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Current Neurovascular Research

Editor-in-Chief

ISSN (Print): 1567-2026
ISSN (Online): 1875-5739

Review Article

The Neurovascular Unit: Focus on the Regulation of Arterial Smooth Muscle Cells

Author(s): Patrícia Quelhas, Graça Baltazar and Elisa Cairrao*

Volume 16, Issue 5, 2019

Page: [502 - 515] Pages: 14

DOI: 10.2174/1567202616666191026122642

Price: $65

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Abstract

The neurovascular unit is a physiological unit present in the brain, which is constituted by elements of the nervous system (neurons and astrocytes) and the vascular system (endothelial and mural cells). This unit is responsible for the homeostasis and regulation of cerebral blood flow. There are two major types of mural cells in the brain, pericytes and smooth muscle cells. At the arterial level, smooth muscle cells are the main components that wrap around the outside of cerebral blood vessels and the major contributors to basal tone maintenance, blood pressure and blood flow distribution. They present several mechanisms by which they regulate both vasodilation and vasoconstriction of cerebral blood vessels and their regulation becomes even more important in situations of injury or pathology. In this review, we discuss the main regulatory mechanisms of brain smooth muscle cells and their contributions to the correct brain homeostasis.

Keywords: Neurovascular unit, smooth muscle cells, cerebral blood flow, vasoconstriction, vasodilatation.

« Previous
[1]
Andreone BJ, Lacoste B, Gu C. Neuronal and vascular interactions. Annu Rev Neurosci 2015; 38: 25-46.
[http://dx.doi.org/10.1146/annurev-neuro-071714-033835] [PMID: 25782970]
[2]
Venkat P, Chopp M, Chen J. New insights into coupling and uncoupling of cerebral blood flow and metabolism in the brain. Croat Med J 2016; 57(3): 223-8.
[http://dx.doi.org/10.3325/cmj.2016.57.223] [PMID: 27374823]
[3]
Itoh Y, Suzuki N. Control of brain capillary blood flow. J Cereb Blood Flow Metab 2012; 32(7): 1167-76.
[http://dx.doi.org/10.1038/jcbfm.2012.5] [PMID: 22293984]
[4]
Jullienne A, Badaut J. Molecular contributions to neurovascular unit dysfunctions after brain injuries: Lessons for target-specific drug development. Future Neurol 2013; 8(6): 677-89.
[http://dx.doi.org/10.2217/fnl.13.55] [PMID: 24489483]
[5]
Muoio V, Persson PB, Sendeski MM. The neurovascular unit - concept review. Acta Physiol (Oxf) 2014; 210(4): 790-8.
[http://dx.doi.org/10.1111/apha.12250] [PMID: 24629161]
[6]
Iadecola C. The neurovascular unit coming of age: A journey through neurovascular coupling in health and disease. Neuron 2017; 96(1): 17-42.
[http://dx.doi.org/10.1016/j.neuron.2017.07.030] [PMID: 28957666]
[7]
Kisler K, Nelson AR, Montagne A, Zlokovic BV. Cerebral blood flow regulation and neurovascular dysfunction in Alzheimer disease. Nat Rev Neurosci 2017; 18(7): 419-34.
[http://dx.doi.org/10.1038/nrn.2017.48] [PMID: 28515434]
[8]
Zhao Z, Nelson AR, Betsholtz C, Zlokovic BV. Establishment and dysfunction of the blood-brain barrier. Cell 2015; 163(5): 1064-78.
[http://dx.doi.org/10.1016/j.cell.2015.10.067] [PMID: 26590417]
[9]
Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014; 508(7494): 55-60.
[http://dx.doi.org/10.1038/nature13165] [PMID: 24670647]
[10]
Lecrux C, Hamel E. Neuronal networks and mediators of cortical neurovascular coupling responses in normal and altered brain states. Philos Trans R Soc Lond B Biol Sci 2016; 371(1705): 371.
[http://dx.doi.org/10.1098/rstb.2015.0350] [PMID: 27574304]
[11]
Yamada K. Vascular potassium channels in NVC.Prog Brain Res. 2016; 225: pp. 63-73.
[http://dx.doi.org/10.1016/bs.pbr.2016.01.001] [PMID: 27130411]
[12]
Mishra A, Reynolds JP, Chen Y, Gourine AV, Rusakov DA, Attwell D. Astrocytes mediate neurovascular signaling to capillary pericytes but not to arterioles. Nat Neurosci 2016; 19(12): 1619-27.
[http://dx.doi.org/10.1038/nn.4428] [PMID: 27775719]
[13]
Mishra A. Binaural blood flow control by astrocytes: Listening to synapses and the vasculature. J Physiol 2017; 595(6): 1885-902.
[PMID: 27619153]
[14]
Liu Z, Chopp M. Astrocytes, therapeutic targets for neuroprotection and neurorestoration in ischemic stroke. Prog Neurobiol 2016; 144: 103-20.
[http://dx.doi.org/10.1016/j.pneurobio.2015.09.008] [PMID: 26455456]
[15]
Filosa JA, Morrison HW, Iddings JA, Du W, Kim KJ. Beyond neurovascular coupling, role of astrocytes in the regulation of vascular tone. Neuroscience 2016; 323: 96-109.
