomic nervous system: the importance of the specialized neuroeffector junction. Neuroscience 73:7–23

    CAS  PubMed  Google Scholar 

  • Hishikawa K, Nakaki T, Suzuki H, Saruta T, Kato R (1992) Transmural pressure inhibits nitric oxide release from human endothelial cells. Eur J Pharmacol 215:329–331

    CAS  PubMed  Google Scholar 

  • Hishikawa K, Nakaki T, Marumo T, Suzuki H, Kato R, Saruta T (1995) Pressure enhances endothelin-1 release from cultured human endothelial cells. Hypertension 25:449–452

    CAS  PubMed  Google Scholar 

  • Huo Y, Wischgoll T, Kassab GS (2007) Flow patterns in three-dimensional porcine epicardial coronary arterial tree. Am J Physiol Heart Circ Physiol 293:H2959–H2970

    CAS  PubMed  Google Scholar 

  • Hwang J, Ing MH, Salazar A, Lassegue B, Griendling K, Navab M, Sevanian A, Hsiai TK (2003a) Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation. Circ Res 93:1225–1232

    CAS  PubMed  Google Scholar 

  • Hwang J, Saha A, Boo YC, Sorescu GP, McNally JS, Holland SM, Dikalov S, Giddens DP, Griendling KK, Harrison DG, Jo H (2003b) Oscillatory shear stress stimulates endothelial production of O2- from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J Biol Chem 278:47291–47298

    CAS  PubMed  Google Scholar 

  • Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265–9269

    CAS  PubMed  Google Scholar 

  • Jenkins NT, Padilla J, Boyle LJ, Credeur DP, Laughlin MH, Fadel PJ (2013) Disturbed blood flow acutely induces activation and apoptosis of the human vascular endothelium. Hypertension 61:615–621

    CAS  PubMed  Google Scholar 

  • Jin SX, Shen LH, Nie P, Yuan W, Hu LH, Li DD, Chen XJ, Zhang XK, He B (2012) Endogenous renovascular hypertension combined with low shear stress induces plaque rupture in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 32:2372–2379

    CAS  PubMed  Google Scholar 

  • Johnson BD, Mather KJ, Wallace JP (2011) Mechanotransduction of shear in the endothelium: basic studies and clinical implications. Vasc Med 16:365–377

    PubMed  Google Scholar 

  • Johnson BD, Mather KJ, Newcomer SC, Mickleborough TD, Wallace JP (2013) Vitamin C prevents the acute decline of flow-mediated dilation after altered shear rate patterns. Appl Physiol Nutr Metab 38:268–274

    CAS  PubMed  Google Scholar 

  • Julius S, Jamerson K, Mejia A, Krause L, Schork N, Jones K (1990) The association of borderline hypertension with target organ changes and higher coronary risk. Tecumseh Blood Pressure study. JAMA 264:354–358

    CAS  PubMed  Google Scholar 

  • Juonala M, Jarvisalo MJ, Maki-Torkko N, Kahonen M, Viikari JS, Raitakari OT (2005) Risk factors identified in childhood and decreased carotid artery elasticity in adulthood: the Cardiovascular Risk in Young Finns Study. Circulation 112:1486–1493

    PubMed  Google Scholar 

  • Juonala M, Viikari JS, Ronnemaa T, Helenius H, Taittonen L, Raitakari OT (2006) Elevated blood pressure in adolescent boys predicts endothelial dysfunction: the cardiovascular risk in young Finns study. Hypertension 48:424–430

    CAS  PubMed  Google Scholar 

  • Jurva JW, Phillips SA, Syed AQ, Syed AY, Pitt S, Weaver A, Gutterman DD (2006) The effect of exertional hypertension evoked by weight lifting on vascular endothelial function. J Am College Cardiol 48:588–589

    Google Scholar 

  • Korshunov VA, Berk BC (2003) Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler Thromb Vasc Biol 23:2185–2191

    CAS  PubMed  Google Scholar 

  • Kroger K, Kucharczik A, Hirche H, Rudofsky G (1999) Atherosclerotic lesions are more frequent in femoral arteries than in carotid arteries independent of increasing number of risk factors. Angiology 50:649–654

