Neurovascular regulation in the ischemic brain

Antioxidants and Redox Signaling

Volumn 22, Issue 2, 2015, Pages 149-160

  Jackman, Katherine ^a   Iadecola, Costantino ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD PRESSURE; BLOOD VESSEL OCCLUSION; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN CIRCULATION; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; COLLATERAL CIRCULATION; DIABETES MELLITUS; HUMAN; HYPEREMIA; HYPERTENSION; NONHUMAN; REVIEW; RISK FACTOR; VASCULARIZATION; ANIMAL; BRAIN; METABOLISM; PIG; RAT;

ANIMALS; BRAIN; BRAIN ISCHEMIA; HUMANS; HYPERTENSION; RATS; RISK FACTORS; STROKE; SWINE;

EID: 84920157539     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5669     Document Type: Review

References (83)

1. Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, and Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 37: 13-25, 2010.
2. Alexander RW. Theodore Cooper Memorial Lecture. Hypertension and the pathogenesis of atherosclerosis. Oxidative stress and the mediation of arterial inflammatory response: a new perspective. Hypertension 25: 155-161, 1995.
3. Andresen J, Shafi NI, and Bryan RM. Endothelial influences on cerebrovascular tone. J Appl Physiol 100: 318-327, 2006.
4. Aoi MC, Hu K, Lo M-T, Selim M, Olufsen MS, and Novak V. Impaired cerebral autoregulation is associated with brain atrophy and worse functional status in chronic ischemic stroke. PLoS One 7: e46794, 2012.
5. Aries MJH, Elting JW, De Keyser J, Kremer BPH, and Vroomen PCAJ. Cerebral autoregulation in stroke: a review of transcranial Doppler studies. Stroke 41: 2697-2704, 2010.
6. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, Fini ME, and Lo EH. Effects of matrix metallopro-teinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21: 7724-7732, 2001.
7. Astrup J, Siesjo BK, and Symon L. Thresholds in cerebral ischemia-the ischemic penumbra. Stroke 12: 723-725, 1981.
8. Baker WB, Sun Z, Hiraki T, Putt ME, Durduran T, Reivich M, Yodh AG, and Greenberg JH. Neurovascular coupling varies with level of global cerebral ischemia in a rat model. J Cereb Blood Flow Metab 33: 97-105, 2012.
9. Bang OY, Saver JL, Buck BH, Alger JR, Starkman S, Ovbiagele B, Kim D, Jahan R, Duckwiler GR, Yoon SR, Vinuela F, and Liebeskind DS. UCLA Collateral Investigators. Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry 79: 625-629, 2008.
10. Baumbach GL, and Heistad DD. Cerebral circulation in chronic arterial hypertension. Hypertension 12: 89-95, 1988.
11. Beckman JA, Creager MA, and Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 287: 2570-2581, 2002.
12. Bentsen N, Larsen B, and Lassen NA. Chronically impaired autoregulation of cerebral blood flow in long-term diabetics. Stroke 6: 497-502, 1975.
13. Blicher JU, Stagg CJ, Shea JOA, Stergaard LO, MacIntosh BJ, Johansen-Berg H, Jezzard P, and Donahue MJ. Visualization of altered neurovascular coupling in chronic stroke patients using multimodal functional MRI. J Cereb Blood Flow Metab 32: 2044-2054, 2012.
14. Blinder P, Shih AY, Rafie C, and Kleinfeld D. Topological basis for the robust distribution of blood to rodent neo-cortex. Proc Natl Acad Sci 107: 12670-12675, 2010.
15. Blinder P, Tsai PS, Kaufhold JP, Knutsen PM, Suhl H, and Kleinfeld D. The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow. Nat Neurosci 16: 889-897, 2013.
16. Buma FE, Lindeman E, Ramsey NF, and Kwakkel G. Functional neuroimaging studies of early upper limb recovery after stroke: a systematic review of the literature. Neurorehabil Neural Repair 24: 589-608, 2010.
17. Calcinaghi N, Wyss MT, Jolivet R, Singh A, Keller AL, Winnik S, Fritschy JM, Buck A, Matter CM, and Weber B. Multimodal imaging in rats reveals impaired neurovascular coupling in sustained hypertension. Stroke 44: 1957-1964, 2013.