[http://dx.doi.org/10.1016/j.neuroscience.2015.03.064] [PMID: 25843438]
[16]
Nuriya M, Hirase H. Involvement of astrocytes in neurovascular communication.Prog Brain Res. 2016; 225: pp. 41-62.
[http://dx.doi.org/10.1016/bs.pbr.2016.02.001] [PMID: 27130410]
[17]
Calcinaghi N, Jolivet R, Wyss MT, et al. Metabotropic glutamate receptor mGluR5 is not involved in the early hemodynamic response. J Cereb Blood Flow Metab 2011; 31(9): e1-e10.
[http://dx.doi.org/10.1038/jcbfm.2011.96] [PMID: 21731033]
[18]
Martindale J, Berwick J, Martin C, Kong Y, Zheng Y, Mayhew J. Long duration stimuli and nonlinearities in the neural-haemodynamic coupling. J Cereb Blood Flow Metab 2005; 25(5): 651-61.
[http://dx.doi.org/10.1038/sj.jcbfm.9600060] [PMID: 15703699]
[19]
Rosenegger DG, Gordon GR. A slow or modulatory role of astrocytes in neurovascular coupling. Microcirculation 2015; 22(3): 197-203.
[http://dx.doi.org/10.1111/micc.12184] [PMID: 25556627]
[20]
Gebremedhin D, Lange AR, Lowry TF, et al. Production of 20-HETE and its role in autoregulation of cerebral blood flow. Circ Res 2000; 87(1): 60-5.
[http://dx.doi.org/10.1161/01.RES.87.1.60] [PMID: 10884373]
[21]
Mulligan SJ, MacVicar BA. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 2004; 431(7005): 195-9.
[http://dx.doi.org/10.1038/nature02827] [PMID: 15356633]
[22]
Roman RJ. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 2002; 82(1): 131-85.
[http://dx.doi.org/10.1152/physrev.00021.2001] [PMID: 11773611]
[23]
Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature 2010; 468(7321): 232-43.
[http://dx.doi.org/10.1038/nature09613] [PMID: 21068832]
[24]
Badaut J, Bix GJ. Vascular neural network phenotypic transformation after traumatic injury: Potential role in long-term sequelae. Transl Stroke Res 2014; 5(3): 394-406.
[http://dx.doi.org/10.1007/s12975-013-0304-z] [PMID: 24323723]
[25]
Thomsen MS, Routhe LJ, Moos T. The vascular basement membrane in the healthy and pathological brain. J Cereb Blood Flow Metab 2017; 37(10): 3300-17.
[http://dx.doi.org/10.1177/0271678X17722436] [PMID: 28753105]
[26]
Weksler BB, Subileau EA, Perrière N, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 2005; 19(13): 1872-4.
[http://dx.doi.org/10.1096/fj.04-3458fje] [PMID: 16141364]
[27]
Sweeney MD, Zhao Z, Montagne A, Nelson AR, Zlokovic BV. Blood-brain barrier: From physiology to disease and back. Physiol Rev 2019; 99(1): 21-78.
[http://dx.doi.org/10.1152/physrev.00050.2017] [PMID: 30280653]
[28]
Loscher W, Potschka H. Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2005; 2(1): 86-98.https://www.ncbi.nlm.nih.gov/pubmed/15717060
[PMID: 5717060]
[29]
Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol 2015; 7(1) a020412
[http://dx.doi.org/10.1101/cshperspect.a020412] [PMID: 25561720]
[30]
Mittapalli RK, Manda VK, Adkins CE, Geldenhuys WJ, Lockman PR. Exploiting nutrient transporters at the blood-brain barrier to improve brain distribution of small molecules. Ther Deliv 2010; 1(6): 775-84.
[http://dx.doi.org/10.4155/tde.10.76] [PMID: 22834013]
[31]
Ufnal M, Skrzypecki J. Blood borne hormones in a cross-talk between peripheral and brain mechanisms regulating blood pressure, the role of circumventricular organs. Neuropeptides 2014; 48(2): 65-73.
[http://dx.doi.org/10.1016/j.npep.2014.01.003] [PMID: 24485840]
[32]
Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 2007; 100(2): 158-73.
[http://dx.doi.org/10.1161/01.RES.0000255691.76142.4a] [PMID: 17272818]
[33]
Duchemin S, Boily M, Sadekova N, Girouard H. The complex contribution of NOS interneurons in the physiology of cerebrovascular regulation. Front Neural Circuits 2012; 6: 51.
[http://dx.doi.org/10.3389/fncir.2012.00051] [PMID: 22907993]
[34]
Macarthur H, Wilken GH, Westfall TC, Kolo LL. Neuronal and non-neuronal modulation of sympathetic neurovascular transmission. Acta Physiol (Oxf) 2011; 203(1): 37-45.
[http://dx.doi.org/10.1111/j.1748-1716.2010.02242.x] [PMID: 21362154]
[35]
Hongjin W, Han C, Baoxiang J, Shiqi Y, Xiaoyu X. Reconstituting neurovascular unit based on the close relations between neural stem cells and endothelial cells: An effective method to explore neurogenesis and angiogenesis. Rev Neurosci 2019. [Epub ahead of print]
[http://dx.doi.org/10.1515/revneuro-2019-0023] [PMID: 31539363]
[36]
Özen I, Roth M, Barbariga M, et al. Loss of regulator of G-protein signaling 5 leads to neurovascular protection in stroke. Stroke 2018; 49(9): 2182-90.