    CAS  PubMed  Google Scholar 

  • Lai FM, Cobuzzi A, Shepherd C, Tanikella T, Hoffman A, Cervoni P (1989) Endothelium-dependent basilar and aortic vascular responses in normotensive and coarctation hypertensive rats. Life Sci 45:607–614

    CAS  PubMed  Google Scholar 

  • LaMack JA, Himburg HA, Friedman MH (2007) Distinct profiles of endothelial gene expression in hyperpermeable regions of the porcine aortic arch and thoracic aorta. Atherosclerosis 195:e35–e41

    CAS  PubMed Central  PubMed  Google Scholar 

  • LaMorte WW, Scott TE, Menzoian JO (1995) Racial differences in the incidence of femoral bypass and abdominal aortic aneurysmectomy in Massachusetts: relationship to cardiovascular risk factors. J Vasc Surg 21:422–431

    CAS  PubMed  Google Scholar 

  • Landmesser U, Drexler H (2007) Endothelial function and hypertension. Curr Opin Cardiol 22:316–320

    PubMed  Google Scholar 

  • Laughlin MH, Newcomer SC, Bender SB (2008) Importance of hemodynamic forces as signals for exercise-induced changes in endothelial cell phenotype. J Appl Physiol 104:588–600

    PubMed Central  PubMed  Google Scholar 

  • Laughlin MH, Bowles DK, Duncker DJ (2012) The coronary circulation in exercise training. Am J Physiol Heart Circ Physiol 302:H10–H23

    CAS  PubMed  Google Scholar 

  • Lawrence MB, McIntire LV, Eskin SG (1987) Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood 70:1284–1290

    CAS  PubMed  Google Scholar 

  • Lawrence AJ, Castillo-Melendez M, McLean KJ, Jarrott B (1998) The distribution of nitric oxide synthase-, adenosine deaminase- and neuropeptide Y-immunoreactivity through the entire rat nucleus tractus solitarius: effect of unilateral nodose ganglionectomy. J Chem Neuroanat 15:27–40

    CAS  PubMed  Google Scholar 

  • Lee HY, Youn SW, Oh BH, Kim HS (2012) Kruppel-like factor 2 suppression by high glucose as a possible mechanism of diabetic vasculopathy. Korean Circ J 42:239–245

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lepori M, Sartori C, Trueb L, Owlya R, Nicod P, Scherrer U (1998) Haemodynamic and sympathetic effects of inhibition of nitric oxide synthase by systemic infusion of N(G)-monomethyl-l-arginine into humans are dose dependent. J Hypertens 16:519–523

    CAS  PubMed  Google Scholar 

  • Lepori M, Sartori C, Duplain H, Nicod P, Scherrer U (2001) Interaction between cholinergic and nitrergic vasodilation: a novel mechanism of blood pressure control. Cardiovasc Res 51:767–772

    CAS  PubMed  Google Scholar 

  • Lewington S, Clarke R, Qizilbash N, Peto R, Collins R (2002) Age-specific relevance of usual blood pressure to vascular mortality: a meta-analysis of individual data for one million adults in 61 prospective studies. Lancet 360:1903–1913

    PubMed  Google Scholar 

  • Li S, Chen W, Srinivasan SR, Bond MG, Tang R, Urbina EM, Berenson GS (2003) Childhood cardiovascular risk factors and carotid vascular changes in adulthood: the Bogalusa Heart Study. JAMA 290:2271–2276

    CAS  PubMed  Google Scholar 

  • Li L, Chen W, Rezvan A, Jo H, Harrison DG (2011) Tetrahydrobiopterin deficiency and nitric oxide synthase uncoupling contribute to atherosclerosis induced by disturbed flow. Arterioscler Thromb Vasc Biol 31:1547–1554

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lockette W, Otsuka Y, Carretero O (1986) The loss of endothelium-dependent vascular relaxation in hypertension. Hypertension 8, II61-II66

  • Lu X, Kassab GS (2004) Nitric oxide is significantly reduced in ex vivo porcine arteries during reverse flow because of increased superoxide production. J Physiol 561:575–582

    CAS  PubMed  Google Scholar 

  • Lyon RT, Runyon-Hass A, Davis HR, Glagov S, Zarins CK (1987) Protection from atherosclerotic lesion formation by reduction of artery wall motion. J Vasc Surg 5:59–67

