Regulation of myogenic tone and structure of parenchymal arterioles by hypertension and the mineralocorticoid receptor

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 1, 2015, Pages H127-H136

  Pires, Paulo W ^a,b   Jackson, William F ^a   Dorrance, Anne M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebral parenchymal arterioles; Hypertension; Inward remodeling; Mineralocorticoid receptor; Myogenic tone

Indexed keywords

CALCIUM CHANNEL L TYPE; MINERALOCORTICOID RECEPTOR; ANTIHYPERTENSIVE AGENT; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; EPLERENONE; HYDRALAZINE; HYDROCHLOROTHIAZIDE; MINERALOCORTICOID ANTAGONIST; NIFEDIPINE; RESERPINE; SPIRONOLACTONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTERY DIAMETER; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; HYPERTENSION; INTESTINE PRESSURE; MALE; MUSCLE TONE; NONHUMAN; PARENCHYMA CELL; PRIORITY JOURNAL; RAT; STROKE PRONE SPONTANEOUSLY HYPERTENSIVE RAT; ANALOGS AND DERIVATIVES; ANIMAL; ARTERIAL STIFFNESS; BRAIN; BRAIN CIRCULATION; COMPLIANCE (PHYSICAL); DRUG EFFECTS; METABOLISM; MIDDLE CEREBRAL ARTERY; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPONTANEOUSLY HYPERTENSIVE RAT; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE; VASCULARIZATION; WISTAR KYOTO RAT;

ANIMALS; ANTIHYPERTENSIVE AGENTS; ARTERIOLES; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CEREBROVASCULAR CIRCULATION; CEREBRUM; COMPLIANCE; HYDRALAZINE; HYDROCHLOROTHIAZIDE; HYPERTENSION; MIDDLE CEREBRAL ARTERY; MINERALOCORTICOID RECEPTOR ANTAGONISTS; MUSCLE TONUS; MUSCLE, SMOOTH, VASCULAR; NIFEDIPINE; ORGAN SIZE; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RECEPTORS, MINERALOCORTICOID; RESERPINE; SPIRONOLACTONE; VASCULAR REMODELING; VASCULAR STIFFNESS;

EID: 84935516567     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00168.2015     Document Type: Article

References (64)

