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Calcium Signaling at the Blood–Brain Barrier in Stroke

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Metal Ion in Stroke

Part of the book series: Springer Series in Translational Stroke Research ((SSTSR))

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Abstract

The blood–brain barrier (BBB) is a critical player in the regulation of the brain’s microenvironment. In a number of pathological disease states, including Alzheimer’s disease, multiple sclerosis, and stroke, this barrier is disrupted, allowing free diffusion of molecules and water into the brain parenchyma. In stroke, the BBB loosens, and ions freely diffuse across the walls of the brain capillaries into the central nervous system. This is followed by passive movement of water, leading to edema formation which contributes to neuronal damage. Disruption of the BBB has been linked to a number of mechanisms, including increases in intracellular calcium and activation of calcium-sensitive signaling cascades. This review outlines some potential routes for hypoxia-stimulated calcium influx and explores some of the calcium signaling cascades and subsequent molecular events that have been linked to BBB disruption.

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References

  • Aaronson PI (2006) TRPC Channel upregulation in chronically hypoxic pulmonary arteries: the HIF-1 bandwagon gathers steam. Circ Res 98(12):1465–1467

    PubMed  CAS  Google Scholar 

  • Aarts MM, Tymianski M (2005) TRPM7 and ischemic CNS injury. Neuroscientist 11(2):116–123

    PubMed  CAS  Google Scholar 

  • Abbott JN (2000) Inflammatory mediators and modulation of the blood-brain barrier permeability. Cell Mol Neurobiol 20(2):131–147

    PubMed  CAS  Google Scholar 

  • Abbott NJ (2005) Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 25(1):5–23

    PubMed  Google Scholar 

  • Abbott NJ, Revest PA (1991) Control of brain endothelial permeability. Cerebrovasc Brain Metab Rev 3(1):39–72

    PubMed  CAS  Google Scholar 

  • Abbott NJ, Ronnback L, Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7(1):41–53

    PubMed  CAS  Google Scholar 

  • Abbott N, Patabendige A, Dolman D, Yusof S, Begley D (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37(1):13–25

    PubMed  CAS  Google Scholar 

  • Abbruscato TJ, Davis TP (1999a) Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity. J Pharmacol Exp Ther 289(2):668–675

    PubMed  CAS  Google Scholar 

  • Abbruscato TJ, Davis TP (1999b) Protein expression of brain endothelial cell E-cadherin after hypoxia/aglycemia: influence of astrocyte contact. Brain Res 842(2):277–286

    PubMed  CAS  Google Scholar 

  • Abbruscato TJ, Lopez SP, Mark KS, Hawkins BT, Davis TP (2002) Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J Pharm Sci 91(12):2525–2538

    PubMed  CAS  Google Scholar 

  • Agam K, von Campenhausen M, Levy S, Ben-Ami H, Cook B, Kirschfeld K, Minke B (2000) Metabolic stress reversibly activates the Drosophila light-sensitive channels TRP and TRPL in vivo. J Neurosci 20(15):5748–5755

    PubMed  CAS  Google Scholar 

  • Agell N, Bachs O, Rocamora N, Villalonga P (2002) Modulation of the Ras/Raf/MEK/ERK pathway by Ca(2+), and calmodulin. Cell Signal 14(8):649–654

    PubMed  CAS  Google Scholar 

  • Ahmmed GU, Malik AB (2005) Functional role of TRPC channels in the regulation of endothelial permeability. Pflugers Arch 451(1):131–142

    PubMed  CAS  Google Scholar 

  • Aktan F (2004) iNOS-mediated nitric oxide production and its regulation. Life Sci 75(6):639–653

    PubMed  CAS  Google Scholar 

  • Alfonso S, Benito O, Alicia S, Angelica Z, Patricia G, Diana K, Vaca L (2008) Regulation of the cellular localization and function of human transient receptor potential channel 1 by other members of the TRPC family. Cell Calcium 43(4):375–387

    PubMed  CAS  Google Scholar 

  • Allen N, Attwell D (2002) Modulation of ASIC channels in rat cerebellar Purkinje neurons by ischaemia-related signals. J Physiol 543(Pt 2):521–529

    PubMed  CAS  Google Scholar 

  • Al-Sarraf H, Ghaaedi F, Redzic Z (2007) Time course of hyperosmolar opening of the blood-brain and blood-CSF barriers in spontaneously hypertensive rats. J Vasc Res 44(2):99–109

    PubMed  CAS  Google Scholar 

  • Alvarez de la Rosa D, Krueger S, Kolar A, Shao D, Fitzsimonds R, Canessa C (2003) Distribution, subcellular localization and ontogeny of ASIC1 in the mammalian central nervous system. J Physiol 546(Pt 1):77–87

    PubMed  CAS  Google Scholar 

  • Ambudkar IS (2007) TRPC1: a core component of store-operated calcium channels. Biochem Soc Trans 35(Pt 1):96–100

    PubMed  CAS  Google Scholar 

  • Anderson JM, Van Itallie CM (1995) Tight junctions and the molecular basis for regulation of paracellular permeability. Am J Physiol 269(4 Pt 1):G467–G475

    PubMed  CAS  Google Scholar 

  • Anderson JM, Fanning AS, Lapierre L, Van Itallie CM (1995) Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGuKs) of the tight junction. Biochem Soc Trans 23(3):470–475

    PubMed  CAS  Google Scholar 

  • Andersson DA, Chase HW, Bevan S (2004) TRPM8 activation by menthol, icilin, and cold is differentially modulated by intracellular pH. J Neurosci 24(23):5364–5369

    PubMed  CAS  Google Scholar 

  • Ando J, Komatsuda T, Kamiya A (1988) Cytoplasmic calcium response to fluid shear stress in cultured vascular endothelial cells. In Vitro Cell Dev Biol 24(9):871–877

    PubMed  CAS  Google Scholar 

  • Aneiros E, Cao L, Papakosta M, Stevens EB, Phillips S, Grimm C (2011) The biophysical and molecular basis of TRPV1 proton gating. EMBO J 30(6):994–1002

    PubMed  CAS  Google Scholar 

  • Antoniotti S, Pla AF, Barral S, Scalabrino O, Munaron L, Lovisolo D (2006) Interaction between TRPC channel subunits in endothelial cells. J Recept Signal Transduct Res 26(4):225–240

    PubMed  CAS  Google Scholar 

  • Aono S, Hirai Y (2008) Phosphorylation of claudin-4 is required for tight junction formation in a human keratinocyte cell line. Exp Cell Res 314(18):3326–3339

    PubMed  CAS  Google Scholar 

  • Arnet UA, McMillan A, Dinerman JL, Ballermann B, Lowenstein CJ (1996) Regulation of endothelial nitric-oxide synthase during hypoxia. J Biol Chem 271(25):15069–15073

    PubMed  CAS  Google Scholar 

  • Aschner JL, Lum H, Fletcher PW, Malik AB (1997) Bradykinin- and thrombin-induced increases in endothelial permeability occur independently of phospholipase C but require protein kinase C activation. J Cell Physiol 173(3):387–396

    PubMed  CAS  Google Scholar 

  • Audo I, Kohl S, Leroy BP, Munier FL, Guillonneau X, Mohand-Said S, Bujakowska K, Nandrot EF, Lorenz B, Preising M, Kellner U, Renner AB, Bernd A, Antonio A, Moskova-Doumanova V, Lancelot ME, Poloschek CM, Drumare I, Defoort-Dhellemmes S, Wissinger B, Leveillard T, Hamel CP, Schorderet DF, De Baere E, Berger W, Jacobson SG, Zrenner E, Sahel JA, Bhattacharya SS, Zeitz C (2009) TRPM1 is mutated in patients with autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 85(5):720–729

    PubMed  CAS  Google Scholar 

  • Avila-Flores A, Rendon-Huerta E, Moreno J, Islas S, Betanzos A, Robles-Flores M, Gonzalez-Mariscal L (2001) Tight-junction protein zonula occludens 2 is a target of phosphorylation by protein kinase C. Biochem J 260:295–304

    Google Scholar 

  • Babes A, Ciobanu AC, Neacsu C, Babes RM (2010) TRPM8, a sensor for mild cooling in mammalian sensory nerve endings. Curr Pharm Biotechnol 12(1):78–88

    Google Scholar 

  • Bair AM, Thippegowda PB, Freichel M, Cheng N, Ye RD, Vogel SM, Yu Y, Flockerzi V, Malik AB, Tiruppathi C (2009) Ca2+ entry via TRPC channels is necessary for thrombin-induced NF-kappaB activation in endothelial cells through AMP-activated protein kinase and protein kinase Cdelta. J Biol Chem 284(1):563–574

    PubMed  CAS  Google Scholar 

  • Banasiak K, Xia Y, Haddad GG (2000) Mechanisms underlying hypoxia-induced neuronal ­apoptosis. Prog Neurobiol 62(3):215–249

    PubMed  CAS  Google Scholar 

  • Barajas M, Andrade A, Hernandez-Hernandez O, Felix R, Arias-Montano JA (2008) Histamine-induced Ca2+ entry in human astrocytoma U373 MG cells: evidence for involvement of store-operated channels. J Neurosci Res 86(15):3456–3468

    PubMed  CAS  Google Scholar 

  • Baskaya MK, Rao AM, Donaldson D, Prasad MR, Dempsey RJ (1997) Protective effects of ifenprodil on ischemic injury size, blood-brain barrier breakdown, and edema formation in focal cerebral ischemia. Neurosurgery 40(2):364–370, discussion 370-1