    CAS  PubMed  Google Scholar 

  • Madhur MS, Funt SA, Li L, Vinh A, Chen W, Lob HE, Iwakura Y, Blinder Y, Rahman A, Quyyumi AA, Harrison DG (2011) Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein e-deficient mice. Arterioscler Thromb Vasc Biol 31:1565–1572

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marshall RJ, Schirger A, Shepherd JT (1961) Blood pressure during supine exercise in idiopathic orthostatic hypotension. Circulation 24:76–81

    CAS  PubMed  Google Scholar 

  • McAllister RM, Newcomer SC, Laughlin MH (2008) Vascular nitric oxide: effects of exercise training in animals. Appl Physiol Nutr Metab 33:173–178

    CAS  PubMed Central  PubMed  Google Scholar 

  • McDermott MM, Guralnik JM, Ferrucci L, Tian L, Liu K, Liao Y, Green D, Sufit R, Hoff F, Nishida T, Sharma L, Pearce WH, Schneider JR, Criqui MH (2008) Asymptomatic peripheral arterial disease is associated with more adverse lower extremity characteristics than intermittent claudication. Circulation 117:2484–2491

    PubMed  Google Scholar 

  • McDonald DA (1955) The relation of pulsatile pressure to flow in arteries. J Physiol 127:533–552

    CAS  PubMed  Google Scholar 

  • McGill HC Jr, McMahan CA, Zieske AW, Sloop GD, Walcott JV, Troxclair DA, Malcom GT, Tracy RE, Oalmann MC, Strong JP (2000) Associations of coronary heart disease risk factors with the intermediate lesion of atherosclerosis in youth. The Pathobiological Determinants of Atherosclerosis in Youth (PDAY) Research Group. Arterioscler Thromb Vasc Biol 20:1998–2004

    PubMed  Google Scholar 

  • Millar PJ, Murai H, Floras JS (2011) Neurogenic retrograde arterial flow during obstructive sleep apnea: a novel mechanism for endothelial dysfunction? Hypertension 58:e17–e18

    CAS  PubMed  Google Scholar 

  • Miller MJ, Pinto A, Mullane KM (1987) Impaired endothelium-dependent relaxations in rabbits subjected to aortic coarctation hypertension. Hypertension 10:164–170

    CAS  PubMed  Google Scholar 

  • Minson CT, Halliwill JR, Young TM, Joyner MJ (2000) Influence of the menstrual cycle on sympathetic activity, baroreflex sensitivity, and vascular transduction in young women. Circulation 101:862–868

    CAS  PubMed  Google Scholar 

  • Montastruc JL, Rascol O, Senard JM (1996) The discovery of vasomotor nerves. Clin Auton Res 6:183–187

    CAS  PubMed  Google Scholar 

  • Moore WS (2002) Vascular surgery: a comprehensive review. W. B Saunders Company, Philadelphia

    Google Scholar 

  • Nam D, Ni C-W, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H (2009) Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 297:H1535–H1543

    CAS  PubMed  Google Scholar 

  • Ni C-W, Qiu H, Rezvan A, Kwon K, Nam D, Son DJ, Visvader JE, Jo H (2010) Discovery of novel mechanosensitive genes in vivo using mouse carotid artery endothelium exposed to disturbed flow. Blood 116:e66–e73

    CAS  PubMed  Google Scholar 

  • O’Keeffe LM, Muir G, Piterina AV, McGloughlin T (2009) Vascular cell adhesion molecule-1 expression in endothelial cells exposed to physiological coronary wall shear stresses. J Biomech Eng 131:081003

    PubMed  Google Scholar 

  • Owlya R, Vollenweider L, Trueb L, Sartori C, Lepori M, Nicod P, Scherrer U (1997) Cardiovascular and sympathetic effects of nitric oxide inhibition at rest and during static exercise in humans. Circulation 96:3897–3903

    CAS  PubMed  Google Scholar 

  • Padilla J, Sheldon RD, Sitar DM, Newcomer SC (2009) Impact of acute exposure to increased hydrostatic pressure and reduced shear rate on conduit artery endothelial function: a limb specific response. Am J Physiol Heart Circ Physiol 297:H1103–H1108