1. Auriel E, Csiba L, Berenyi E, Varkonyi I, Mehes G, Kardos L, Karni A, Bornstein NM. Leukoaraiosis is associated with arterial wall thickness: a quantitative analysis. Neuropathology 32: 227–233, 2012.
2. Baumbach GL, Hajdu MA. Mechanics and composition of cerebral arterioles in renal and spontaneously hypertensive rats. Hypertension 21: 816–826, 1993.
3. Baumbach GL, Heistad DD. Remodeling of cerebral arterioles in chronic hypertension. Hypertension 13: 968–972, 1989.
4. Baumbach GL, Heistad DD, Siems JE. Effect of sympathetic nerves on composition and distensibility of cerebral arterioles in rats. J Physiol 416: 123–140, 1989.
5. Baumbach GL, Walmsley JG, Hart MN. Composition and mechanics of cerebral arterioles in hypertensive rats. Am J Pathol 133: 464–471, 1988.
6. Chan SL, Chapman AC, Sweet JG, Gokina NI, Cipolla MJ. Effect of PPARgamma inhibition during pregnancy on posterior cerebral artery function and structure. Front Physiol 1: 130, 2010.
7. Chan SL, Sweet JG, Cipolla MJ. Treatment for cerebral small vessel disease: effect of relaxin on the function and structure of cerebral paren-chymal arterioles during hypertension. FASEB J 27: 3917–3927, 2013.
8. Chrissobolis S, Sobey CG. Evidence that Rho-kinase activity contributes to cerebral vascular tone in vivo and is enhanced during chronic hypertension: comparison with protein kinase C. Circ Res 88: 774–779, 2001.
9. Cipolla MJ. The Cerebral Circulation. San Rafael, CA: Morgan & Claypool Life Sciences, 2009.
10. Cipolla MJ, Li R, Vitullo L. Perivascular innervation of penetrating brain parenchymal arterioles. J Cardiovasc Pharmacol 44: 1–8, 2004.
11. Cipolla MJ, Sweet J, Chan SL, Tavares MJ, Gokina N, Brayden JE. Increased pressure-induced tone in rat parenchymal arterioles vs. middle cerebral arteries: role of ion channels and calcium sensitivity. J Appl Physiol 117: 53–59, 2014.
12. Cohen Z, Bonvento G, Lacombe P, Hamel E. Serotonin in the regulation of brain microcirculation. Prog Neurobiol 50: 335–362, 1996.
13. Cohen Z, Molinatti G, Hamel E. Astroglial and vascular interactions of noradrenaline terminals in the rat cerebral cortex. J Cereb Blood Flow Metab 17: 894-904, 1997.
14. Cox RH, Rusch NJ. New expression profiles of voltage-gated ion channels in arteries exposed to high blood pressure. Microcirculation 9: 243-257, 2002.
15. Davis MJ, Hill MA. Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79: 387-423, 1999.
16. de la Torre JC. Cerebral hemodynamics and vascular risk factors: setting the stage for Alzheimer’s disease. J Alzheimers Dis 32: 553-567, 2012.
17. Dorrance AM, Pollock DM, Romanko OP, Stepp DW. A high-potassium diet reduces infarct size and improves vascular structure in hypertensive rats. Am J Physiol Regul Integr Comp Physiol 292: R415-R422, 2007.
18. Duckworth JW, Wellman GC, Walters CL, Bevan JA. Aminergic histofluorescence and contractile responses to transmural electrical field stimulation and norepinephrine of human middle cerebral arteries obtained promptly after death. Circ Res 65: 316-324, 1989.
19. Dunn KM, Nelson MT. Neurovascular signaling in the brain and the pathological consequences of hypertension. Am J Physiol Heart Circ Physiol 306: H1-H14, 2014.
20. Dunn WR, Wallis SJ, Gardiner SM. Remodelling and enhanced myogenic tone in cerebral resistance arteries isolated from genetically hypertensive Brattleboro rats. J Vasc Res 35: 18-26, 1998.
21. Endemann DH, Touyz RM, Iglarz M, Savoia C, Schiffrin EL. Epler-enone prevents salt-induced vascular remodeling and cardiac fibrosis in stroke-prone spontaneously hypertensive rats. Hypertension 43: 1252-1257, 2004.
22. Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 66: 8-17, 1990.