    PubMed  CAS  Google Scholar 

  • Baumann E, Preston E, Slinn J, Stanimirovic D (2009) Post-ischemic hypothermia attenuates loss of the vascular basement membrane proteins, agrin and SPAR$C, and the blood-brain barrier disruption after global cerebral ischemia. Brain Res 1269:185–197

    PubMed  CAS  Google Scholar 

  • Baylie RL, Brayden JE (2011) TRPV channels and vascular function. Acta Physiol (Oxf) 203(1):99–116

    CAS  Google Scholar 

  • Beck B, Zholos A, Sydorenko V, Roudbaraki M, Lehen’kyi V, Bordat P, Prevarskaya N, Skryma R (2006) TRPC7 is a receptor-operated DAG-activated channel in human keratinocytes. J Invest Dermatol 126(9):1982–1993

    PubMed  CAS  Google Scholar 

  • Becker D, Blase C, Bereiter-Hahn J, Jendrach M (2005) TRPV4 exhibits a functional role in cell-volume regulation. J Cell Sci 118(Pt 11):2435–2440

    PubMed  CAS  Google Scholar 

  • Beech DJ (2005) TRPC1: store-operated channel and more. Pflugers Arch 451(1):53–60

    PubMed  CAS  Google Scholar 

  • Belayev L, Busto R, Zhao W, Ginsberg MD (1996) Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res 739(1–2):88–96

    PubMed  CAS  Google Scholar 

  • Bellone RR, Brooks SA, Sandmeyer L, Murphy BA, Forsyth G, Archer S, Bailey E, Grahn B (2008) Differential gene expression of TRPM1, the potential cause of congenital stationary night blindness and coat spotting patterns (LP) in the Appaloosa horse (Equus caballus). Genetics 179(4):1861–1870

    PubMed  CAS  Google Scholar 

  • Bender FL, Mederos YSM, Li Y, Ji A, Weihe E, Gudermann T, Schafer MK (2005) The temperature-sensitive ion channel TRPV2 is endogenously expressed and functional in the primary sensory cell line F-11. Cell Physiol Biochem 15(1–4):183–194

    PubMed  CAS  Google Scholar 

  • Benedikt J, Teisinger J, Vyklicky L, Vlachova V (2007) Ethanol inhibits cold-menthol receptor TRPM8 by modulating its interaction with membrane phosphatidylinositol 4,5-bisphosphate. J Neurochem 100(1):211–224

    PubMed  CAS  Google Scholar 

  • Bennett J, Basivireddy J, Kollar A, Biron KE, Reickmann P, Jefferies WA, McQuaid S (2010) Blood-brain barrier disruption and enhanced vascular permeability in the multiple sclerosis model EAE. J Neuroimmunol 229(1–2):180–191

    PubMed  CAS  Google Scholar 

  • Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RWT (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100(21):12480–12485

    PubMed  CAS  Google Scholar 

  • Bianchi BR, Lee CH, Jarvis MF, El Kouhen R, Moreland RB, Faltynek CR, Puttfarcken PS (2006) Modulation of human TRPV1 receptor activity by extracellular protons and host cell expression system. Eur J Pharmacol 537(1–3):20–30

    PubMed  CAS  Google Scholar 

  • Bodding M, Wissenbach U, Flockerzi V (2002) The recombinant human TRPV6 channel functions as Ca2+ sensor in human embryonic kidney and rat basophilic leukemia cells. J Biol Chem 277(39):36656–36664

    PubMed  CAS  Google Scholar 

  • Bogatcheva N, Garcia JG, Verin AD (2002) Molecular mechanisms of thrombin-induced endothelial cell permeability. Biochemistry (Mosc) 67(1):75–84

    CAS  Google Scholar 

  • Bohmer C, Palmada M, Kenngott C, Lindner R, Klaus F, Laufer J, Lang F (2007) Regulation of the epithelial calcium channel TRPV6 by the serum and glucocorticoid-inducible kinase isoforms SGK1 and SGK3. FEBS Lett 581(29):5586–5590

    PubMed  CAS  Google Scholar 

  • Boje KM, Lakhman SS (2000) Nitric oxide redox species exert differential permeability effects on the blood-brain barrier. J Pharmacol Exp Ther 293(2):545–550

    PubMed  CAS  Google Scholar 

  • Borbiev T, Verin AD, Shi S, Feng L, Garcia JG (2001) Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II. Am J Physiol Lung Cell Mol Physiol 280:L983–L990

    PubMed  CAS  Google Scholar 

  • Borbiev T, Verin AD, Birukova A, Liu F, Crow M, Garcia J (2003) Role of CaM kinase II and ERK activation in thrombin-induced endothelial cell barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 285:L43–L54

    PubMed  CAS  Google Scholar 

  • Bradbury MW, Lightman SL (1990) The blood-brain interface. Eye 4(Pt 2):249–254

    PubMed  Google Scholar 

  • Bredt DS (1999) Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 31(6):577–596

    PubMed  CAS  Google Scholar 

  • Breese NM, George AC, Pauers LE, Stucky CL (2005) Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 115(1–2):37–49

    PubMed  CAS  Google Scholar 

  • Brouns R, De Deyn PP (2009) The complexity of neurobiological processes in acute ischemic stroke. Clin Neurol Neurosurg 111(6):483–495

    PubMed  CAS  Google Scholar 

  • Brown RC, Davis TP (2002) Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke. Stroke 33:1706–1711

    PubMed  CAS  Google Scholar 

  • Brown RC, Davis TP (2005) Hypoxia/aglycemia alters expression of occludin and actin in brain endothelial cells. Biochem Biophys Res Commun 327:1114–1123

    PubMed  CAS  Google Scholar 

  • Brown RC, Egleton RD, Davis TP (2004a) Mannitol opening of the blood-brain barrier: regional variation in the permeability of sucrose, but not 86Rb+ or albumin. Brain Res 1014:221–227

    PubMed  CAS  Google Scholar 

  • Brown RC, Mark KS, Egleton RD, Davis TP (2004b) Protection against hypoxia-induced blood-brain barrier disruption: changes in intracellular calcium. Am J Physiol Cell Physiol 286(5):C1045–C1052

    PubMed  CAS  Google Scholar 

  • Brown R, Wu L, Hicks K, O’Neil RG (2008) Regulation of blood-brain barrier permeability by transient receptor potential type C and type V calcium-permeable channels. Microcirculation 15(4):359–371

    PubMed  CAS  Google Scholar 

  • Brownlow SL, Sage SO (2005) Transient receptor potential protein subunit assembly and membrane distribution in human platelets. Thromb Haemost 94(4):839–845

    PubMed  Google Scholar 

  • Busse R, Mulsch A (1990) Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Lett 265:133–136

    PubMed  CAS  Google Scholar 

  • Butt AM, Jones HC, Abbott NJ (1990) Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study. J Physiol 429:47–62

    PubMed  CAS  Google Scholar 

  • Cai H, McNally JS, Weber M, Harrison DG (2004) Oscillatory shear stress upregulation of endothelial nitric oxide synthase requires intracellular hydrogen peroxide and CaMKII. J Mol Cell Cardiol 37(1):121–125

    PubMed  CAS  Google Scholar 

  • Cai H, Liu D, Garcia JG (2008) CaM Kinase II-dependent pathophysiological signalling in endothelial cells. Cardiovasc Res 77(1):30–34

    PubMed  CAS  Google Scholar 

  • Caraballo JC, Yshii C, Butti ML, Westphal W, Borcherding JA, Allamargot C, Comellas AP (2011) Hypoxia increases transepithelial electrical conductance and reduces occludin at the plasma membrane in alveolar epithelial cells via PKC-zeta and PP2A pathway. Am J Physiol Lung Cell Mol Physiol 300(4):L569–L578

    PubMed  CAS  Google Scholar 

  • Caterina M, Schumacher M, Tominaga M, Rosen T, Levine J, Julius D (1997) The capsaicin ­receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824

    PubMed  CAS  Google Scholar 

  • Cha SK, Huang CL (2010) WNK4 kinase stimulates caveola-mediated endocytosis of TRPV5 amplifying the dynamic range of regulation of the channel by protein kinase C. J Biol Chem 285(9):6604–6611

    PubMed  CAS  Google Scholar 

  • Chattopadhyaya R, Meador WE, Means AR, Quiocho FA (1992) Calmodulin structure refined at 1.7 A resolution. J Mol Biol 228(4):1177–1192

    PubMed  CAS  Google Scholar 

  • Choi D (1996) Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol 6(5):667–672

    PubMed  CAS  Google Scholar 

  • Chuang HH, Neuhausser WM, Julius D (2004) The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43(6):859–869

    PubMed  CAS  Google Scholar 

  • Chung DW, Yoo KY, Hwang IK, Kim DW, Chung JY, Lee CH, Choi JH, Choi SY, Youn HY, Lee IS, Won MH (2009) Systemic administration of lipopolysaccharide induces cyclooxygenase-2 immunoreactivity in endothelium and increases microglia in the mouse hippocampus. Cell Mol Neurobiol 30(4):531–541

    PubMed  Google Scholar 

  • Cioffi DL, Stevens T (2006) Regulation of endothelial cell barrier function by store-operated ­calcium entry. Microcirculation 13(8):709–723

    PubMed  CAS  Google Scholar 

  • Cioffi DL, Wu SW, Stevens T (2003) On the endothelial cell I-SOC. Cell Calcium 33(5–6):323–336

    PubMed  CAS  Google Scholar 

  • Cioffi DL, Wu SW, Alexeyev M, Goodman SR, Zhu MX, Stevens T (2005) Activation of the endothelial store-operated I-SOC Ca2+ channel requires interaction of protein 4.1 with TRPC4. Circ Res 97(11):1164–1172