[http://dx.doi.org/10.1161/STROKEAHA.118.020124] [PMID: 30354999]
[37]
Iadecola C, Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci 2007; 10(11): 1369-76.
[http://dx.doi.org/10.1038/nn2003] [PMID: 17965657]
[38]
MacVicar BA, Newman EA. Astrocyte regulation of blood flow in the brain. Cold Spring Harb Perspect Biol 2015; 7(5) a020388
[http://dx.doi.org/10.1101/cshperspect.a020388] [PMID: 25818565]
[39]
Hamilton NB, Attwell D, Hall CN. Pericyte-mediated regulation of capillary diameter: A component of neurovascular coupling in health and disease. Front Neuroenerget 2010; 2: 2.
[http://dx.doi.org/10.3389/fnene.2010.00005] [PMID: 20725515]
[40]
Hill RA, Tong L, Yuan P, Murikinati S, Gupta S, Grutzendler J. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron 2015; 87(1): 95-110.
[http://dx.doi.org/10.1016/j.neuron.2015.06.001] [PMID: 26119027]
[41]
Chasseigneaux S, Moraca Y, Cochois-Guégan V, et al. Isolation and differential transcriptome of vascular smooth muscle cells and mid-capillary pericytes from the rat brain. Sci Rep 2018; 8(1): 12272.
[http://dx.doi.org/10.1038/s41598-018-30739-5] [PMID: 30116021]
[42]
Eilken HM, Diéguez-Hurtado R, Schmidt I, et al. Pericytes regulate VEGF-induced endothelial sprouting through VEGFR1. Nat Commun 2017; 8(1): 1574.
[http://dx.doi.org/10.1038/s41467-017-01738-3] [PMID: 29146905]
[43]
Sweeney MD, Kisler K, Montagne A, Toga AW, Zlokovic BV. The role of brain vasculature in neurodegenerative disorders. Nat Neurosci 2018; 21(10): 1318-31.
[http://dx.doi.org/10.1038/s41593-018-0234-x] [PMID: 30250261]
[44]
Wagenseil JE, Mecham RP. Vascular extracellular matrix and arterial mechanics. Physiol Rev 2009; 89(3): 957-89.
[http://dx.doi.org/10.1152/physrev.00041.2008] [PMID: 19584318]
[45]
Alexander MR, Owens GK. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol 2012; 74: 13-40.
[http://dx.doi.org/10.1146/annurev-physiol-012110-142315] [PMID: 22017177]
[46]
Owens GK. Molecular control of vascular smooth muscle cell differentiation and phenotypic plasticity. Novartis Found Symp 2007; 283: 174-91.
[http://dx.doi.org/10.1002/9780470319413.ch14]
[47]
Uranishi R, Baev NI, Kim JH, Awad IA. Vascular smooth muscle cell differentiation in human cerebral vascular malformations. Neurosurgery 2001; 49(3): 671-9.
[PMID: 11523679]
[48]
Wu J, Zhang Y, Yang P, et al. Recombinant osteopontin stabilizes smooth muscle cell phenotype via integrin receptor/integrin-linked kinase/Rac-1 pathway after subarachnoid hemorrhage in rats. Stroke 2016; 47(5): 1319-27.
[http://dx.doi.org/10.1161/STROKEAHA.115.011552] [PMID: 27006454]
[49]
Edvinsson LI, Povlsen GK. Vascular plasticity in cerebrovascular disorders. J Cereb Blood Flow Metab 2011; 31(7): 1554-71.
[http://dx.doi.org/10.1038/jcbfm.2011.70] [PMID: 21559027]
[50]
Rensen SS, Doevendans PA, van Eys GJ. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J 2007; 15(3): 100-8.
[http://dx.doi.org/10.1007/BF03085963] [PMID: 17612668]
[51]
Cairrão E, Santos-Silva AJ, Alvarez E, Correia I, Verde I. Isolation and culture of human umbilical artery smooth muscle cells expressing functional calcium channels. In Vitro Cell Dev Biol Anim 2009; 45(3-4): 175-84.
[http://dx.doi.org/10.1007/s11626-008-9161-6] [PMID: 19118440]
[52]
Han DH, Bai GY, Yang TK, Sim BS, Kwak YG, Kim CJ. The effect of papaverine on ion channels in rat basilar smooth muscle cells. Neurol Res 2007; 29(6): 544-50.
[http://dx.doi.org/10.1179/016164107X191021] [PMID: 17535590]
[53]
Contard F, Sabri A, Glukhova M, et al. Arterial smooth muscle cell phenotype in stroke-prone spontaneously hypertensive rats. Hypertension 1993; 22(5): 665-76.
[http://dx.doi.org/10.1161/01.HYP.22.5.665] [PMID: 8225526]
[54]
Hubbell MC, Semotiuk AJ, Thorpe RB, et al. Chronic hypoxia and VEGF differentially modulate abundance and organization of myosin heavy chain isoforms in fetal and adult ovine arteries. Am J Physiol Cell Physiol 2012; 303(10): C1090-103.
[http://dx.doi.org/10.1152/ajpcell.00408.2011] [PMID: 22992677]
[55]
Oishi K, Ogawa Y, Gamoh S, Uchida MK. Contractile responses of smooth muscle cells differentiated from rat neural stem cells. J Physiol 2002; 540(Pt 1): 139-52.