    CAS  PubMed  Google Scholar 

  • Padilla J, Young CN, Simmons GH, Deo SH, Newcomer SC, Sullivan JP, Laughlin MH, Fadel PJ (2010) Increased muscle sympathetic nerve activity acutely alters conduit artery shear rate patterns. Am J Physiol Heart Circ Physiol 298:H1128–H1135

    CAS  PubMed  Google Scholar 

  • Padilla J, Simmons GH, Fadel PJ, Laughlin MH, Joyner MJ, Casey DP (2011a) Impact of aging on conduit artery artery retrograde and oscillatory shear at rest and during exercise: role of nitric oxide. Hypertension 57:484–489

    CAS  PubMed Central  PubMed  Google Scholar 

  • Padilla J, Simmons GH, Vianna LC, Davis MJ, Laughlin MH, Fadel PJ (2011b) Brachial artery vasodilation during prolonged lower limb exercise: role of shear rate. Exp Physiol 96:1019–1027

    PubMed Central  PubMed  Google Scholar 

  • Palmer RM, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–526

    CAS  PubMed  Google Scholar 

  • Panza J, Quyyumi A, Brush JJ, Epsterin S (1990) Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. N Engl J Med 323:22–27

    CAS  PubMed  Google Scholar 

  • Passerini AG, Polacek DC, Shi C, Francesco NM, Manduchi E, Grant GR, Pritchard WF, Powell S, Chang GY, Stoeckert CJ Jr, Davies PF (2004) Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc Natl Acad Sci USA 101:2482–2487

    CAS  PubMed  Google Scholar 

  • Paton JF, Lonergan T, Deuchars J, James PE, Kasparov S (2006) Detection of angiotensin II mediated nitric oxide release within the nucleus of the solitary tract using electron-paramagnetic resonance (EPR) spectroscopy. Auton Neurosci 126–127:193–201

    PubMed  Google Scholar 

  • Perticone F, Ceravalo R, Pujia A, Ventura G, Iacopino S, Scozzafava A, Ferrano A, Chello M, Mastroroberto P, Verdecchia P, Schillaci G (2001) Prognostic significance of endothelial dysfunction in hypertensive patients. Circulation 104:191–196

    CAS  PubMed  Google Scholar 

  • Pl Pacher, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315–424

    Google Scholar 

  • Raitakari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, Jarvisalo MJ, Uhari M, Jokinen E, Ronnemaa T, Akerblom HK, Viikari JS (2003) Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA 290:2277–2283

    CAS  PubMed  Google Scholar 

  • Rapacz J, Hasler-Rapacz J, Taylor KM, Checovich WJ, Attie AD (1986) Lipoprotein mutations in pigs are associated with elevated plasma cholesterol and atherosclerosis. Science 234:1573–1577

    CAS  PubMed  Google Scholar 

  • Ray CA, Monahan KD (2002) Sympathetic vascular transduction is augmented in young normotensive blacks. J Appl Physiol 92:651–656

    PubMed  Google Scholar 

  • Ross R, Wight TN, Strandness E, Thiele B (1984) Human atherosclerosis. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. Am J Pathol 114:79–93

    CAS  PubMed  Google Scholar 

  • Sander M, Hansen PG, Victor RG (1995) Sympathetically mediated hypertension caused by chronic inhibition of nitric oxide. Hypertension 26:691–695

    CAS  PubMed  Google Scholar 

  • Sander M, Hansen J, Victor RG (1997) The sympathetic nervous system is involved in the maintenance but not initiation of the hypertension induced by N(omega)-nitro-l-arginine methyl ester. Hypertension 30:64–70

    CAS  PubMed  Google Scholar 

  • Sander M, Chavoshan B, Victor RG (1999) A large blood pressure-raising effect of nitric oxide synthase inhibition in humans. Hypertension 33:937–942

    CAS  PubMed  Google Scholar 

  • Sartori C, Lepori M, Scherrer U (2005) Interaction between nitric oxide and the cholinergic and sympathetic nervous system in cardiovascular control in humans. Pharmacol Ther 106:209–220

