Age-related autoregulatory dysfunction and cerebromicrovascular injury in mice with angiotensin II-induced hypertension

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 11, 2013, Pages 1732-1742

  Toth, Peter ^a   Tucsek, Zsuzsanna ^a   Sosnowska, Danuta ^a   Gautam, Tripti ^a   Mitschelen, Matthew ^a   Tarantini, Stefano ^a   Deak, Ferenc ^a   Koller, Akos ^b,c   Sonntag, William E ^a,d   Csiszar, Anna ^a,b,d   Ungvari, Zoltan ^a,b,d  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF PÉCS   (Hungary)

^c NEW YORK MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

blood brain barrier; CBF; dementia; inflammation; myogenic; TRPC

Indexed keywords

3 NITROTYROSINE; ANGIOTENSIN II;

AGING; ANIMAL EXPERIMENT; ARTICLE; AUTOREGULATORY DYSFUNCTION; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; BRAIN BLOOD FLOW; CAPILLARY DENSITY; CEREBROMICROVASCULAR INJURY; HEMODYNAMICS; HYPERTENSION; MALE; MIDDLE CEREBRAL ARTERY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ADAPTATION, PHYSIOLOGICAL; AGING; ANGIOTENSIN II; ANIMALS; BEHAVIOR, ANIMAL; BLOOD-BRAIN BARRIER; CEREBROVASCULAR CIRCULATION; CYTOKINES; DISEASE MODELS, ANIMAL; HYDROXYEICOSATETRAENOIC ACIDS; HYPERTENSION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROVESSELS; MIDDLE CEREBRAL ARTERY; TRPC CATION CHANNELS; UP-REGULATION;

EID: 84887041623     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.143     Document Type: Article

References (46)