[http://dx.doi.org/10.1113/jphysiol.2001.013278] [PMID: 11927676]
[56]
Yang J, Clark JW Jr, Bryan RM, Robertson C. The myogenic response in isolated rat cerebrovascular arteries: Smooth muscle cell model. Med Eng Phys 2003; 25(8): 691-709.
[http://dx.doi.org/10.1016/S1350-4533(03)00100-0] [PMID: 12900184]
[57]
Wong AY, Klassen GA. A model of calcium regulation in smooth muscle cell. Cell Calcium 1993; 14(3): 227-43.
[http://dx.doi.org/10.1016/0143-4160(93)90070-M] [PMID: 8388778]
[58]
Brenner R, Peréz GJ, Bonev AD, et al. Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 2000; 407(6806): 870-6.
[http://dx.doi.org/10.1038/35038011] [PMID: 11057658]
[59]
Armstead WM, Raghupathi R. Endothelin and the neurovascular unit in pediatric traumatic brain injury. Neurol Res 2011; 33(2): 127-32.
[http://dx.doi.org/10.1179/016164111X12881719352138] [PMID: 21801587]
[60]
Tao XG, Shi JH, Hao SY, Chen XT, Liu BY. Protective effects of calpain inhibition on neurovascular unit injury through downregulating nuclear factor-κB-related inflammation during traumatic brain injury in mice. Chin Med J (Engl) 2017; 130(2): 187-98.
[PMID: 28091411]
[61]
Badaut J, Ajao DO, Sorensen DW, Fukuda AM, Pellerin L. Caveolin expression changes in the neurovascular unit after juvenile traumatic brain injury: Signs of blood-brain barrier healing? Neuroscience 2015; 285: 215-26.
[http://dx.doi.org/10.1016/j.neuroscience.2014.10.035] [PMID: 25450954]
[62]
Ahmad A, Crupi R, Campolo M, Genovese T, Esposito E, Cuzzocrea S. Absence of TLR4 reduces neurovascular unit and secondary inflammatory process after traumatic brain injury in mice. PLoS One 2013; 8(3) e57208
[http://dx.doi.org/10.1371/journal.pone.0057208] [PMID: 23555560]
[63]
Wang R, Zhang X, Zhang J, et al. Oxygen-glucose deprivation induced glial scar-like change in astrocytes. PLoS One 2012; 7(5) e37574
[http://dx.doi.org/10.1371/journal.pone.0037574] [PMID: 22629422]
[64]
Ishikawa M, Kajimura M, Morikawa T, et al. Cortical microcirculatory disturbance in the super acute phase of subarachnoid hemorrhage - In vivo analysis using two-photon laser scanning microscopy. J Neurol Sci 2016; 368: 326-33.
[http://dx.doi.org/10.1016/j.jns.2016.06.067] [PMID: 27538658]
[65]
Tso MK, Macdonald RL. Subarachnoid hemorrhage: A review of experimental studies on the microcirculation and the neurovascular unit. Transl Stroke Res 2014; 5(2): 174-89.
[http://dx.doi.org/10.1007/s12975-014-032 3-4] [PMID: 24510780]
[66]
Wang Y, Reis C, Applegate RII, Stier G, Martin R, Zhang JH. Ischemic conditioning-induced endogenous brain protection: Applications pre-, per- or post-stroke. Exp Neurol 2015; 272: 26-40.
[http://dx.doi.org/10.1016/j.expneurol.2015.04.009] [PMID: 25900056]
[67]
Zhang Z, Zhang L, Chen J, et al. 2-(2-Benzofuranyl)-2-Imidazoline mediates neuroprotection by regulating the neurovascular unit integrity in a rat model of focal cerebral ischemia. J Stroke Cerebrovasc Dis 2018; 27(6): 1481-9.
[68]
Bastide M, Ouk T, Plaisier F, Pétrault O, Stolc S, Bordet R. Neurogliovascular unit after cerebral ischemia: Is the vascular wall a pharmacological target. Psychoneuroendocrinology 2007; 32(Suppl. 1): S36-9.
[http://dx.doi.org/10.1016/j.psyneuen.2007.03.015] [PMID: 17628344]
[69]
Toth P, Tarantini S, Csiszar A, Ungvari Z. Functional vascular contributions to cognitive impairment and dementia: Mechanisms and consequences of cerebral autoregulatory dysfunction, endothelial impairment, and neurovascular uncoupling in aging. Am J Physiol Heart Circ Physiol 2017; 312(1): H1-H20.
[http://dx.doi.org/10.1152/ajpheart.00581.2016] [PMID: 27793855]
[70]
Mandel S, Amit T, Bar-Am O, Youdim MB. Iron dysregulation in Alzheimer’s disease: Multimodal brain permeable iron chelating drugs, possessing neuroprotective-neurorescue and amyloid precursor protein-processing regulatory activities as therapeutic agents. Prog Neurobiol 2007; 82(6): 348-60.
[http://dx.doi.org/10.1016/j.pneurobio.2007.06.001] [PMID: 17659826]
[71]
Busch S, Wu L, Feng Y, Gretz N, Hoffmann S, Hammes HP. Alzheimer’s disease and retinal neurodegeneration share a consistent stress response of the neurovascular unit. Cell Physiol Biochem 2012; 30(6): 1436-43.