18. Capone C, Faraco G, Park L, Cao X, Davisson RL, and Iadecola C. The cerebrovascular dysfunction induced by slow pressor doses of angiotensin II precedes the development of hypertension. Am J Physiol 300: H397-H407, 2011.
19. Capone C, Faraco G, Peterson JR, Coleman C, Anrather J, Milner TA, Pickel VM, Davisson RL, and Iadecola C. Central cardiovascular circuits contribute to the neurovas-cular dysfunction in angiotensin II hypertension. J Neurosci 32: 4878-4886, 2012.
20. Cipolla MJ. The Cerebral Circulation. San Rafael, CA: Morgan & Claypool Life Sciences, 2009.
21. Dabertrand F, Hannah RM, Pearson JM, Hill-Eubanks DC, Brayden JE, and Nelson MT. Prostaglandin E2, a postulated astrocyte-derived neurovascular coupling agent, constricts rather than dilates parenchymal arterioles. J Cereb Blood Flow Metab 33: 479-482, 2013.
22. del Zoppo GJ and Hallenbeck JM. Advances in the vascular pathophysiology of ischemic stroke. Thromb Res 98: 73-81, 2000.
23. Delles C, Michelson G, Harazny J, Oehmer S, Hilgers KF, and Schmieder RE. Impaired endothelial function of the retinal vasculature in hypertensive patients. Stroke 35: 1289-1293, 2004.
24. Dirnagl U and Pulsinelli W. Autoregulation of cerebral blood flow in experimental focal brain ischemia. J Cereb Blood Flow Metab 10: 327-336, 1990.
25. Drake CT and Iadecola C. The role of neuronal signaling in controlling cerebral blood flow. Brain Lang 102: 141-152, 2007.
26. Faraci FM. Protecting against vascular disease in brain. Am J Physiol 300: H1566-H1582, 2011.
27. Faraci FM and Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 66: 8-17, 1990.
28. Faraco G and Iadecola C. Hypertension: a harbinger of stroke and dementia. Hypertension 62: 810-817.
29. Giannopoulos S, Katsanos AH, Tsivgoulis G, and Marshall RS. Statins and cerebral hemodynamics. J Cereb Blood Flow Metab 32: 1973-1976, 2012.
30. Ginsberg MD, Castella Y, Dietrich WD, Watson BD, and Busto R. Acute thrombotic infarction suppresses metabolic activation of ipsilateral somatosensory cortex: evidence for functional diaschisis. J Cereb Blood Flow Metab 9: 329-341, 1989.
31. Girouard H and Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100: 328-335, 2006.
32. Girouard H, Park L, Anrather J, Zhou P, and Iadecola C. Cerebrovascular nitrosative stress mediates neurovascular and endothelial dysfunction induced by angiotensin II. Arterioscler Thromb Vasc Biol 27: 303-309, 2007.
33. Harris AK, Hutchinson JR, Sachidanandam K, Johnson MH, Dorrance AM, Stepp DW, Fagan SC, and Ergul A. Type 2 diabetes causes remodeling of cerebrovasculature via differential regulation of matrix metalloproteinases and collagen synthesis: role of endothelin-1. Diabetes 54: 2638-2644, 2005.
34. Hirsch S, Reichold J, Schneider M, Székely G, and Weber B. Topology and hemodynamics of the cortical cerebro-vascular system. J Cereb Blood Flow Metab 32: 952-967, 2012.
35. Hu K, Lo M-T, Peng C-K, Liu Y, and Novak V. A nonlinear dynamic approach reveals a long-term stroke effect on cerebral blood flow regulation at multiple time scales. PLoS Comp Biol 8: e1002601, 2012.
36. Hu K, Peng CK, Huang NE, Wu Z, Lipsitz LA, Cavallerano J, and Novak V. Altered phase interactions between spontaneous blood pressure and flow fluctuations in type 2 diabetes mellitus: nonlinear assessment of cerebral autoregulation. Physica A 387: 2279-2292, 2008.
37. Huber JD. Diabetes, cognitive function, and the blood-brain barrier. Curr Pharm Des 14: 1594-1600, 2008.
38. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5: 347-360, 2004.
39. Iadecola C and Davisson RL. Hypertension and cerebro-vascular dysfunction. Cell Metab 7: 476-484, 2008.
40. Iadecola C and Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci 10: 1369-1376, 2007.
41. Immink RV, van Montfrans GA, Stam J, Karemaker JM, Diamant M, and van Lieshout JJ. Dynamic cerebral auto-regulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke 36: 2595-2600, 2005.