    PubMed  CAS  Google Scholar 

  • Cioffi D, Lowe K, Alvarez DF, Barry C, Stevens T (2009) TRPing on the lung endothelium: ­calcium channels that regulate barrier function. Antioxid Redox Signal 11(4):765–776

    PubMed  CAS  Google Scholar 

  • Cohen DM (2006) Regulation of TRP channels by N-linked glycosylation. Semin Cell Dev Biol 17(6):630–637

    PubMed  CAS  Google Scholar 

  • Cortright DN, Szallasi A (2004) Biochemical pharmacology of the vanilloid receptor TRPV1. An update. Eur J Biochem 271(10):1814–1819

    PubMed  CAS  Google Scholar 

  • Crone C, Olesen SP (1982) Electrical resistance of brain microvascular endothelium. Brain Res 241(1):49–55

    PubMed  CAS  Google Scholar 

  • Daniels RL, Takashima Y, McKemy DD (2009) Activity of the neuronal cold sensor TRPM8 is regulated by phospholipase C via the phospholipid phosphoinositol 4,5-bisphosphate. J Biol Chem 284(3):1570–1582

    PubMed  CAS  Google Scholar 

  • de Groot T, Lee K, Langeslag M, Xi Q, Jalink K, Bindels RJ, Hoenderop JG (2009) Parathyroid hormone activates TRPV5 via PKA-dependent phosphorylation. J Am Soc Nephrol 20(8):1693–1704

    PubMed  Google Scholar 

  • Del Zoppo GJ (2010) The neurovascular unit in the setting of stroke. J Intern Med 267(2):156–171

    PubMed  Google Scholar 

  • Deli MA, Joo F, Krizbai I, Lengyel I, Nunzi MG, Wolff JR (1993) Calcium/calmodulin-stimulated protein kinase II is present in primary cultures of cerebral endothelial cells. J Neurochem 60(5):1960–1963

    PubMed  CAS  Google Scholar 

  • Deli M, Abraham C, Kataoka Y, Niwa M (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol 25(1):59–127

    PubMed  Google Scholar 

  • Desai BS, Monahan AJ, Carvey PM, Hendey B (2007) Blood-brain barrier pathology in Alzheimer’s and Parkinson’s disease: implications for drug therapy. Cell Transplant 16(3):285–299

    PubMed  Google Scholar 

  • Dhaka A, Earley TJ, Watson J, Patapoutian A (2008) Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J Neurosci 28(3):566–575

    PubMed  CAS  Google Scholar 

  • Dietrich A, Mederos y Schnitzler M, Kalwa H, Storch U, Gudermann T (2005) Functional characterization and physiological relevance of the TRPC3/6/7 subfamily of cation channels. Naunyn Schmiedebergs Arch Pharmacol 37(4):257–265

    Google Scholar 

  • Dinapoli VA, Huber JD, Houser K, Li X, Rosen CL (2008) Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery ­following stroke in aged rats. Neurobiol Aging 29(5):753–764

    PubMed  CAS  Google Scholar 

  • Dodelet-Devillers A, Cayrol R, van Horssen J, Haggani A, de Vriese H, Engelhardt B, Greenwood J, Prat A (2009) Functions of lipid raft membrane microdomains at the blood-brain barrier. J Mol Med 87(8):765–774

    PubMed  CAS  Google Scholar 

  • Domotor E, Abbott NJ, Adam-Vizi V (1999) Na+-Ca2+ exchange and its implications for calcium homeostasis in primary cultured rat brain microvascular endothelial cells. J Physiol 515(Pt 1):147–155

    PubMed  CAS  Google Scholar 

  • Donahue J, Johanson CE (2008) Apolipoprotein E, amyloid-beta and blood-brain barrier permeability in Alzheimer’s disease. J Neuropathol Exp Neurol 67(4):261–270

    PubMed  CAS  Google Scholar 

  • Duz B, Oztas E, Erginay T, Erdogan E, Gonul E (2007) The effect of moderate hypothermia in acute ischemic stroke on pericyte migration: an ultrastructural study. Cryobiology 55(3):279–284

    PubMed  Google Scholar 

  • Easton A, Abbott N (2002) Bradykinin increases permeability by calcium and 5-lipoxygenase in the ECV304/C6 cell culture model of the blood-brain barrier. Brain Res 953(1–2):157–169

    PubMed  CAS  Google Scholar 

  • Embark HM, Setiawan I, Poppendieck S, van de Graaf SF, Boehmer C, Palmada M, Wieder T, Gerstberger R, Cohen P, Yun CC, Bindels RJ, Lang F (2004) Regulation of the epithelial Ca2+ channel TRPV5 by the NHE regulating factor NHERF2 and the serum and glucocorticoid inducible kinase isoforms SGK1 and SGK3 expressed in Xenopus oocytes. Cell Physiol Biochem 14(4–6):203–212

    PubMed  CAS  Google Scholar 

  • Fantozzi I, Zhang S, Platoshyn O, Remillard CV, Cowling RT, Yuan JX (2003) Hypoxia increases AP-1 binding activity by enhancing capacitative Ca2+ entry in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 285(6):L1233–L1245

    PubMed  CAS  Google Scholar 

  • Farshori P, Kachar B (1999) Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells. J Membr Biol 170(2):147–156

    PubMed  CAS  Google Scholar 

  • Fian R, Grasser E, Treiber F, Schmidt R, Niederl P, Rosker C (2007) The contribution of TRPV4-mediated calcium signaling to calcium homeostasis in endothelial cells. J Recept Signal Transduct Res 27(2–3):113–125

    PubMed  CAS  Google Scholar 

  • Fischer S, Wobben M, Marti HH, Renz D, Schaper W (2002) Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc Res 63(1):70–80

    PubMed  CAS  Google Scholar 

  • Fischer S, Wiesnet M, Renz D, Schaper W (2005) H2O2 induces paracellular permeability of porcine brain-derived microvascular endothelial cells by activation of the p44/42 MAP kinase pathway. Eur J Cell Biol 84(7):687–697

    PubMed  CAS  Google Scholar 

  • Fisher M (2008) Injuries to the vascular endothelium: vascular wall and endothelial dysfunction. Rev Neurol Dis 5(Suppl 1):S4–S11

    PubMed  Google Scholar 

  • Fleegal M, Hom S, Borg L, Davis TP (2005) Activation of PKC modulates blood-brain barrier endothelial cell permeability changes induced by hypoxia and post-hypoxic reoxygenation. Am J Physiol Heart Circ Physiol 289(5):H2012–H2019

    PubMed  CAS  Google Scholar 

  • Fleming I, Busse R (2003) Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 284(1):R1–R12

    PubMed  CAS  Google Scholar 

  • Fonfria E, Marshall IC, Benham CD, Boyfield I, Brown JD, Hill K, Hughes JP, Skaper SD, McNulty S (2004) TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase. Br J Pharmacol 143(1):186–192

    PubMed  CAS  Google Scholar 

  • Fonfria E, Murdock PR, Cusdin FS, Benham CD, Kelsell RE, McNulty S (2006) Tissue distribution profiles of the human TRPM cation channel family. J Recept Signal Transduct Res 26(3):159–178

    PubMed  CAS  Google Scholar 

  • Forster C, Clark HB, Ross ME, Iadecola C (1999) Inducible nitric oxide synthase expression in human cerebral infarcts. Acta Neuropathol (Berl) 97(3):215–220

    CAS  Google Scholar 

  • Fucile S, Sucapane A, Eusebi F (2005) Ca2+ permeability of nicotinic acetylcholine receptors from rat dorsal root ganglion neurones. J Physiol 565(Pt 1):219–228

    PubMed  CAS  Google Scholar 

  • Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S (1998a) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141(7):1539–1550

    PubMed  CAS  Google Scholar 

  • Furuse M, Sasaki H, Fujimoto K, Tsukita S (1998b) A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143(2):391–401

    PubMed  CAS  Google Scholar 

  • Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156(6):1099–1111

    PubMed  CAS  Google Scholar 

  • Gao X, Wu L, O’Neil RG (2003) Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278(29):27129–27137

    PubMed  CAS  Google Scholar 

  • Gazzieri D, Trevisani M, Tarantini F, Bechi P, Masotti G, Gensini GF, Castellani S, Marchionni N, Geppetti P, Harrison S (2006) Ethanol dilates coronary arteries and increases coronary flow via transient receptor potential vanilloid 1 and calcitonin gene-related peptide. Cardiovasc Res 70(3):589–599

    PubMed  CAS  Google Scholar 

  • Gerzanich V, Ivanova S, Simard JM (2003) Early pathophysiological changes in cerebral vessels predisposing to stroke. Clin Hemorheol Microcirc 29(3–4):291–294

    PubMed  CAS  Google Scholar 

  • Grimm C, Kraft R, Sauerbruch S, Schultz G, Harteneck C (2003) Molecular and functional characterization of the melastatin-related cation channel TRPM3. J Biol Chem 278(24):21493–21501

    PubMed  CAS  Google Scholar 

  • Gryglewski RJ, Uracz W, Chlopicki S, Marcinkiewicz E (2002) Bradykinin as a major endogenous regulator of endothelial function. Pediatr Pathol Mol Med 21(3):279–290

    PubMed  CAS  Google Scholar 

  • Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22(15):6408–6414

    PubMed  CAS  Google Scholar 

  • Haorah J, Heilman D, Knipe B, Chrastil J, Leibhart J, Ghorpade A, Miller DW, Persidsky Y (2005) Ethanol-induced activation of myosin light chain kinase leads to dysfunction of tight junctions and blood-brain barrier compromise. Alcohol Clin Exp Res 29(6):999–1009