1. Aronow WS, Fleg JL, Pepine CJ, Artinian NT, Bakris G, Brown AS et al. ACCF/AHA 2011 expert consensus document on hypertension in the elderly: a report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents. Circulation 2011; 123: 2434-2506.
2. Iadecola C, Park L, Capone C. Threats to the mind: aging, amyloid, and hypertension. Stroke 2009; 40: S40-S44.
3. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2011; 42: 2672-2713.
4. Brickman AM, Reitz C, Luchsinger JA, Manly JJ, Schupf N, Muraskin J et al. Long-term blood pressure fluctuation and cerebrovascular disease in an elderly cohort. Arch Neurol 2010; 67: 564-569.
5. Reitz C, Tang MX, Manly J, Mayeux R, Luchsinger JA. Hypertension and the risk of mild cognitive impairment. Arch Neurol 2007; 64: 1734-1740. (Pubitemid 350254935)
6. Kuller LH, Lopez OL, Jagust WJ, Becker JT, DeKosky ST, Lyketsos C et al. Determinants of vascular dementia in the cardiovascular health cognition study. Neurology 2005; 64: 1548-1552. (Pubitemid 40617690)
7. Hachinski V, Iadecola C, Petersen RC, Breteler MM, Nyenhuis DL, Black SE et al. National institute of neurological disorders and stroke-canadian stroke network vascular cognitive impairment harmonization standards. Stroke 2006; 37: 2220-2241. (Pubitemid 44337162)
8. Paulson OB, Strandgaard S, Edvinsson L. Cerebral autoregulation. Cerebrovasc Brain Metab Rev 1990; 2: 161-192.
9. Strandgaard S, Jones JV, MacKenzie ET, Harper AM. Upper limit of cerebral blood flow autoregulation in experimental renovascular hypertension in the baboon. Circ Res 1975; 37: 164-167.
10. Harper SL, Bohlen HG. Microvascular adaptation in the cerebral cortex of adult spontaneously hypertensive rats. Hypertension 1984; 6: 408-419. (Pubitemid 14091470)
11. Kontos HA, Wei EP, Navari RM, Levasseur JE, Rosenblum WI, Patterson Jr. JL. Responses of cerebral arteries and arterioles to acute hypotension and hypertension. Am J Physiol 1978; 234: H371-H383. (Pubitemid 9125782)
12. Osol G, Halpern W. Myogenic properties of cerebral blood vessels from normotensive and hypertensive rats. Am J Physiol 1985; 249: H914-H921. (Pubitemid 16197331)
13. Kontos HA, Wei EP, Raper AJ, Rosenblum WI, Navari RM, Patterson Jr. JL. Role of tissue hypoxia in local regulation of cerebral microcirculation. Am J Physiol 1978; 234: H582-H591.
14. Smeda JS. Cerebral vascular changes associated with hemorrhagic stroke in hypertension. Can J Physiol Pharmacol 1992; 70: 552-564.
15. Koller A, Toth P. Contribution of flow-dependent vasomotor mechanisms to the autoregulation of cerebral blood flow. J Vasc Res 2012; 49: 375-389.
16. Toth P, Rozsa B, Springo Z, Doczi T, Koller A. Isolated human and rat cerebral arteries constrict to increases in flow: Role of 20-HETE and TP receptors. J Cereb Blood Flow Metab 2011; 31: 2096-2105.
17. Gebremedhin D, Lange AR, Lowry TF, Taheri MR, Birks EK, Hudetz AG et al. Production of 20-HETE and its role in autoregulation of cerebral blood flow. Circ Res 2000; 87: 60-65. (Pubitemid 30456936)
18. Winkler EA, Bell RD, Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci 2011; 14: 1398-1405.
19. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008; 57: 178-201.
20. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010; 68: 409-427.
21. Capone C, Faraco G, Park L, Cao X, Davisson RL, Iadecola C. The cerebrovascular dysfunction induced by slow pressor doses of Angiotensin II precedes the development of hypertension. Am J Physiol Heart Circ Physiol 2011; 300: H397-H407.
22. Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 1990; 66: 8-17. (Pubitemid 20033921)
23. 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 Heart Circ Physiol 2003; 284: H1212-H1216. (Pubitemid 36348584)
24. Dunn KM, Renic M, Flasch AK, Harder DR, Falck J, Roman RJ. Elevated production of 20-HETE in the cerebral vasculature contributes to severity of ischemic stroke and oxidative stress in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 2008; 295: H2455-H2465.
25. Roman RJ. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 2002; 82: 131-185. (Pubitemid 34654217)
26. Muller DN, Schmidt C, Barbosa-Sicard E, Wellner M, Gross V, Hercule H et al. Mouse cyp4a isoforms: enzymatic properties, gender-and strain-specific expression, and role in renal 20-hydroxyeicosatetraenoic acid formation. Biochem J 2007; 403: 109-118. (Pubitemid 46569872)