42. Inao S, Tadokoro M, Nishino M, Mizutani N, Terada K, Bundo M, Kuchiwaki H, and Yoshida J. Neural activation of the brain with hemodynamic insufficiency. J Cereb Blood Flow Metab 18: 960-967, 1998.
43. Jennings JR, Muldoon MF, Ryan C, Price JC, Greer P, Sutton-Tyrrell K, van der Veen FM, and Meltzer CC. Reduced cerebral blood flow response and compensation among patients with untreated hypertension. Neurology 64: 1358-1365, 2005.
44. Kazama K, Anrather J, Zhou P, Girouard H, Frys K, Milner TA, and Iadecola C. Angiotensin II impairs neurovascular coupling in neocortex through NADPH oxidase-derived radicals. Circ Res 95: 1019-1026, 2004.
45. Kazama K, Wang G, Frys K, Anrather J, and Iadecola C. Angiotensin II attenuates functional hyperemia in the mouse somatosensory cortex. Am J Physiol 285: H1890-H1899, 2003.
46. Kelly-Cobbs AI, Prakash R, Coucha M, Knight RA, Li W, Ogbi SN, Johnson M, and Ergul A. Cerebral myogenic reactivity and blood flow in type 2 diabetic rats: role of peroxynitrite in hypoxia-mediated loss of myogenic tone. J Pharmacol Exp Therapeut 342: 407-415, 2012.
47. Kim Y-S, Immink RV, Stok WJ, Karemaker JM, Secher NH, and van Lieshout JJ. Dynamic cerebral autoregulatory capacity is affected early in type 2 diabetes. Clin Sci 115: 255-262, 2008.
48. Kunz A and Iadecola C. Chapter 14 cerebral vascular dysregulation in the ischemic brain. Handb Clin Neurol 92: 283-305, 2009.
49. Kunz A, Park L, Abe T, Gallo EF, Anrather J, Zhou P, and Iadecola C. Neurovascular protection by ischemic tolerance: role of nitric oxide and reactive oxygen species. J Neurosci 27: 7083-7093, 2007.
50. Lima FO, Furie KL, Silva GS, Lev MH, Camargo ECS, Singhal AB, Harris GJ, Halpern EF, Koroshetz WJ, Smith WS, Yoo AJ, and Nogueira RG. The pattern of leptome-ningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke 41: 2316-2322, 2010.
51. Lin WH, Hao Q, Rosengarten B, Leung WH, and Wong KS. Impaired neurovascular coupling in ischaemic stroke patients with large or small vessel disease. Eur J Neurol 18: 731-736, 2011.
52. Liu J, Jin X, Liu KJ, and Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J Neurosci 32: 3044-3057, 2012.
53. Logothetis NK. What we can do and what we cannot do with fMRI. Nature 453: 869-878, 2008.
54. MacGregor DG, Carswell HV, Graham DI, McCulloch J, and Macrae IM. Impaired cerebral autoregulation 24h after induction of transient unilateral focal ischaemia in the rat. Eur J Neurosci 12: 58-66, 2000.
55. Moskowitz MA, Lo EH, and Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 67: 181-198, 2010.
56. Nguyen J, Nishimura N, Fetcho RN, Iadecola C, and Schaffer CB. Occlusion of cortical ascending venules causes blood flow decreases, reversals in flow direction, and vessel dilation in upstream capillaries. J Cereb Blood Flow Metab 31: 2243-2254, 2011.
57. Nishimura N, Rosidi NL, Iadecola C, and Schaffer CB. Limitations of collateral flow after occlusion of a single cortical penetrating arteriole. J Cereb Blood Flow Metab 30: 1914-1927, 2010.
58. Paulson OB, Strandgaard S, and Edvinsson L. Cerebral autoregulation. Cerebrovasc Brain Metab Rev 2: 161-192, 1990.
59. Pineiro R. Altered hemodynamic responses in patients after subcortical stroke measured by functional MRI. Stroke 33: 103-109, 2002.
60. Pires PW, Dams Ramos CM, Matin N, and Dorrance AM. The effects of hypertension on the cerebral circulation. Am J Physiol 304: H1598-H1614, 2013.
61. Powers WJ, Videen TO, Diringer MN, Aiyagari V, and Zazulia AR. Autoregulation after ischaemic stroke. J Hy-pertens 27: 2218-2222, 2009.
62. Reckelhoff JF. Gender differences in the regulation of blood pressure. Hypertension 37: 1199-1208, 2001.