    PubMed  CAS  Google Scholar 

  • Haorah J, Knipe B, Gorantla S, Zheng J, Persidsky Y (2007) Alcohol-induced blood-brain barrier dysfunction is mediated via inositol 1,4,5-triphosphate receptor (IP3R)-gated intracellular calcium release. J Neurochem 100(2):324–336

    PubMed  CAS  Google Scholar 

  • Harhaj NS, Felinski EA, Wolpert EB, Sundstrom JM, Gardner TW, Antonetti DA (2006) VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest Ophthalmol Vis Sci 47(11):5106–5115

    PubMed  Google Scholar 

  • Harnett KM, Biancani P (2003) Calcium-dependent and calcium-independent contractions in smooth muscles. Am J Med 115(Suppl 3A):24S–30S

    PubMed  CAS  Google Scholar 

  • Hartel F, Rodewald C, Alsam M, Gunduz D, Hafer L, Neumann J, Piper HM, Noll T (2007) Extracellular ATP induces assembly and activation of the myosin light chain phosphatase ­complex in endothelial cells. Cardiovasc Res 74(3):487–496

    PubMed  CAS  Google Scholar 

  • Harteneck C (2005) Function and pharmacology of TRPM cation channels. Naunyn Schmiedebergs Arch Pharmacol 371(4):307–314

    PubMed  CAS  Google Scholar 

  • Harteneck C, Reiter B (2007) TRP channels activated by extracellular hypo-osmoticity in ­epithelia. Biochem Soc Trans 35(Pt 1):91–95

    PubMed  CAS  Google Scholar 

  • Harteneck C, Schultz G (2007) TRPV4 and TRPM3 as volume-regulated cation channels. In: Liedtke WB, Heller S (eds) TRP ion channel function in sensory transduction and cellular signaling cascades. CRC, Boca Raton, FL

    Google Scholar 

  • Haseldonckx M, van Bedaf D, van de Ven M, van Reempts J, Borgers M (2000) Vasogenic oedema and brain infarction in an experimental penumbra model. Acta Neurochir Suppl 76:105–109

    PubMed  CAS  Google Scholar 

  • Haskins J, Gu L, Wittchen ES, Hibbard J, Stevenson BR (1998) ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol 141(1):199–208

    PubMed  CAS  Google Scholar 

  • Hecquet CM, Ahmmed GU, Malik AB (2010) TRPM2 channel regulates endothelial barrier function. Adv Exp Med Biol 661:155–167

    PubMed  CAS  Google Scholar 

  • Hellwig N, Plant TD, Janson W, Schafer M, Schultz G, Schaefer M (2004) TRPV1 acts as proton channel to induce acidification in nociceptive neurons. J Biol Chem 279(33):34553–34561

    PubMed  CAS  Google Scholar 

  • Hempel A, Lindschau C, Maasch C, Mahn M, Bychkov R, Noll T, Luft FC, Haller H (1999) Calcium antagonists ameliorate ischemia-induced endothelial cell permeability by inhibiting protein kinase C. Circulation 99(19):2523–2529

    PubMed  CAS  Google Scholar 

  • Hicks K, O’Neil R, Dubinsky W, Brown R (2010a) TRPC-mediated actin-myosin contraction is critical for BBB disruption following hypoxic stress. Am J Physiol Cell Physiol 298(6):C1583–C1593

    PubMed  CAS  Google Scholar 

  • Hicks K, O’Neil RG, Dubinsky WS, Brown RC (2010b) TRPC-mediated actin-myosin contraction is critical for BBB disruption following hypoxic stress. Am J Physiol Cell Physiol 298(6):C1584–C1593

    Google Scholar 

  • Hirt L, Ternon B, Price M, Mastour N, Brunet J, Badaut J (2008) Protective role of early aquaporin 4 induction against postischemic edema formation. J Cereb Blood Flow Metab 29:423–433

    PubMed  Google Scholar 

  • Hoenderop J, van Leeuwen J, van der Eerden B, Kersten F, van der Kemp A, Merrillat A, Waarsing J, Rossier B, Vallon V, Hummler E, Bindels R (2003) Renal Ca2+ wasting, hyperabsorption, and reduced bone thickness in mice lacking TRPV5. J Clin Invest 112(12):1906–1914

    PubMed  CAS  Google Scholar 

  • Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397(6716):259–263

    PubMed  CAS  Google Scholar 

  • Hofmann T, Schaefer M, Schultz G, Gudermann T (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci USA 99(11):7461–7466

    PubMed  CAS  Google Scholar 

  • Hofmann T, Chubanov V, Gudermann T, Montell C (2003) TRPM5 is a voltage-modulated and Ca(2+)-activated monovalent selective cation channel. Curr Biol 13(13):1153–1158

    PubMed  CAS  Google Scholar 

  • Hu HZ, Xiao R, Wang C, Gao N, Colton CK, Wood JD, Zhu MX (2006) Potentiation of TRPV3 channel function by unsaturated fatty acids. J Cell Physiol 208(1):201–212

    PubMed  CAS  Google Scholar 

  • Huang J, Upadhyay UM, Tamargo RJ (2006) Inflammation in stroke and focal cerebral ischemia. Surg Neurol 66(3):232–245

    PubMed  Google Scholar 

  • Ikeda H, Kubo N, Nakamura A, Harada N, Minamino M, Yamashita T (1997a) Histamine-induced calcium released from cultured human mucosal microvascular endothelial cells from nasal inferior turbinate. Acta Otolaryngol 117(6):864–870

    PubMed  CAS  Google Scholar 

  • Ikeda K, Nagashima T, Wu S, Yamaguchi M, Tamaki N (1997b) The role of calcium ion in anoxia/reoxygenation damage of cultured brain capillary endothelial cells. Acta Neurochir Suppl 70:4–7

    PubMed  CAS  Google Scholar 

  • Immke D, McCleskey E (2001) Lactate enhances the acid-sensing Na+ channel on ischemia-­sensing neurons. Nat Neurosci 4(9):869–870

    PubMed  CAS  Google Scholar 

  • Inoue R, Jian Z, Kawarabayashi Y (2009) Mechanosensitive TRP channels in cardiovascular pathophysiology. Pharmacol Ther 123(3):371–385

    PubMed  CAS  Google Scholar 

  • Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147(6):1351–1363

    PubMed  CAS  Google Scholar 

  • Jardin I, Gomez L, Salido G, Rosado J (2009) Dynamic interaction of hTRPC6 with the Orai1-STIM1 complex or hTRPC3 mediates its role in capacitative or non-capacitative Ca(2+) entry pathways. Biochem J 420(2):267–276

    PubMed  CAS  Google Scholar 

  • Joice SL, Mydeen F, Couraud PO, Weksler BB, Romero IA, Fraser PA, Easton AS (2009) Modulation of blood-brain barrier permeability by neutrophils: in vitro and in vivo studies. Brain Res 1298:13–23

    PubMed  CAS  Google Scholar 

  • Ju M, Shi J, Saleh SN, Albert AP, Large WA (2010) Ins(1,4,5)P3 interacts with PIP2 to regulate activation of TRPC6/C7 channels by diacylglycerol in native vascular myocytes. J Physiol 588(Pt 9):1419–1433

    PubMed  CAS  Google Scholar 

  • Kahle KT, Simard JM, Staley KJ, Nahed BV, Jones PS, Sun D (2009) Molecular mechanisms of ischemic cerebral edema: role of electroneutral ion transport. Physiology (Bethesda) 24:257–265

    CAS  Google Scholar 

  • Kalaria RN (1999) The blood-brain barrier and cerebrovascular pathology in Alzheimer’s disease. Ann N Y Acad Sci 893:113–125

    PubMed  CAS  Google Scholar 

  • Kale G, Naren A, Sheth P, Rao R (2003) Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2 and ZO-3. Biochem Biophys Res Commun 302(2):324–329

    PubMed  CAS  Google Scholar 

  • Kashiwagi F, Katayama Y, Igarashi H, Iida S, Muramatsu H, Terashi A (1994) Effect of a new calcium antagonist (SM-6586) on experimental cerebral ischemia. Acta Neurochir Suppl (Wien) 60:289–292

    CAS  Google Scholar 

  • Kaur C, Ling EA (2008) Blood brain barrier in hypoxic-ischemic conditions. Curr Neurovasc Res 5(1):71–81

    PubMed  CAS  Google Scholar 

  • Kawanishi M, Kawai N, Nakamura T, Luo C, Tamiya T, Nagao S (2008) Effect of delayed mild brain hypothermia on edema formation after intracerebral hemorrhage in rats. J Stroke Cerebrovasc Dis 17(4):187–195

    PubMed  Google Scholar 

  • Keeble J, Russell F, Curtis B, Starr A, Pinter E, Brain SD (2005) Involvement of transient receptor potential vanilloid 1 in the vascular and hyperalgesic components of joint inflammation. Arthritis Rheum 52(10):3248–3256

    PubMed  CAS  Google Scholar 

  • Keller PS, Shen X, Hume J (2009) TRPC1 and STIM1 mediate capacitative Ca2+ entry into mouse pulmonary arterial smooth muscle cells. J Physiol 587(Pt 11):2429–2442

    PubMed  Google Scholar 

  • Kempski O, Staub F, Jansen M, Schodel F, Baethmann A (1988) Glial swelling during extracellular acidosis in vitro. Stroke 19(3):385–392

    PubMed  CAS  Google Scholar 

  • Kiedrowski L (2007) NCX and NCKX operation in ischemic neurons. Ann N Y Acad Sci 1099:383–395