[72]
Montagne A, Zhao Z, Zlokovic BV. Alzheimer’s disease: A matter of blood-brain barrier dysfunction? J Exp Med 2017; 214(11): 3151-69.
[http://dx.doi.org/10.1084/jem.20171406] [PMID: 29061693]
[73]
Nag S, Venugopalan R, Stewart DJ. Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during blood-brain barrier breakdown. Acta Neuropathol 2007; 114(5): 459-69.
[http://dx.doi.org/10.1007/s00401-007-0274-x] [PMID: 17687559]
[74]
Keaney J, Campbell M. The dynamic blood-brain barrier. FEBS J 2015; 282(21): 4067-79.
[http://dx.doi.org/10.1111/febs.13412] [PMID: 26277326]
[75]
Stamatovic SM, Phillips CM, Martinez-Revollar G, Keep RF, Andjelkovic AV. Involvement of epigenetic mechanisms and non-coding RNAs in blood-brain barrier and neurovascular unit injury and recovery after stroke. Front Neurosci 2019; 13: 864.
[http://dx.doi.org/10.3389/fnins.2019.00864] [PMID: 31543756]
[76]
Yu GX, Mueller M, Hawkins BE, et al. Traumatic brain injury in vivo and in vitro contributes to cerebral vascular dysfunction through impaired gap junction communication between vascular smooth muscle cells. J Neurotrauma 2014; 31(8): 739-48.
[http://dx.doi.org/10.1089/neu.2013.3187] [PMID: 24341563]
[77]
Duffin J, Sobczyk O, McKetton L, et al. Cerebrovascular resistance: The basis of cerebrovascular reactivity. Front Neurosci 2018; 12: 409.
[http://dx.doi.org/10.3389/fnins.2018.00409] [PMID: 29973862]
[78]
Purkayastha S, Raven PB. The functional role of the alpha-1 adrenergic receptors in cerebral blood flow regulation. Indian J Pharmacol 2011; 43(5): 502-6.
[http://dx.doi.org/10.4103/0253-7613.84950] [PMID: 22021989]
[79]
Davis MJ, Hill MA. Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 1999; 79(2): 387-423.
[http://dx.doi.org/10.1152/physrev.1999.79.2.387] [PMID: 10221985]
[80]
Longden TA, Hill-Eubanks DC, Nelson MT. Ion channel networks in the control of cerebral blood flow. J Cereb Blood Flow Metab 2016; 36(3): 492-512.
[http://dx.doi.org/10.1177/0271678X15616138] [PMID: 26661232]
[81]
Brayden JE, Li Y, Tavares MJ. Purinergic receptors regulate myogenic tone in cerebral parenchymal arterioles. J Cereb Blood Flow Metab 2013; 33(2): 293-9.
[http://dx.doi.org/10.1038/jcbfm.2012.169] [PMID: 23168530]
[82]
Liu Y, Harder DR, Lombard JH. Interaction of myogenic mechanisms and hypoxic dilation in rat middle cerebral arteries. Am J Physiol Heart Circ Physiol 2002; 283(6): H2276-81.
[http://dx.doi.org/10.1152/ajpheart.00635.2002] [PMID: 12388266]
[83]
Gonzales AL, Earley S. Regulation of cerebral artery smooth muscle membrane potential by Ca2+-activated cation channels. Microcirculation 2013; 20(4): 337-47.
[http://dx.doi.org/10.1111/micc.12023] [PMID: 23116477]
[84]
Grayson TH, Murphy TV, Sandow SL. Transient receptor potential canonical type 3 channels: Interactions, role and relevance - A vascular focus. Pharmacol Ther 2017; 174: 79-96.
[http://dx.doi.org/10.1016/j.pharmthera.2017.02.022] [PMID: 28223224]
[85]
Brayden JE, Earley S, Nelson MT, Reading S. Transient receptor potential (TRP) channels, vascular tone and autoregulation of cerebral blood flow. Clin Exp Pharmacol Physiol 2008; 35(9): 1116-20.
[http://dx.doi.org/10.1111/j.1440-1681.2007.04855.x] [PMID: 18215190]
[86]
Earley S. TRPM4 channels in smooth muscle function. Pflugers Arch 2013; 465(9): 1223-31.
[http://dx.doi.org/10.1007/s00424-013-1250-z] [PMID: 23443854]
[87]
Earley S, Waldron BJ, Brayden JE. Critical role for transient receptor potential channel TRPM4 in myogenic constriction of cerebral arteries. Circ Res 2004; 95(9): 922-9.
[http://dx.doi.org/10.1161/01.RES.0000147311.54833.03] [PMID: 15472118]
[88]
Reading SA, Brayden JE. Central role of TRPM4 channels in cerebral blood flow regulation. Stroke 2007; 38(8): 2322-8.
[http://dx.doi.org/10.1161/STROKEAHA.107.483404] [PMID: 17585083]
[89]
Earley S, Brayden JE. Transient receptor potential channels in the vasculature. Physiol Rev 2015; 95(2): 645-90.
[http://dx.doi.org/10.1152/physrev.00026.2014] [PMID: 25834234]
[90]
Nilius B, Mahieu F, Prenen J, et al. The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 2006; 25(3): 467-78.