27. Inoue R, Jensen LJ, Jian Z, Shi J, Hai L, Lurie AI et al. Synergistic activation of vascular trpc6 channel by receptor and mechanical stimulation via phospholipase c/diacylglycerol and phospholipase a2/omega-hydroxylase/20-hete pathways. Circ Res 2009; 104: 1399-1409.
28. Welsh DG, Morielli AD, Nelson MT, Brayden JE. Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res 2002; 90: 248-250. (Pubitemid 34633924)
29. Linde CI, Karashima E, Raina H, Zulian A, Wier WG, Hamlyn JM et al. Increased arterial smooth muscle ca2\+ signaling, vasoconstriction, and myogenic reactivity in milan hypertensive rats. Am J Physiol Heart Circ Physiol 2012; 302: H611-H620.
30. Bae YM, Kim A, Lee YJ, Lim W, Noh YH, Kim EJ et al. Enhancement of receptoroperated cation current and trpc6 expression in arterial smooth muscle cells of deoxycorticosterone acetate-salt hypertensive rats. J Hypertens 2007; 25: 809-817. (Pubitemid 46398876)
31. Pulina MV, Zulian A, Baryshnikov SG, Linde CI, Karashima E, Hamlyn JM et al. Cross talk between plasma membrane Na(\+)/Ca (2\+) exchanger-1 and TRPC/Oraicontaining channels: key players in arterial hypertension. Adv Exp Med Biol 2013; 961: 365-374.
32. Zulian A, Baryshnikov SG, Linde CI, Hamlyn JM, Ferrari P, Golovina VA. Upregulation of Na\+/Ca2\+ exchanger and TRPC6 contributes to abnormal Ca2\+ homeostasis in arterial smooth muscle cells from milan hypertensive rats. Am J Physiol Heart Circ Physiol 2010; 299: H624-H633.
33. Takahashi H. Upregulation of the renin-angiotensin-aldosterone-ouabain system in the brain is the core mechanism in the genesis of all types of hypertension. Int J Hypertens 2012; 2012: 242786.
34. Huang BS, Ahmadi S, Ahmad M, White RA, Leenen FH. Central neuronal activation and pressor responses induced by circulating ANG II: role of the brain aldosterone-" ouabain" pathway. Am J Physiol Heart Circ Physiol 2010; 299: H422-H430.
35. Ungvari Z, Csiszar A. The emerging role of IGF-1 deficiency in cardiovascular aging: Recent advances. J Gerontol A Biol Sci Med Sci 2012; 67: 599-610.
36. Girouard H, Park L, Anrather J, Zhou P, Iadecola C. Angiotensin II attenuates endothelium-dependent responses in the cerebral microcirculation through Nox-2-derived radicals. Arterioscler Thromb Vasc Biol 2006; 26: 826-832. (Pubitemid 43732158)
37. Girouard H, Park L, Anrather J, Zhou P, Iadecola C. Cerebrovascular nitrosative stress mediates neurovascular and endothelial dysfunction induced by angiotensin II. Arterioscler Thromb Vasc Biol 2007; 27: 303-309. (Pubitemid 46143044)
38. Fernandez-Vizarra P, Lopez-Franco O, Mallavia B, Higuera-Matas A, Lopez-Parra V, Ortiz-Munoz G et al. Immunoglobulin g fc receptor deficiency prevents Alzheimer-like pathology and cognitive impairment in mice. Brain 2012; 135: 2826-2837.
39. Gao HM, Liu B, Zhang W, Hong JS. Critical role of microglial NADPH oxidasederived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J 2003; 17: 1954-1956.
40. Kaneko YS, Nakashima A, Mori K, Nagatsu T, Nagatsu I, Ota A. Microglial activation in neuroinflammation: implications for the etiology of neurodegeneration. Neurodegener Dis 2012; 10: 100-103.
41. PROGRESS Collaborative Group. Randomised trial of a perindopril-based bloodpressure-lowering regimen among 6,105 individuals with previous stroke or transient ischaemic attack. Lancet 2001; 358: 1033-1041.
42. Forette F, Seux ML, Staessen JA, Thijs L, Birkenhager WH, Babarskiene MR et al. Prevention of dementia in randomised double-blind placebo-controlled Systolic Hypertension in Europe (Syst-Eur) trial. Lancet 1998; 352: 1347-1351. (Pubitemid 28510916)
43. Trenkwalder P. The study on cognition and prognosis in the elderly (scope)-recent analyses. J Hypertens Suppl 2006; 24: S107-S114. (Pubitemid 44336832)
44. Dietrich A, Mederos YSM, Gollasch M, Gross V, Storch U, Dubrovska G et al. Increased vascular smooth muscle contractility in TRPC6-/-mice. Mol Cell Biol 2005; 25: 6980-6989. (Pubitemid 41105898)
45. Boulay G, Zhu X, Peyton M, Jiang M, Hurst R, Stefani E et al. Cloning and expression of a novel mammalian homolog of drosophila transient receptor potential (Trp) involved in calcium entry secondary to activation of receptors coupled by the Gq class of G protein. J Biol Chem 1997; 272: 29672-29680.
46. Poels MM, Ikram MA, van der Lugt A, Hofman A, Krestin GP, Breteler MM et al. Incidence of cerebral microbleeds in the general population: The Rotterdam Scan Study. Stroke 2011; 42: 656-661.