    PubMed  CAS  Google Scholar 

  • Kim YA, Park SL, Kim MY, Lee SH, Baik EJ, Moon CH, Jung YS (2010) Role of PKCbetaII and PKCdelta in blood-brain barrier permeability during aglycemic hypoxia. Neurosci Lett 468(3):254–258

    PubMed  CAS  Google Scholar 

  • Kleindienst A, Dunbar JG, Glisson R, Okuno K, Marmarou A (2006) Effect of dimethyl sulfoxide on blood-brain barrier integrity following middle cerebral artery occlusion in the rat. Acta Neurochir Suppl 96:258–262

    PubMed  CAS  Google Scholar 

  • Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 493(4):596–606

    PubMed  CAS  Google Scholar 

  • Koizumi J, Kojima T, Ogasawara N, Kamekura R, Kurose M, Go M, Harimaya A, Murata M, Osanai M, Chiba H, Himi T, Sawada N (2008) Protein kinase C enhances tight junction barrier function of human nasal epithelial cells in primary culture by transcriptional regulation. Mol Pharmacol 74(2):432–442

    PubMed  CAS  Google Scholar 

  • Koizumi K, Iwasaki Y, Narukawa M, Iitsuka Y, Fukao T, Seki T, Ariga T, Watanabe T (2009) Diallyl sulfides in garlic activate both TRPA1 and TRPV1. Biochem Biophys Res Commun 382(3):545–548

    PubMed  CAS  Google Scholar 

  • Kolisek M, Beck A, Fleig A, Penner R (2005) Cyclic ADP-ribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol Cell 18(1):61–69

    PubMed  CAS  Google Scholar 

  • Komarova Y, Malik AB (2010) Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 72:463–493

    PubMed  CAS  Google Scholar 

  • Kozak JA, Matsushita M, Nairn AC, Cahalan MD (2005) Charge screening by internal pH and polyvalent cations as a mechanism for activation, inhibition, and rundown of TRPM7/MIC channels. J Gen Physiol 126(5):499–514

    PubMed  CAS  Google Scholar 

  • Kraft R, Harteneck C (2005) The mammalian melastatin-related transient receptor potential cation channels: an overview. Pflugers Arch 451(1):204–211

    PubMed  CAS  Google Scholar 

  • Krishtal O, Pidoplichko V (1981) Receptor for protons in the membrane of sensory neurons. Brain Res 214(1):150–154

    PubMed  CAS  Google Scholar 

  • Krizanac-Bengez L, Kapural M, Parkinson F, Cucullo L, Hossain M, Mayberg MR, Janigro D (2003) Effects of transient loss of shear stress on blood-brain barrier endothelium: role of nitric oxide and IL-6. Brain Res 977(2):239–246

    PubMed  CAS  Google Scholar 

  • Krizbai IA, Bauer H, Bresgen N, Eckl PM, Farkas A, Szatmari E, Traweger A, Wejksza K, Bauer HC (2005) Effect of oxidative stress on the junctional proteins of cultured cerebral endothelial cells. Cell Mol Neurobiol 25(1):129–139

    PubMed  CAS  Google Scholar 

  • Kwan HY, Huang Y, Yao X (2007) TRP channels in endothelial function and dysfunction. Biochim Biophys Acta 1772(8):907–914

    PubMed  CAS  Google Scholar 

  • Lee S, Lo E (2003) Interactions between p38 mitogen-activated protein kinase and caspase-3 in cerebral endothelial cell death after hypoxia-reoxygenation. Stroke 34:2704–2709

    PubMed  CAS  Google Scholar 

  • Lee K, Kawai N, Kim S, Sagher O, Hoff JT (1997) Mechanisms of edema formation after intracerebral hemorrhage: effects of thrombin on cerebral blood flow, blood-brain barrier permeability, and cell survival in a rat model. J Neurosurg 86(2):272–278

    PubMed  CAS  Google Scholar 

  • Lee J, Cha SK, Sun TJ, Huang CL (2005) PIP2 activates TRPV5 and releases its inhibition by intracellular Mg2+. J Gen Physiol 126(5):439–451

    PubMed  CAS  Google Scholar 

  • Leech S, Kirk J, Plumb J, McQuaid S (2007) Persistent endothelial abnormalities and blood-brain barrier leak in primary and secondary progressive multiple sclerosis. Neuropathol Appl Neurobiol 33(1):86–98

    PubMed  CAS  Google Scholar 

  • Lemonnier L, Trebak M, Putney JW Jr (2008) Complex regulation of the TRPC3, 6 and 7 channel subfamily by diacylglycerol and phosphatidylinositol-4,5-bisphosphate. Cell Calcium 43(5):506–514

    PubMed  CAS  Google Scholar 

  • Leung PC, Cheng KT, Liu C, Cheung WT, Kwan HY, Lau KL, Huang Y, Yao X (2006) Mechanism of non-capacitative Ca2+ influx in response to bradykinin in vascular endothelial cells. J Vasc Res 43(4):367–376

    PubMed  CAS  Google Scholar 

  • Li S, Jiang Q, Stys PK (2000) Important role of reverse Na(+)-Ca(2+) exchange in spinal cord white matter injury at physiological temperature. J Neurophysiol 84(2):1116–1119

    PubMed  CAS  Google Scholar 

  • Li H, Burkhardt C, Heinrich U, Brausch I, Xia N, Forstermann U (2003) Histamine upregulates gene expression of endothelial nitric oxide synthase in human vascular endothelial cells. Circulation 107:2348–2354

    PubMed  CAS  Google Scholar 

  • Li Z, Sergouniotis PI, Michaelides M, Mackay DS, Wright GA, Devery S, Moore AT, Holder GE, Robson AG, Webster AR (2009) Recessive mutations of the gene TRPM1 abrogate ON bipolar cell function and cause complete congenital stationary night blindness in humans. Am J Hum Genet 85(5):711–719

    PubMed  CAS  Google Scholar 

  • Liao Y, Erxleben C, Yildirim E, Abramowitz J, Armstrong DL, Birnbaumer L (2007) Orai proteins interact with TRPC channels and confer responsiveness to store depletion. Proc Natl Acad Sci USA 104(11):4682–4687

    PubMed  CAS  Google Scholar 

  • Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L (2008) Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci USA 105(8):2895–2900

    PubMed  CAS  Google Scholar 

  • Liebner S, Gerhardt H, Wolburg H (2000) Differential expression of endothelial beta-catenin and plakoglobin during development and maturation of the blood-brain and blood-retina barrier in the chicken. Dev Dyn 217(1):86–98

    PubMed  CAS  Google Scholar 

  • Liedtke W, Friedman JM (2003) Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci USA 100(23):13698–13703

    PubMed  CAS  Google Scholar 

  • Liman E (2006) Thermal gating of TRP ion channels: food for thought? Sci STKE 326:pe12

    Google Scholar 

  • Lin M, Leung G, Zhang W, Yang X, Yip K, Tse C, Sham J (2004) Chronic hypoxia-induced upregulation of store-operated and receptor operated Ca2+ channels in pulmonary artery smooth ­muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ Res 95:496–505

    PubMed  CAS  Google Scholar 

  • Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25(7):1674–1681

    PubMed  CAS  Google Scholar 

  • Liu L, Zhu W, Zhang ZS, Yang T, Grant A, Oxford G, Simon SA (2004) Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol 91(4):1482–1491

    PubMed  CAS  Google Scholar 

  • Liu CL, Huang Y, Ngai CY, Leung YK, Yao XQ (2006) TRPC3 is involved in flow- and bradykinin-induced vasodilation in rat small mesenteric arteries. Acta Pharmacol Sin 27(8):981–990

    PubMed  CAS  Google Scholar 

  • Liu XB, Cheng KT, Bandyopadhyay BC, Pani B, Dietrich A, Paria BC, Swaim WD, Beech D, Yildrim E, Singh BB, Birnbaumer L, Ambudkar IS (2007) Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(-/-) mice. Proc Natl Acad Sci USA 104(44):17542–17547

    PubMed  CAS  Google Scholar 

  • Loukin SH, Su Z, Kung C (2009) Hypotonic shocks activate rat TRPV4 in yeast in the absence of polyunsaturated fatty acids. FEBS Lett 583(4):754–758

    PubMed  CAS  Google Scholar 

  • Luh C, Kuhlmann CR, Ackermann B, Timaru-Kast R, Luhmann HJ, Behl C, Werner C, Engelhard K, Thal SC (2010) Inhibition of myosin light chain kinase reduces brain edema formation after traumatic brain injury. J Neurochem 112(4):1015–1025

    PubMed  CAS  Google Scholar 

  • Lum H, Malik AB (1994) Regulation of vascular endothelial barrier function. Am J Physiol 267(3 Pt 1):L223–L241

    PubMed  CAS  Google Scholar 

  • Lum H, Malik AB (1996) Mechanisms of increased endothelial permeability. Can J Physiol Pharmacol 74(7):787–800

    PubMed  CAS  Google Scholar 

  • Mackic JB, Stins M, Jovanovic S, Kim KS, Bartus RT, Zlokovic BV (1999) Cereport (RMP-7) increases the permeability of human brain microvascular endothelial cell monolayers. Pharm Res 16(9):1360–1365

    PubMed  CAS  Google Scholar 

  • Macpherson LJ, Geierstanger BH, Viswanath V, Bandell M, Eid SR, Hwang S, Patapoutian A (2005) The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15(10):929–934

    PubMed  CAS  Google Scholar 

  • Malek AM, Izumo S (1996) Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress. J Cell Sci 109(Pt 4):713–726