[http://dx.doi.org/10.1038/sj.emboj.7600963] [PMID: 16424899]
[91]
Nilius B, Prenen J, Janssens A, Voets T, Droogmans G. Decavanadate modulates gating of TRPM4 cation channels. J Physiol 2004; 560(Pt 3): 753-65.
[http://dx.doi.org/10.1113/jphysiol.2004.070839] [PMID: 15331675]
[92]
Nilius B, Prenen J, Tang J, et al. Regulation of the Ca2+ sensitivity of the nonselective cation channel TRPM4. J Biol Chem 2005; 280(8): 6423-33.
[http://dx.doi.org/10.1074/jbc.M411089200] [PMID: 15590641]
[93]
Gonzales AL, Amberg GC, Earley S. Ca2+ release from the sarcoplasmic reticulum is required for sustained TRPM4 activity in cerebral artery smooth muscle cells. Am J Physiol Cell Physiol 2010; 299(2): C279-88.
[http://dx.doi.org/10.1152/ajpcell.00550.2009] [PMID: 20427713]
[94]
Bannister JP, Adebiyi A, Zhao G, et al. Smooth muscle cell alpha2delta-1 subunits are essential for vasoregulation by CaV1.2 channels. Circ Res 2009; 105(10): 948-55.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.203620] [PMID: 19797702]
[95]
Harraz OF, Abd El-Rahman RR, Bigdely-Shamloo K, et al. Ca(V)3.2 channels and the induction of negative feedback in cerebral arteries. Circ Res 2014; 115(7): 650-61.
[http://dx.doi.org/10.1161/CIRCRESAHA.114.304056] [PMID: 25085940]
[96]
Narayanan D, Bulley S, Leo MD, et al. Smooth muscle cell transient receptor potential polycystin-2 (TRPP2) channels contribute to the myogenic response in cerebral arteries. J Physiol 2013; 591(20): 5031-46.
[http://dx.doi.org/10.1113/jphysiol.2013.258319] [PMID: 23858011]
[97]
Knot HJ, Nelson MT. Regulation of arterial diameter and wall [Ca2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol 1998; 508(Pt 1): 199-209.
[http://dx.doi.org/10.1111/j.1469-7793.1998.199br.x] [PMID: 9490839]
[98]
Ureña J, Fernández-Tenorio M, Porras-González C, González-Rodríguez P, Castellano A, López-Barneo J. A new metabotropic role for L-type Ca(2+) channels in vascular smooth muscle contraction. Curr Vasc Pharmacol 2013; 11(4): 490-6.
[http://dx.doi.org/10.2174/1570161111311040012] [PMID: 23905643]
[99]
Longo LD, Goyal R. Cerebral artery signal transduction mechanisms: Developmental changes in dynamics and Ca2+ sensitivity. Curr Vasc Pharmacol 2013; 11(5): 655-711.
[http://dx.doi.org/10.2174/1570161111311050008] [PMID: 24063382]
[100]
Piascik MT, Perez DM. Alpha1-adrenergic receptors: New insights and directions. J Pharmacol Exp Ther 2001; 298(2): 403-10.
[PMID: 11454900]
[101]
Pearce WJ, Williams JM, White CR, Lincoln TM. Effects of chronic hypoxia on soluble guanylate cyclase activity in fetal and adult ovine cerebral arteries 2009; 107(1): 192-9.
[http://dx.doi.org/ 10.1152/japplphysiol.00233.2009]
[102]
Dabertrand F, Nelson MT, Brayden JE. Ryanodine receptors, calcium signaling, and regulation of vascular tone in the cerebral parenchymal microcirculation. Microcirculation 2013; 20(4): 307-16.
[http://dx.doi.org/10.1111/micc.12027] [PMID: 23216877]
[103]
Straub SV, Bonev AD, Wilkerson MK, Nelson MT. Dynamic inositol trisphosphate-mediated calcium signals within astrocytic endfeet underlie vasodilation of cerebral arterioles. J Gen Physiol 2006; 128(6): 659-69.
[http://dx.doi.org/10.1085/jgp.200609650] [PMID: 17130519]
[104]
Girouard H, Bonev AD, Hannah RM, Meredith A, Aldrich RW, Nelson MT. Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 2010; 107(8): 3811-6.
[http://dx.doi.org/10.1073/pnas.0914722107] [PMID: 20133576]
[105]
Takano T, Tian GF, Peng W, et al. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 2006; 9(2): 260-7.
[http://dx.doi.org/10.1038/nn1623] [PMID: 16388306]
[106]
Zhao G, Neeb ZP, Leo MD, et al. Type 1 IP3 receptors activate BKCa channels via local molecular coupling in arterial smooth muscle cells. J Gen Physiol 2010; 136(3): 283-91.
[http://dx.doi.org/10.1085/jgp.201010453] [PMID: 20713546]
[107]
Jadhav V, Jabre A, Lin SZ, Lee TJ. EP1- and EP3-receptors mediate prostaglandin E2-induced constriction of porcine large cerebral arteries. J Cereb Blood Flow Metab 2004; 24(12): 1305-16.
[http://dx.doi.org/10.1097/01.WCB.0000139446.61789.14] [PMID: 15625406]
[108]
Rivera-Lara L, Zorrilla-Vaca A, Geocadin RG, Healy RJ, Ziai W, Mirski MA. Cerebral autoregulation-oriented therapy at the bedside: A comprehensive review. Anesthesiology 2017; 126(6): 1187-99.