23. Gonzalez JM, Somoza B, Conde MV, Fernandez-Alfonso MS, Gonzalez MC, Arribas SM. Hypertension increases middle cerebral artery resting tone in spontaneously hypertensive rats: role of tonic vasoactive factor availability. Clin Sci (Lond) 114: 651-659, 2008.
24. Hajdu MA, Baumbach GL. Mechanics of large and small cerebral arteries in chronic hypertension. Am J Physiol Heart Circ Physiol 266: H1027-H1033, 1994.
25. Halaris AE, Freedman DX. Loss of body weight as a predictor of reserpine-induced amine depletion. Eur J Pharmacol 32: 93-101, 1975.
26. Hamel E. Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100: 1059-1064, 2006.
27. Hart MN, Heistad DD, Brody MJ. Effect of chronic hypertension and sympathetic denervation on wall/lumen ratio of cerebral vessels. Hypertension 2: 419-423, 1980.
28. Hilgers RH, Todd J Jr, Webb RC. Increased PDZ-RhoGEF/RhoA/Rho kinase signaling in small mesenteric arteries of angiotensin II-induced hypertensive rats. J Hypertens 25: 1687-1697, 2007.
29. Hill MA, Zou H, Potocnik SJ, Meininger GA, Davis MJ. Invited review: arteriolar smooth muscle mechanotransduction: Ca2+ signaling pathways underlying myogenic reactivity. J Appl Physiol 91: 973-983, 2001.
30. Hogestatt ED, Andersson KE. On the postjunctional alpha-adrenorecep-tors in rat cerebral and mesenteric arteries. J Auton Pharmacol 4:161-173, 1984.
31. Iadecola C, Davisson RL. Hypertension and cerebrovascular dysfunction. Cell Metab 7: 476–484, 2008.
32. Ibrahim J, McGee A, Graham D, McGrath JC, Dominiczak AF. Sex-specific differences in cerebral arterial myogenic tone in hypertensive and normotensive rats. Am J Physiol Heart Circ Physiol 290: H1081-H1089, 2006.
33. Izzard AS, Bund SJ, Heagerty AM. Myogenic tone in mesenteric arteries from spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 270: H1-H6, 1996.
34. Joseph BK, Thakali KM, Moore CL, Rhee SW. Ion channel remodeling in vascular smooth muscle during hypertension: implications for novel therapeutic approaches. Pharm Res 70: 126-138, 2013.
35. Joutel A, Monet-Lepretre M, Gosele C, Baron-Menguy C, Hammes A, Schmidt S, Lemaire-Carrette B, Domenga V, Schedl A, Lacombe P, Hubner N. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J Clin Invest 120: 433-445, 2010.
36. Kang KT, Sullivan JC, Spradley FT, d’Uscio LV, Katusic ZS, Pollock JS. Antihypertensive therapy increases tetrahydrobiopterin levels and NO/cGMP signaling in small arteries of angiotensin II-infused hypertensive rats. Am J Physiol Heart Circ Physiol 300: H718–H724, 2011.
37. Lammie GA. Hypertensive cerebral small vessel disease and stroke. Brain Pathol 12: 358–370, 2002.
38. Lincoln J. Innervation of cerebral arteries by nerves containing 5-hy-droxytryptamine and noradrenaline. Pharmacol Ther 68: 473–501, 1995.
39. Moody DM, Bell MA, Challa VR. Features of the cerebral vascular pattern that predict vulnerability to perfusion or oxygenation deficiency: an anatomic study. AJNR Am J Neuroradiol 11: 431–439, 1990.
40. Mukai Y, Shimokawa H, Matoba T, Kandabashi T, Satoh S, Hiroki J, Kaibuchi K, Takeshita A. Involvement of Rho-kinase in hypertensive vascular disease: a novel therapeutic target in hypertension. FASEB J 15: 1062–1064, 2001.
41. Nishimura N, Schaffer CB, Friedman B, Lyden PD, Kleinfeld D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc Natl Acad Sci U S A 104: 365–370, 2007.
42. O’Brien RC, Cooper ME, Jerums G, Doyle AE. The effects of perin-dopril and triple therapy in a normotensive model of diabetic nephropathy. Diabetes 42: 604–609, 1993.
43. Ohya Y, Tsuchihashi T, Kagiyama S, Abe I, Fujishima M. Single L-type calcium channels in smooth muscle cells from resistance arteries of spontaneously hypertensive rats. Hypertension 31: 1125–1129, 1998.
44. Osol G, Halpern W. Myogenic properties of cerebral blood vessels from normotensive and hypertensive rats. Am J Physiol Heart Circ Physiol 249: H914–H921, 1985.