    PubMed  CAS  Google Scholar 

  • Marchenko SM, Sage SO (2000) Effects of shear stress on [Ca2+]i and membrane potential of vascular endothelium of intact rat blood vessels. Exp Physiol 85(1):43–48

    PubMed  CAS  Google Scholar 

  • Mark KS, Davis TP (2002) Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 282(4):H1485–H1494

    PubMed  CAS  Google Scholar 

  • Mark KS, Brown RC, Hom S, Davis TP (2001) Hypoxia-induced changes in permeability and tight junctional protein localization of brain microvessel endothelial cells. Soc Neurosci Abstr 434.3

    Google Scholar 

  • Mark KS, Burroughs A, Brown RC, Huber JD, Davis TP (2004) Nitric oxide mediates hypoxia-induced changes in paracellular permeability of cerebral microvasculature. Am J Physiol Heart Circ Physiol 286:H174–H180

    PubMed  CAS  Google Scholar 

  • Mayhan WG (2001) Regulation of blood-brain barrier permeability. Microcirculation 8(2):89–104

    PubMed  CAS  Google Scholar 

  • McCarthy KM, Skare IB, Stankewich MC, Furuse M, Tsukita S, Rogers RA, Lynch RD, Schneeberger EE (1996) Occludin is a functional component of the tight junction. J Cell Sci 109(Pt 9):2287–2298

    PubMed  CAS  Google Scholar 

  • McColl B, Rothwell N, Allan S (2008) Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 28(38):9451–9462

    PubMed  CAS  Google Scholar 

  • McNamara FN, Randall A, Gunthorpe MJ (2005) Effects of piperine, the pungent component of black pepper, at the human vanilloid receptor (TRPV1). Br J Pharmacol 144(6):781–790

    PubMed  CAS  Google Scholar 

  • Melchior B, Frangos JA (2010) Shear-induced endothelial cell-cell junction inclination. Am J Physiol Cell Physiol 299(3):C621–C629

    PubMed  CAS  Google Scholar 

  • Mitic LL, Schneeberger EE, Fanning AS, Anderson JM (1999) Connexin-occludin chimeras containing the ZO-binding domain of occludin localize at MDCK tight junctions and NRK cell contacts. J Cell Biol 146(3):683–693

    PubMed  CAS  Google Scholar 

  • Montell C (2003) Mg2+ homeostasis: the Mg2+nificent TRPM chanzymes. Curr Biol 13(20):R799–R801

    PubMed  CAS  Google Scholar 

  • Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005(272):re3

    PubMed  Google Scholar 

  • Moore TM, Brough GH, Babal P, Kelly J, Li M, Stevens T (1998) Store-operated calcium entry promotes shape change in pulmonary endothelial cells expressing Trp1. Am J Physiol Lung Cell Mol Physiol 275(19):L574–L582

    CAS  Google Scholar 

  • Moore TM, Norwood N, Creighton JR, Babal P, Brough GH, Shasby DM, Stevens T (2000) Receptor-dependent activation of store-operated calcium entry increases endothelial cell permeability. Am J Physiol Lung Cell Mol Physiol 279(4):L691–L698

    PubMed  CAS  Google Scholar 

  • Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, Andahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307(5714):1468–1472

    PubMed  CAS  Google Scholar 

  • Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, Imaizumi Y (2003) TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93(9):829–838

    PubMed  CAS  Google Scholar 

  • Narasimhan P, Liu J, Song Y, Massengale J, Chan P (2009) VEGF stimulates the ERK 1/2 signaling pathway and apoptosis in cerebral endothelial cells after ischemic conditions. Stroke 40(4):1467–1473

    PubMed  CAS  Google Scholar 

  • Naves L, McCleskey E (2005) An acid-sensing ion channel that detects ischemic pain. Braz J Med Biol Res 38(11):1561–1569

    PubMed  CAS  Google Scholar 

  • Nealen ML, Gold MS, Thut PD, Caterina MJ (2003) TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90(1):515–520

    PubMed  CAS  Google Scholar 

  • Nedergaard M, Kraig RP, Tanabe J, Pulsinelli WA (1991) Dynamics of interstitial and intracellular pH in evolving brain infarct. Am J Physiol Regul Integr Comp Physiol 60(3):R581–R588

    Google Scholar 

  • Neelands TR, Jarvis MF, Han P, Faltynek CR, Surowy CS (2005) Acidification of rat TRPV1 alters the kinetics of capsaicin responses. Mol Pain 1:28

    PubMed  Google Scholar 

  • Ng LC, McCormack MD, Airey JA, Singer CA, Keller PS, Shen XM, Hume JR (2009) TRPC1 and STIM1 mediate capacitative Ca2+ entry into mouse pulmonary arterial smooth muscle cells. J Physiol 587(Pt 11):2429–2442

    PubMed  CAS  Google Scholar 

  • Nilius B, Voets T (2004) Diversity of TRP channel activation. Novartis Found Symp 258:140–149, discussion 149–159, 263–266

    PubMed  CAS  Google Scholar 

  • Nilius B, Schwartz G, Oike M, Droogmans G (1993) Histamine-activated, non-selective cation currents and Ca2+ transients in endothelial cells from human umbilical vein. Pflugers Arch 424(3–4):285–293

    PubMed  CAS  Google Scholar 

  • Nilius B, Droogmans G, Wondergem R (2003) Transient receptor potential channels in endothelium: solving the calcium entry puzzle? Endothelium 10:5–15

    PubMed  CAS  Google Scholar 

  • Nilius B, Mahieu F, Prenen J, Janssens A, Owsianik G, Vennekens R, Voets T (2006) The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 25(3):467–478

    PubMed  CAS  Google Scholar 

  • Norwood N, Moore TM, Dean D, Bhattacharjee R, Li M, Stevens T (2000) Store-operated calcium entry and increased endothelial cell permeability. Am J Physiol Lung Cell Mol Physiol 279:L815–L824

    PubMed  CAS  Google Scholar 

  • O’Neil RG, Heller S (2005) The mechanosensitive nature of TRPV channels. Pflugers Arch 451(1):193–203

    PubMed  Google Scholar 

  • Oancea E, Wicks NL (2011) TRPM1: new trends for an old TRP. Adv Exp Med Biol 704:135–145

    PubMed  CAS  Google Scholar 

  • Obukhov AG, Nowycky MC (2002) TRPC4 can be activated by G-protein-coupled receptors and provides sufficient Ca(2+) to trigger exocytosis in neuroendocrine cells. J Biol Chem 277(18):16172–16178

    PubMed  CAS  Google Scholar 

  • Ohta T, Morishita M, Mori Y, Ito S (2004) Ca2+ store-independent augmentation of [Ca2+]i responses to G-protein coupled receptor activation in recombinantly TRPC5-expressed rat pheochromocytoma (PC12) cells. Neurosci Lett 358(3):161–164

    PubMed  CAS  Google Scholar 

  • Ohtsuki S, Yamaguchi H, Katsukura Y, Asashima T, Terasaki T (2008) mRNA expression levels of tight junction protein genes in mouse brain capillary endothelial cells highly purified by magnetic cell sorting. J Neurochem 104(1):147–154

    PubMed  CAS  Google Scholar 

  • Oka M, Itoh Y, Ukai Y (2000) Preferential inhibition by a novel Na(+)/Ca(2+) channel blocker NS-7 of severe to mild hypoxic injury in rat cerebrocortical slices: a possible involvement of a highly voltage-dependent blockade of Ca(2+) channel. J Pharmacol Exp Ther 293(2):522–529

    PubMed  CAS  Google Scholar 

  • Okumura Y, Narukawa M, Iwasaki Y, Ishikawa A, Matsuda H, Yoshikawa M, Watanabe T (2010) Activation of TRPV1 and TRPA1 by black pepper components. Biosci Biotechnol Biochem 74(5):1068–1072

    PubMed  CAS  Google Scholar 

  • Ozaki H, Ishii K, Arai H, Horiuchi H, Kawamoto T, Suzuki H, Kita T (2000) Junctional adhesion molecule (JAM) is phosphorylated by protein kinase C upon platelet activation. Biochem Biophys Res Commun 276(3):873–878

    PubMed  CAS  Google Scholar 

  • Paemeleire K, de Hemptinne A, Leybaert L (1999) Chemically, mechanically, and hyperosmolarity-induced calcium responses of rat cortical capillary endothelial cells in culture. Exp Brain Res 126(4):473–481

    PubMed  CAS  Google Scholar 

  • Paltauf-Doburzynska J, Frieden M, Spitaler M, Graier WF (2000) Histamine-induced Ca2+ oscillations in a human endothelial cell line depend on transmembrane ion flux, ryanodine receptors and endoplasmic reticulum Ca2+-ATPase. J Physiol 524(Pt 3):701–713

    PubMed  CAS  Google Scholar 

  • Pan W, Kastin AJ (2007) Tumor necrosis factor and stroke: role of the blood-brain barrier. Prog Neurobiol 83(6):363–374

    PubMed  CAS  Google Scholar 

  • Park SI, Park EJ, Kim NH, Baek WK, Lee YT, Lee CJ, Suh CK (2001) Hypoxia delays the intracellular Ca2+ clearance by Na+-Ca2+ exchanger in human adult cardiac myocytes. Yonsei Med J 42(3):333–337

    PubMed  CAS  Google Scholar 

  • Park JJ, Lee J, Kim MA, Back SK, Hong SK, Na HS (2007) Induction of total insensitivity to capsaicin and hypersensitivity to garlic extract in human by decreased expression of TRPV1. Neurosci Lett 411(2):87–91