[http://dx.doi.org/10.1097/ALN.0000000000001625] [PMID: 28383324]
[109]
Ansar S, Eftekhari S, Waldsee R, et al. MAPK signaling pathway regulates cerebrovascular receptor expression in human cerebral arteries. BMC Neurosci 2013; 14: 12.
[http://dx.doi.org/10.1186/1471-2202-14-12] [PMID: 23343134]
[110]
Irving EA, Bamford M. Role of mitogen- and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab 2002; 22(6): 631-47.
[http://dx.doi.org/10.1097/00004647-200206000-00001] [PMID: 12045661]
[111]
Zhou J, Du T, Li B, Rong Y, Verkhratsky A, Peng L. Crosstalk between MAPK/ERK and PI3K/AKT signal pathways during brain ischemia/reperfusion. ASN Neuro 2015; 7(5)1759091415602463
[112]
Chen TT, Luykenaar KD, Walsh EJ, Walsh MP, Cole WC. Key role of Kv1 channels in vasoregulation. Circ Res 2006; 99(1): 53-60.
[http://dx.doi.org/10.1161/01.RES.0000229654.45090.57] [PMID: 16741158]
[113]
Dunn KM, Nelson MT. Potassium channels and neurovascular coupling. Circ J 2010; 74(4): 608-16.
[http://dx.doi.org/10.1253/circj.CJ-10-0174] [PMID: 20234102]
[114]
Haddy FJ, Vanhoutte PM, Feletou M. Role of potassium in regulating blood flow and blood pressure. Am J Physiol Regul Integr Comp Physiol 2006; 290(3): R546-52.
[http://dx.doi.org/10.1152/ajpregu.00491.2005] [PMID: 16467502]
[115]
Rubaiy HN. The therapeutic agents that target ATP-sensitive potassium channels. Acta Pharm 2016; 66(1): 23-34.
[http://dx.doi.org/10.1515/acph-2016-0006] [PMID: 27029082]
[116]
Longden TA, Nelson MT. Vascular inward rectifier K+ channels as external K+ sensors in the control of cerebral blood flow. Microcirculation 2015; 22(3): 183-96.
[http://dx.doi.org/10.1111/micc.12190] [PMID: 25641345]
[117]
Rodrigo GC, Standen NB. ATP-sensitive potassium channels. Curr Pharm Des 2005; 11(15): 1915-40.
[http://dx.doi.org/10.2174/1381612054021015] [PMID: 15974968]
[118]
Crecelius AR, Richards JC, Luckasen GJ, Larson DG, Dinenno FA. Reactive hyperemia occurs via activation of inwardly rectifying potassium channels and Na+/K+-ATPase in humans. Circ Res 2013; 113(8): 1023-32.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.301675] [PMID: 23940309]
[119]
Arabian M, Aboutaleb N, Soleimani M, Ajami M, Habibey R, Pazoki-Toroudi H. Activation of mitochondrial KATP channels mediates neuroprotection induced by chronic morphine preconditioning in hippocampal CA-1 neurons following cerebral ischemia. Adv Med Sci 2018; 63(2): 213-9.
[http://dx.doi.org/10.1016/j.advms.2017.11.003] [PMID: 29223124]
[120]
Tano JY, Gollasch M. Calcium-activated potassium channels in ischemia reperfusion: A brief update. Front Physiol 2014; 5: 381.
[http://dx.doi.org/10.3389/fphys.2014.00381] [PMID: 25339909]
[121]
Howitt L, Sandow SL, Grayson TH, Ellis ZE, Morris MJ, Murphy TV. Differential effects of diet-induced obesity on BKCa beta1-subunit expression and function in rat skeletal muscle arterioles and small cerebral arteries. Am J Physiol Heart Circ Physiol 2011; 301(1): H29-40.
[http://dx.doi.org/10.1152/ajpheart.00134.2011] [PMID: 21536854]
[122]
Singh H, Lu R, Bopassa JC, Meredith AL, Stefani E, Toro L. mitoBKCa is encoded by the Kcnma1 gene, and a splicing sequence defines its mitochondrial location. Proceedings of the National Academy of Sciences of the United States of America. 10836-41.
[http://dx.doi.org/10.1073/pnas.1302028110]
[123]
Liao Y, Kristiansen AM, Oksvold CP, et al. Neuronal Ca2+-activated K+ channels limit brain infarction and promote survival. PLoS One 2010; 5(12) e15601
[http://dx.doi.org/10.1073/pnas.1302028110]
[124]
Chen YJ, Raman G, Bodendiek S, O’Donnell ME, Wulff H. The KCa3.1 blocker TRAM-34 reduces infarction and neurological deficit in a rat model of ischemia/reperfusion stroke. J Cereb Blood Flow Metab 2011; 31(12): 2363-74.
[http://dx.doi.org/10.1038/jcbfm.2011.101] [PMID: 21750563]
[125]
Su F, Guo AC, Li WW, et al. Low-dose ethanol preconditioning protects against oxygen-glucose deprivation/reoxygenation-induced neuronal injury by activating large conductance, Ca2+-activated K+ channels in vitro. Neurosci Bull 2017; 33(1): 28-40.