    CAS  PubMed  Google Scholar 

  • Schulz E, Jansen T, Wenzel P, Daiber A, Munzel T (2008) Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension. Antioxid Redox Signal 10:1115–1126

    CAS  PubMed  Google Scholar 

  • Shapoval LN, Sagach VF, Pobegailo LS (1991) Nitric oxide influences ventrolateral medullary mechanisms of vasomotor control in the cat. Neurosci Lett 132:47–50

    CAS  PubMed  Google Scholar 

  • Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93:13176–13181

    CAS  PubMed  Google Scholar 

  • Simmons GH, Padilla J, Young CN, Wong BJ, Lang JA, Davis MJ, Laughlin MH, Fadel PJ (2011) Increased brachial artery retrograde shear rate at exercise onset is abolished during prolonged cycling: role of thermoregulatory vasodilation. J Appl Physiol 110:389–397

    PubMed  Google Scholar 

  • Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW (1995) A definition of advanced types of atherosclerosis lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 92:1355–1374

    CAS  PubMed  Google Scholar 

  • Stauss HM, Godecke A, Mrowka R, Schrader J, Persson PB (1999) Enhanced blood pressure variability in eNOS knockout mice. Hypertension 33:1359–1363

    CAS  PubMed  Google Scholar 

  • Stewart KJ, Hiatt WR, Regensteiner JG, Hirsch AT (2002) Exercise training for claudication. N Engl J Med 347:1941–1951

    PubMed  Google Scholar 

  • Su C (1978) Modes of vasoconstrictor and vasodilator neurotransmission. Blood Vessels 15:183–189

    CAS  PubMed  Google Scholar 

  • Takabe W, Jen N, Ai L, Hamilton R, Wang S, Holmes K, Dharbandi F, Khalsa B, Bressler S, Barr ML, Li R, Hsiai TK (2011) Oscillatory shear stress induces mitochondrial superoxide production: implication of NADPH oxidase and c-Jun NH2-terminal kinase signaling. Antioxid Redox Signal 15:1379–1388

    CAS  PubMed  Google Scholar 

  • Thijssen DHJ, Dawson EA, Tinken TM, Cable NT, Green DJ (2009) Retrograde flow and shear rate acutely impair endothelial function in humans. Hypertension 53:986–992

    CAS  PubMed  Google Scholar 

  • Thubrikar MJ, Robicsek F (1995) Pressure-induced arterial wall stress and atherosclerosis. Ann Thorac Surg 59:1594–1603

    CAS  PubMed  Google Scholar 

  • Tinken TM, Thijssen DH, Hopkins N, Black MA, Dawson EA, Minson CT, Newcomer SC, Laughlin MH, Cable NT, Green DJ (2009) Impact of shear rate modulation on vascular function in humans. Hypertension 54:278–285

    CAS  PubMed Central  PubMed  Google Scholar 

  • Togashi H, Sakuma I, Yoshioka M, Kobayashi T, Yasuda H, Kitabatake A, Saito H, Gross SS, Levi R (1992) A central nervous system action of nitric oxide in blood pressure regulation. J Pharmacol Exp Ther 262:343–347

    CAS  PubMed  Google Scholar 

  • Traystman RJ, Moore LE, Helfaer MA, Davis S, Banasiak K, Williams M, Hurn PD (1995) Nitro-l-arginine analogues. Dose- and time-related nitric oxide synthase inhibition in brain. Stroke J Cereb Circ 26:864–869

    CAS  Google Scholar 

  • Tropea BI, Schwarzacher SP, Chang A, Asvar C, Huie P, Sibley RK, Zarins CK (2000) Reduction of aortic wall motion inhibits hypertension-mediated experimental atherosclerosis. Arterioscler Thromb Vasc Biol 20:2127–2133

    CAS  PubMed  Google Scholar 

  • Ungvari Z, Csiszar A, Huang A, Kaminski PM, Wolin MS, Koller A (2003) High pressure induces superoxide production in isolated arteries via protein kinase C-dependent activation of NAD(P)H oxidase. Circulation 108:1253–1258

    CAS  PubMed  Google Scholar 

  • Vallance P, Chan N (2001) Endothelial function and nitric oxide: clinical relevance. Heart 85:342–350