45. Pantoni L, Garcia JH. Cognitive impairment and cellular/vascular changes in the cerebral white matter. Ann N Y Acad Sci 826: 92–102, 1997.
46. Pires PW, Dams Ramos CM, Matin N, Dorrance AM. The effects of hypertension on the cerebral circulation. Am J Physiol Heart Circ Physiol 304: H1598–H1614, 2013.
47. Pires PW, Deutsch C, McClain JL, Rogers CT, Dorrance AM. Tempol, a superoxide dismutase mimetic, prevents cerebral vessel remodeling in hypertensive rats. Microvasc Res 80: 445–452, 2010.
48. Pires PW, Girgla SS, McClain JL, Kaminski NE, van Rooijen N, Dorrance AM. Improvement in middle cerebral artery structure and endothelial function in stroke-prone spontaneously hypertensive rats after macrophage depletion. Microcirculation 20: 650–661, 2013.
49. Pires PW, Rogers CT, McClain JL, Garver HS, Fink GD, Dorrance AM. Doxycycline, a matrix metalloprotease inhibitor, reduces vascular remodeling and damage after cerebral ischemia in stroke-prone spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 301: H87–H97, 2011.
50. Qiu C, Fratiglioni L. A major role for cardiovascular burden in age-related cognitive decline. Nat Rev Cardiol 12: 267–277, 2015.
51. Rensen SS, Doevendans PA, van Eys GJ. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J 15: 100-108, 2007.
52. Reusch P, Wagdy H, Reusch R, Wilson E, Ives HE. Mechanical strain increases smooth muscle and decreases nonmuscle myosin expression in rat vascular smooth muscle cells. Circ Res 79: 1046-1053, 1996.
53. Rigsby CS, Ergul A, Portik Dobos V, Pollock DM, Dorrance AM. Effects of spironolactone on cerebral vessel structure in rats with sustained hypertension. Am J Hypertens 24: 708-715, 2011.
54. Rigsby CS, Pollock DM, Dorrance AM. Spironolactone improves structure and increases tone in the cerebral vasculature of male spontaneously hypertensive stroke-prone rats. Microvasc Res 73: 198-205, 2007.
55. Rusch NJ, Hermsmeyer K. Calcium currents are altered in the vascular muscle cell membrane of spontaneously hypertensive rats. Circ Res 63: 997-1002, 1988.
56. Schubert R, Lidington D, Bolz SS. The emerging role of Ca2+ sensitivity regulation in promoting myogenic vasoconstriction. Cardiovasc Res 77: 8-18, 2008.
57. Shih AY, Blinder P, Tsai PS, Friedman B, Stanley G, Lyden PD, Kleinfeld D. The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat Neurosci 16: 55-63, 2013.
58. Sonkusare S, Palade PT, Marsh JD, Telemaque S, Pesic A, Rusch NJ. Vascular calcium channels and high blood pressure: pathophysiology and therapeutic implications. Vascul Pharmacol 44: 131-142, 2006.
59. Velasquez MT, Striffler JS, Abraham AA, Michaelis OE Scalbert E, Thibault N. Perindopril ameliorates glomerular and renal tubulointersti-tial injury in the SHR/N-corpulent rat. Hypertension 30: 1232-1237, 1997.
60. Weber DS, Webb RC. Enhanced relaxation to the rho-kinase inhibitor Y-27632 in mesenteric arteries from mineralocorticoid hypertensive rats. Pharmacology 63: 129-133, 2001.
61. Westcott EB, Jackson WF. Heterogeneous function of ryanodine receptors, but not IP3 receptors, in hamster cremaster muscle feed arteries and arterioles. Am J Physiol Heart Circ Physiol 300: H1616-H1630, 2011.
62. Yang ST, Mayhan WG, Faraci FM, Heistad DD. Endothelium-depen-dent responses of cerebral blood vessels during chronic hypertension. Hypertension 17: 612-618, 1991.
63. Zakrzeska A, Gromotowicz-Poplawska A, Szemraj J, Szoka P, Kisiel W, Purta T, Kasacka I, Chabielska E. Eplerenone reduces arterial thrombosis in diabetic rats. J Renin Angiotensin Aldosterone Syst. In press.
64. Zhao Y, Gong CX. From chronic cerebral hypoperfusion to Alzheimerlike brain pathology and neurodegeneration. Cell Mol Neurobiol 35: 101-110, 2015.