63. Reinhard M, Rutsch S, Lambeck J, Wihler C, Czosnyka M, Weiller C, and Hetzel A. Dynamic cerebral autoregulation associates with infarct size and outcome after ischemic stroke. Acta Neurol Scand 125: 156-162, 2012.
64. Roehl AB, Zoremba N, Kipp M, Schiefer J, Goetzenich A, Bleilevens C, Kuehn-Velten N, Tolba R, Rossaint R, and Hein M. The effects of levosimendan on brain metabolism during initial recovery from global transient ischaemia/hypoxia. BMC Neurol 12: 81, 2012.
65. Saeed NP, Panerai RB, Horsfield MA, and Robinson TG. Does stroke subtype and measurement technique influence estimation of cerebral autoregulation in acute ischaemic stroke? Cerebrovasc Dis 35: 257-261, 2013.
66. Salinet ASM, Haunton VJ, Panerai RB, and Robinson TG. A systematic review of cerebral hemodynamic responses to neural activation following stroke. J Neurol 260: 2715-2721, 2013.
67. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF, Lyden PD, and Kleinfeld D. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol 4: e22, 2006.
68. Shen Q, Ren H, Cheng H, Fisher M, and Duong TQ. Functional, perfusion and diffusion MRI of acute focal is-chemic brain injury. J Cereb Blood Flow Metab 25: 1265-1279, 2005.
69. Shih AY, Blinder P, Tsai PS, Friedman B, Stanley G, Ly-den PD, and Kleinfeld D. The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat Neurosci 16: 55-63, 2013.
70. Shiokawa O, Sadoshima S, Kusuda K, Nishimura Y, Ibayashi S, and Fujishima M. Cerebral and cerebellar blood flow autoregulations in acutely induced cerebral ischemia in spontaneously hypertensive rats-transtentorial remote effect. Stroke 17: 1309-1313, 1986.
71. Shuaib A, Butcher K, Mohammad AA, Saqqur M, and Liebeskind DS. Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. Lancet Neurol 10: 909-921, 2011.
72. Starr JM, Wardlaw J, Ferguson K, MacLullich A, Deary IJ, and Marshall I. Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. J Neurol Neurosurg Psychiatry 74: 70-76, 2003.
73. Takano T, Tian G-F, Peng W, Lou N, Libionka W, Han X, and Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9: 260-267, 2005.
74. Takata N, Nagai T, Ozawa K, Oe Y, Mikoshiba K, and Hirase H. Cerebral blood flow modulation by basal fore-brain or whisker stimulation can occur independently of large cytosolic Ca2+ signaling in astrocytes. PLoS One 8: e66525, 2013.
75. Tryambake D, He J, Firbank MJ, O'Brien JT, Blamire AM, and Ford GA. Intensive blood pressure lowering increases cerebral blood flow in older subjects with hypertension. Hypertension 61: 1309-1315, 2013.
76. Ueki M, Linn F, and Hossmann KA. Functional activation of cerebral blood flow and metabolism before and after global ischemia of rat brain. J Cereb Blood Flow Metab 8: 486-494, 1988.
77. Vetri F, Xu H, Paisansathan C, and Pelligrino DA. Impairment of neurovascular coupling in type 1 diabetes mellitus in rats is linked to PKC modulation of BK(Ca) and Kir channels. Am J Physiol 302: H1274-H1284, 2012.
78. Wang Z, Ma N, Riley J, Armstead WM, and Liu R. Sal-vinorin A administration after global cerebral hypoxia/ischemia preserves cerebrovascular autoregulation via kappa opioid receptor in piglets. PLoS One 7: e41724, 2012.
79. Yamauchi H, Kudoh T, Sugimoto K, Takahashi M, Kishibe Y, and Okazawa H. Altered patterns of blood flow response during visual stimulation in carotid artery occlusive disease. NeuroImage 25: 554-560, 2005.
80. Yang Y, Estrada EY, Thompson JF, Liu W, and Rosenberg GA. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 27: 697-709, 2007.
81. Yang Y and Rosenberg GA. Blood-brain barrier breakdown in acute and chronic cerebrovascular disease. Stroke 42: 3323-3328, 2011.
82. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201, 2008.
83. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann K-A, Pozzan T, and Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain micro-circulation. Nat Neurosci 6: 43-50, 2002.