[http://dx.doi.org/10.1007/s12264-016-0080-3] [PMID: 27854008]
[126]
Sakai Y, Sokolowski B. The large conductance calcium-activated potassium channel affects extrinsic and intrinsic mechanisms of apoptosis. J Neurosci Res 2015; 93(5): 745-54.
[http://dx.doi.org/10.1002/jnr.23538] [PMID: 25581503]
[127]
Szarka N, Pabbidi MR, Amrein K, et al. Traumatic brain injury impairs myogenic constriction of cerebral arteries: Role of mitochondria-derived H2O2 and TRPV4-dependent activation of BKca Channels. J Neurotrauma 2018. [Epub ahead of print]
[http://dx.doi.org/10.1089/neu.2017.5056] [PMID: 29179622]
[128]
Aleksandrowicz M, Dworakowska B, Dolowy K, Kozniewska E. Restoration of the response of the middle cerebral artery of the rat to acidosis in hyposmotic hyponatremia by the opener of large-conductance calcium sensitive potassium channels (BKCa). J Cereb Blood Flow Metab 2017; 37(9): 3219-30.
[http://dx.doi.org/10.1177/0271678X16685575] [PMID: 28058990]
[129]
Amberg GC, Santana LF. Kv2 channels oppose myogenic constriction of rat cerebral arteries. Am J Physiol Cell Physiol 2006; 291(2): C348-56.
[http://dx.doi.org/10.1152/ajpcell.00086.2006] [PMID: 16571867]
[130]
Liu W, Wang D, Song K, et al. Inhibition of 15-lipoxygenase (15-LOX) reverses hypoxia-induced down-regulation of potassium channels Kv1.5 and Kv2.1Inhibition of 15-lipoxygenase (15-LOX) reverses hypoxia-induced down-regulation of potassium channels Kv1.5 and Kv2.1. Int J Clin Exp Med 2014; 7(11): 4147-53.
[PMID: 25550925]
[131]
Ishiguro M, Murakami K, Link T, et al. Acute and chronic effects of oxyhemoglobin on voltage-dependent ion channels in cerebral arteries 2008; 104: 99-102.
[http://dx.doi.org/ 10.1007/978-3-211-75718-5_19]
[132]
Sepúlveda FV, Pablo Cid L, Teulon J, Niemeyer MI. Molecular aspects of structure, gating, and physiology of pH-sensitive background K2P and Kir K+-transport channels. Physiol Rev 2015; 95(1): 179-217.
[http://dx.doi.org/10.1152/physrev.00016.2014] [PMID: 25540142]
[133]
Borsotto M, Veyssiere J, Moha Ou Maati H, Devader C, Mazella J, Heurteaux C. Targeting two-pore domain K(+) channels TREK-1 and TASK-3 for the treatment of depression: A new therapeutic concept. Br J Pharmacol 2015; 172(3): 771-84.
[http://dx.doi.org/10.1111/bph.12953] [PMID: 25263033]
[134]
Sanders KM, Koh SD. Two-pore-domain potassium channels in smooth muscles: new components of myogenic regulation. J Physiol 2006; 570(Pt 1): 37-43.
[http://dx.doi.org/10.1113/jphysiol.2005.098897] [PMID: 16239268]
[135]
Bittner S, Budde T, Wiendl H, Meuth SG. From the background to the spotlight: TASK channels in pathological conditions. Brain Pathol 2010; 20(6): 999-1009.
[http://dx.doi.org/10.1111/j.1750-3639.2010.00407.x] [PMID: 20529081]
[136]
Lei Q, Pan XQ, Chang S, Malkowicz SB, Guzzo TJ, Malykhina AP. Response of the human detrusor to stretch is regulated by TREK-1, a two-pore-domain (K2P) mechano-gated potassium channel. J Physiol 2014; 592(14): 3013-30.
[http://dx.doi.org/10.1113/jphysiol.2014.271718] [PMID: 24801307]
[137]
Enyedi P, Czirják G. Molecular background of leak K+ currents: Two-pore domain potassium channels. Physiol Rev 2010; 90(2): 559-605.
[http://dx.doi.org/10.1152/physrev.00029.2009] [PMID: 20393194]
[138]
Filosa JA, Yao X, Rath G. TRPV4 and the regulation of vascular tone. J Cardiovasc Pharmacol 2013; 61(2): 113-9.
[http://dx.doi.org/10.1097/FJC.0b013e318279ba42] [PMID: 23107877]
[139]
Earley S, Heppner TJ, Nelson MT, Brayden JE. TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 2005; 97(12): 1270-9.
[http://dx.doi.org/10.1161/01.RES.0000194321.60300.d6] [PMID: 16269659]
[140]
Essin K, Gollasch M. Role of ryanodine receptor subtypes in initiation and formation of calcium sparks in arterial smooth muscle: Comparison with striated muscle. J Biomed Biotechnol 2009; 2009 135249
[141]
Gebremedhin D, Zhang DX, Weihrauch D, Uche NN, Harder DR. Detection of TRPV4 channel current-like activity in Fawn Hooded hypertensive (FHH) rat cerebral arterial muscle cells. PLoS One 2017; 12(5) e0176796
[142]
Mercado J, Baylie R, Navedo MF, et al. Local control of TRPV4 channels by AKAP150-targeted PKC in arterial smooth muscle. J Gen Physiol 2014; 143(5): 559-75.
[http://dx.doi.org/10.1085/jgp.201311050] [PMID: 24778429]

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