    PubMed  CAS  Google Scholar 

  • Patterson CE, Lum H, Schaphorst KL, Verin AD, Garcia JG (2000) Regulation of endothelial barrier function by the cAMP-dependent protein kinase. Endothelium 7(4):287–308

    PubMed  CAS  Google Scholar 

  • Penner R, Fleig A (2007) The Mg2+ and Mg(2+)-nucleotide-regulated channel-kinase TRPM7. Handb Exp Pharmacol (179):313–328

    Google Scholar 

  • Perez LM, Milkiewicz P, Ahmed-Choudhury J, Elias E, Ochoa JE, Sanchez Pozzi EJ, Coleman R, Roma MG (2006) Oxidative stress induces actin-cytoskeletal and tight-junctional alterations in hepatocytes by a Ca2+ -dependent, PKC-mediated mechanism: protective effect of PKA. Free Radic Biol Med 40(11):2005–2017

    PubMed  CAS  Google Scholar 

  • Perez-Moreno M, Avila A, Islas S, Sanchez S, Gonzalez-Mariscal L (1998) Vinculin but not alpha-actinin is a target of PKC phosphorylation during junctional assembly induced by calcium. J Cell Sci 111(Pt 23):3563–3571

    PubMed  CAS  Google Scholar 

  • Perraud AL, Takanishi CL, Shen B, Kang S, Smith MK, Schmitz C, Knowles HM, Ferraris D, Li W, Zhang J, Stoddard BL, Scharenberg AM (2005) Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels. J Biol Chem 280(7):6138–6148

    PubMed  CAS  Google Scholar 

  • Pfitzer G (2001) Invited review: regulation of myosin phosphorylation in smooth muscle. J Appl Physiol 91(1):497–503

    PubMed  CAS  Google Scholar 

  • Phan MN, Leddy HA, Votta BJ, Kumar S, Levy DS, Lipshutz DB, Lee SH, Liedtke W, Guilak F (2009) Functional characterization of TRPV4 as an osmotically sensitive ion channel in porcine articular chondrocytes. Arthritis Rheum 60(10):3028–3037

    PubMed  CAS  Google Scholar 

  • Plant T, Schaefer M (2003) TRPC4 and TRPC5: receptor-operated Ca2+-permeable nonselective cation channels. Cell Calcium 33:441–450

    PubMed  CAS  Google Scholar 

  • Pogatzki-Zahn EM, Shimizu I, Caterina M, Raja SN (2005) Heat hyperalgesia after incision requires TRPV1 and is distinct from pure inflammatory pain. Pain 115(3):296–307

    PubMed  Google Scholar 

  • Rafalowska J (2002) Experimental and human ischaemia: is the penumbra present in human ischaemic stroke? Folia Neuropathol 40(4):211–217

    PubMed  Google Scholar 

  • Ramsey IS, Delling M, Clapham DE (2006) An introduction to TRP channels. Annu Rev Physiol 68:619–647

    PubMed  CAS  Google Scholar 

  • Rehncrona S (1985) Brain acidosis. Ann Emerg Med 14(8):770–776

    PubMed  CAS  Google Scholar 

  • Revest PA, Abbott NJ, Gillespie JI (1991) Receptor-mediated changes in intracellular [Ca2+] in cultured rat brain capillary endothelial cells. Brain Res 549(1):159–161

    PubMed  CAS  Google Scholar 

  • Rigor RR, Hawkins BT, Miller DS (2010) Activation of PKC isoform beta(I) at the blood-brain barrier rapidly decreases P-glycoprotein activity and enhances drug delivery to the brain. J Cereb Blood Flow Metab 30(7):1373–1383

    PubMed  CAS  Google Scholar 

  • Rossi D, Brady J, Mohr C (2007) Astrocyte metabolism and signaling during brain ischemia. Nat Neurosci 10:1377–1386

    PubMed  CAS  Google Scholar 

  • Rychkov G, Barritt GJ (2007) TRPC1 Ca(2+)-permeable channels in animal cells. Handb Exp Pharmacol (179):23–52

    Google Scholar 

  • Ryu S, Liu B, Yao J, Fu Q, Qin F (2007) Uncoupling proton activation of vanilloid receptor TRPV1. J Neurosci 27(47):12797–12807

    PubMed  CAS  Google Scholar 

  • Sabourin J, Lamiche C, Vandebrouck A, Magaud C, Rivet J, Cognard C, Bourmeyster N, Constantin B (2009) Regulation of TRPC1 and TRPC4 cation channels requires an alpha1-syntrophin-dependent complex in skeletal mouse myotubes. J Biol Chem 284(52):36248–36261

    PubMed  CAS  Google Scholar 

  • Sacks RS, Firth AL, Remillard CV, Agange N, Yau J, Ko EA, Yuan JX (2008) Thrombin-mediated increases in cytosolic [Ca2+] involve different mechanisms in human pulmonary artery smooth muscle and endothelial cells. Am J Physiol Lung Cell Mol Physiol 295(6):L1048–L1055

    PubMed  CAS  Google Scholar 

  • Salazar H, Llorente I, Jara-Oseguera A, Garcia-Villegas R, Munari M, Gordon SE, Islas LD, Rosenbaum T (2008) A single N-terminal cysteine in TRPV1 determines activation by pungent compounds from onion and garlic. Nat Neurosci 11(3):255–261

    PubMed  CAS  Google Scholar 

  • Sandoval KE, Witt KA (2008) Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32(2):200–219

    PubMed  CAS  Google Scholar 

  • Sandoval R, Malik AB, Naqvi T, Mehta D, Tiruppathi C (2001) Requirement for Ca2+ signaling in the mechanism of thrombin-induced increase in endothelial permeability. Am J Physiol Lung Cell Mol Physiol 280(2):L239–L247

    PubMed  CAS  Google Scholar 

  • Scharenberg AM (2005) TRPM2 and TRPM7: channel/enzyme fusions to generate novel intracellular sensors. Pflugers Arch 451(1):220–227

    PubMed  CAS  Google Scholar 

  • Schierling W, Troidl K, Apfelbeck H, Troidl C, Kasprzak PM, Schaper W, Schmitz-Rixen T (2011) Cerebral Arteriogenesis is Enhanced by Pharmacological as Well as Fluid-Shear-Stress Activation of the Trpv4 Calcium Channel. Eur J Vasc Endovasc Surg 41(5):589–596

    PubMed  CAS  Google Scholar 

  • Schlingmann KP, Gudermann T (2005) A critical role of TRPM channel-kinase for human magnesium transport. J Physiol 566(Pt 2):301–308

    PubMed  CAS  Google Scholar 

  • Schmitz C, Perraud AL, Johnson CO, Inabe K, Smith MK, Penner R, Kurosaki T, Fleig A, Scharenberg AM (2003) Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114(2):191–200

    PubMed  CAS  Google Scholar 

  • Schneider JC, El Kebir D, Chereau C, Mercier JC, Dall’Ava-Santucci J, Dinh-Xuan AT (2002) Involvement of Na(+)/Ca(2+) exchanger in endothelial NO production and endothelium-dependent relaxation. Am J Physiol Heart Circ Physiol 283(2):H837–H844

    PubMed  CAS  Google Scholar 

  • Schneider J, El Kabir D, Chereau C, Lanone S, Huang X, De Buys Roessingh A, Mercier J, Dall’ava-Santucci J, Dinh-Xuan A (2003) Involvement of Ca2+/calmodulin-dependent protein kinase II in endothelial NO production and endothelium-depended relaxation. Am J Physiol Heart Circ Physiol 284:H2311–H2319

    PubMed  CAS  Google Scholar 

  • Schoch HJ, Fischer S, Marti HH (2002) Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 125(Pt 11):2549–2557

    PubMed  Google Scholar 

  • Schulze C, Firth JA (1993) Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat. J Cell Sci 104(Pt 3):773–782

    PubMed  Google Scholar 

  • Schwarz G, Callewaert G, Droogmans G, Nilius B (1992) Shear stress-induced calcium transients in endothelial cells from human umbilical cord veins. J Physiol 458:527–538

    PubMed  CAS  Google Scholar 

  • Seth A, Sheth P, Elias BC, Rao R (2007) Protein phosphatases 2A and 1 interact with occludin and negatively regulate the assembly of tight junctions in the CACO-2 cell monolayer. J Biol Chem 282(15):11487–11498

    PubMed  CAS  Google Scholar 

  • Sherkheli MA, Benecke H, Doerner JF, Kletke O, Vogt-Eisele AK, Gisselmann G, Hatt H (2009) Monoterpenoids induce agonist-specific desensitization of transient receptor potential vanilloid-3 (TRPV3) ion channels. J Pharm Pharm Sci 12(1):116–128

    PubMed  CAS  Google Scholar 

  • Simka M (2009) Blood brain barrier compromise with endothelial inflammation may lead to autoimmune loss of myelin during multiple sclerosis. Curr Neurovasc Res 6(2):132–139

    PubMed  CAS  Google Scholar 

  • Sjo A, Magnusson KE, Peterson KH (2010) Protein kinase C activation has distinct effects on the localization, phosphorylation and detergent solubility of the claudin protein family in tight and leaky epithelial cells. J Membr Biol 236(2):181–189

    PubMed  Google Scholar 

  • Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, Wright JE, Jerman JC, Walhin JP, Ooi L, Egerton J, Charles KJ, Smart D, Randall AD, Anand P, Davis JB (2002) TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418(6894):186–190

    PubMed  CAS  Google Scholar 

  • Soboloff J, Spassova M, Hewavitharana T, He LP, Luncsford P, Xu W, Venkatachalam K, van Rossum D, Patterson RL, Gill DL (2007) TRPC channels: integrators of multiple cellular ­signals. Handb Exp Pharmacol (179):575–591