    CAS  PubMed  Google Scholar 

  • Vallance P, Collier J, Moncada S (1989) Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man. Lancet 2:997–1000

    CAS  PubMed  Google Scholar 

  • Vanhoutte PM, Verbeuren TJ, Webb RC (1981) Local modulation of adrenergic neuroeffector interaction in the blood vessel well. Physiol Rev 61:151–247

    CAS  PubMed  Google Scholar 

  • Vianna LC, Hart EC, Fairfax ST, Charkoudian N, Joyner MJ, Fadel PJ (2012) Influence of age and sex on the pressor response following a spontaneous burst of muscle sympathetic nerve activity. Am J Physiol Heart Circ Physiol 302:H2419–H2427

    CAS  PubMed  Google Scholar 

  • Vogt MT, Wolfson SK, Kuller LH (1993) Segmental arterial disease in the lower extremities: correlates of disease and relationship to mortality. J Clin Epidemiol 46:1267–1276

    CAS  PubMed  Google Scholar 

  • Wallin BG, Nerhed C (1982) Relationship between spontaneous variations of muscle sympathetic activity and succeeding changes in blood pressure in man. J Auton Nerv Syst 6:293–302

    CAS  PubMed  Google Scholar 

  • Wallin BG, Sundlof G, Delius W (1975) The effect of carotid sinus nerve stimulation on muscle and skin nerve sympathetic activity in man. Pflugers Arch 358:101–110

    CAS  PubMed  Google Scholar 

  • Wang DL, Wung BS, Shyy YJ, Lin CF, Chao YJ, Usami S, Chien S (1995) Mechanical strain induces monocyte chemotactic protein-1 gene expression in endothelial cells. Effects of mechanical strain on monocyte adhesion to endothelial cells. Circ Res 77:294–302

    CAS  PubMed  Google Scholar 

  • Waugh WH (1962) Adrenergic stimulation of depolarized arterial muscle. Circ Res 11:264–276

    CAS  PubMed  Google Scholar 

  • Willett NJ, Kundu K, Knight SF, Dikalov S, Murthy N, Taylor WR (2011) Redox signaling in an in vivo murine model of low magnitude oscillatory wall shear stress. Antioxid Redox Signal 15:1369–1378

    CAS  PubMed  Google Scholar 

  • Wung BS, Cheng JJ, Chao YJ, Lin J, Shyy YJ, Wang DL (1996) Cyclical strain increases monocyte chemotactic protein-1 secretion in human endothelial cells. Am J Physiol 270:H1462–H1468

    CAS  PubMed  Google Scholar 

  • Youmans PL, Green HD, Denison AB Jr (1955) Nature of the vasodilator and vasoconstrictor receptors in skeletal muscle of the dog. Circ Res 3:171–180

    CAS  PubMed  Google Scholar 

  • Young CN, Fisher JP, Gallagher KM, Whaley-Connell A, Chaudhary K, Victor RG, Thomas GD, Fadel PJ (2009) Inhibition of nitric oxide synthase evokes central sympatho-excitation in healthy humans. J Physiol 587:4977–4986

    CAS  PubMed  Google Scholar 

  • Young CN, Deo SH, Padilla J, Laughlin MH, Fadel PJ (2010) Pro-atherogenic shear rate patterns in the femoral artery of healhty older adults. Atherosclerosis 211:390–392

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zanzinger J, Czachurski J, Seller H (1995) Inhibition of basal and reflex-mediated sympathetic activity in the RVLM by nitric oxide. Am J Physiol 268:R958–R962

    CAS  PubMed  Google Scholar 

  • Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S (1983) Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res 53:502–514

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Dr. Seth Fairfax for his contributions to the data presented in Fig. 6. NTJ is supported by NIH T32-AR048523, MHL by NIH RO1-HL-036088, and PJF by NIH R01-HL093167.

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Correspondence to Jaume Padilla.

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Communicated by Nigel A.S. Taylor.

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Padilla, J., Jenkins, N.T., Laughlin, M.H. et al. Blood pressure regulation VIII: resistance vessel tone and implications for a pro-atherogenic conduit artery endothelial cell phenotype. Eur J Appl Physiol 114, 531–544 (2014). https://doi.org/10.1007/s00421-013-2684-x

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