    Google Scholar 

  • Soderling TR, Stull JT (2001) Structure and regulation of calcium/calmodulin-dependent protein kinases. Chem Rev 101(8):2341–2352

    PubMed  CAS  Google Scholar 

  • Sopjani M, Kunert A, Czarkowski K, Klaus F, Laufer J, Foller M, Lang F (2010) Regulation of the Ca(2+) channel TRPV6 by the kinases SGK1, PKB/Akt, and PIKfyve. J Membr Biol 233(1–3):35–41

    PubMed  CAS  Google Scholar 

  • Srinivas SP, Satpathy M, Guo Y, Anandan V (2006) Histamine-induced phosphorylation of the regulatory light chain of myosin II disrupts the barrier integrity of corneal endothelial cells. Invest Ophthalmol Vis Sci 47(9):4011–4018

    PubMed  Google Scholar 

  • Staaf S, Franck MC, Marmigere F, Mattsson JP, Ernfors P (2010) Dynamic expression of the TRPM subgroup of ion channels in developing mouse sensory neurons. Gene Expr Patterns 10(1):65–74

    PubMed  CAS  Google Scholar 

  • Stamatovic S, Keep R, Andjelkovic A (2008) Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr Neuropharmacol 6(3):179–192

    PubMed  CAS  Google Scholar 

  • Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88(4):1341–1378

    PubMed  CAS  Google Scholar 

  • Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986) Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103(3):755–766

    PubMed  CAS  Google Scholar 

  • Stuart RO, Nigam SK (1995) Regulated assembly of tight junctions by protein kinase C. Proc Natl Acad Sci USA 92(13):6072–6076

    PubMed  CAS  Google Scholar 

  • Suh YG, Oh U (2005) Activation and activators of TRPV1 and their pharmaceutical implication. Curr Pharm Des 11(21):2687–2698

    PubMed  CAS  Google Scholar 

  • Suzuki M, Mizuno A, Kodaira K, Imai M (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278(25):22664–22668

    PubMed  CAS  Google Scholar 

  • Suzuki T, Elias BC, Seth A, Shen L, Turner JR, Giorgianni F, Desiderio D, Guntaka R, Rao R (2009) PKC eta regulates occludin phosphorylation and epithelial tight junction integrity. Proc Natl Acad Sci USA 106(1):61–66

    PubMed  CAS  Google Scholar 

  • Swulius M, Waxham MN (2008) Ca2+/calmodulin-dependent protein kinases. Cell Mol Life Sci 65:2637–2657

    PubMed  CAS  Google Scholar 

  • Tai YH, Flick J, Levine SA, Madara JL, Sharp GW, Donowitz M (1996) Regulation of tight junction resistance in T84 monolayers by elevation in intracellular Ca2+: a protein kinase C effect. J Membr Biol 149(1):71–79

    PubMed  CAS  Google Scholar 

  • Takagaki Y, Itoh Y, Aoki Y, Ukai Y, Yoshikuni Y, Kimura K (1997) Inhibition of ischemia-induced fodrin breakdown by a novel phenylpyrimidine derivative NS-7: an implication for its neuroprotective action in rats with middle cerebral artery occlusion. J Neurochem 68(6):2507–2513

    PubMed  CAS  Google Scholar 

  • Takahashi M, Ishida T, Traub O, Corson MA, Berk BC (1997) Mechanotransduction in endothelial cells: temporal signaling events in response to shear stress. J Vasc Res 34(3):212–219

    PubMed  CAS  Google Scholar 

  • Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438(7070):1022–1025

    PubMed  CAS  Google Scholar 

  • Tamura M, Aoki Y, Seto T, Itoh Y, Ukai Y (2001) Cerebroprotective action of a Na+/Ca2+ channel blocker NS-7. II. Effect on the cerebral infarction, behavioral and cognitive impairments at the chronic stage of permanent middle cerebral artery occlusion in rats. Brain Res 890(1):170–176

    PubMed  CAS  Google Scholar 

  • Tatlisumak T, Carano RA, Takano K, Meiler MR, Li F, Sotak CH, Pschorn U, Fisher M (2000) Broad-spectrum cation channel inhibition by LOE 908 MS reduces infarct volume in vivo and postmortem in focal cerebral ischemia in the rat. Acta Neurochir Suppl 76:329–330

    PubMed  CAS  Google Scholar 

  • Thiel VE, Audus KL (2001) Nitric oxide and blood-brain barrier integrity. Antioxid Redox Signal 3(2):273–278

    PubMed  CAS  Google Scholar 

  • Tiruppathi C, Freichel M, Vogel SM, Paria B, Mehta D, Flockerzi V, Malik AB (2002a) Impairment of store-operated Ca2+ entry in TRPC4-/- mice interferes with increase in lung microvascular permeability. Circ Res 91:70–76

    PubMed  CAS  Google Scholar 

  • Tiruppathi C, Minshall RD, Paria BC, Vogel SM, Malik AB (2002b) Role of Ca2+ signaling in the regulation of endothelial permeability. Vascul Pharmacol 39(4–5):173–185

    PubMed  CAS  Google Scholar 

  • Tiruppathi C, Ahmmed GU, Vogel SM, Malik AB (2006) Ca2+ signaling, TRP channels, and endothelial permeability. Microcirculation 13(8):693–708

    PubMed  CAS  Google Scholar 

  • Tomas-Camardiel M, Venero JL, Herrera A, De Pablos R, Pintor-Toro J, Machado A, Cano J (2005) Blood-brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals. J Neurosci Res 80(2):235–246

    PubMed  CAS  Google Scholar 

  • Topala CN, Bindels RJ, Hoenderop JG (2007) Regulation of the epithelial calcium channel TRPV5 by extracellular factors. Curr Opin Nephrol Hypertens 16(4):319–324

    PubMed  CAS  Google Scholar 

  • Topala CN, Schoeber JP, Searchfield LE, Riccardi D, Hoenderop JG, Bindels RJ (2009) Activation of the Ca2+-sensing receptor stimulates the activity of the epithelial Ca2+ channel TRPV5. Cell Calcium 45(4):331–339

    PubMed  CAS  Google Scholar 

  • Townsley MI, King JA, Alvarez DF (2006) Ca2+ channels and pulmonary endothelial permeability: insights from study of intact lung and chronic pulmonary hypertension. Microcirculation 13(8):725–739

    PubMed  CAS  Google Scholar 

  • Trebak M, Vazquez G, Bird GS, Putney JW Jr (2003) The TRPC3/6/7 subfamily of cation ­channels. Cell Calcium 33(5–6):451–461

    PubMed  CAS  Google Scholar 

  • Tsukamoto T, Nigam SK (1999) Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. Am J Physiol 276(5 Pt 2):F737–F750

    PubMed  CAS  Google Scholar 

  • Turner JR, Angle JM, Black ED, Joyal JL, Sacks DB, Madara JL (1999) PKC-dependent ­regulation of transepithelial resistance: roles of MLC and MLC kinase. Am J Physiol 277(3 Pt 1):C554–C562

    PubMed  CAS  Google Scholar 

  • Ueno M (2007) Molecular anatomy of the brain endothelial barrier: an overview of the distributional features. Curr Med Chem 14(11):1199–1206

    PubMed  CAS  Google Scholar 

  • Ueno M (2009) Mechanisms of the penetration of blood-borne substances into the brain. Curr Neuropharmacol 7(2):142–149

    PubMed  CAS  Google Scholar 

  • Urquhart BL, Kim RB (2009) Blood-brain barrier transporters and response to CNS-active drugs. Eur J Clin Pharmacol 65(11):1063–1070

    PubMed  CAS  Google Scholar 

  • Valeski J, Baldwin A (2003) Role of the actin cytoskeleton in regulating endothelial permeability in venules. Microcirculation 10(5):411–420

    PubMed  CAS  Google Scholar 

  • Van Der Stelt M, Di Marzo V (2004) Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem 271(10):1827–1834

    Google Scholar 

  • van Genderen MM, Bijveld MM, Claassen YB, Florijn RJ, Pearring JN, Meire FM, McCall MA, Riemslag FC, Gregg RG, Bergen AA, Kamermans M (2009) Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. Am J Hum Genet 85(5):730–736

    PubMed  Google Scholar 

  • van Hinsbergh VW, van Nieuw Amerongen GP (2002) Intracellular signalling involved in modulating human endothelial barrier function. J Anat 200(6):549–560

    PubMed  Google Scholar 

  • van Nieuw Amerongen G, Draijer R, Vermeer M, van Hinsbergh V (1998) Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium and RhoA. Circ Res 83:1115–1123

    PubMed  Google Scholar 

  • Vandenbroucke E, Mehta D, Minshall R, Malik AB (2008) Regulation of endothelial junctional permeability. Ann N Y Acad Sci 1123:134–145

    PubMed  CAS  Google Scholar 

  • Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417

    PubMed  CAS  Google Scholar 

  • Vennekens R, Owsianik G, Nilius B (2008) Vanilloid transient receptor potential cation channels: an overview. Curr Pharm Des 14(1):18–31

    PubMed  CAS  Google Scholar 

  • Vogt-Eisele AK, Weber K, Sherkheli MA, Vielhaber G, Panten J, Gisselmann G, Hatt H (2007) Monoterpenoid agonists of TRPV3. Br J Pharmacol 151(4):530–540

    PubMed  CAS  Google Scholar 

  • Vorbrodt AW, Dobrogowska DH (2003) Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers: electron microscopist’s view. Brain Res Brain Res Rev 42(3):221–242

    PubMed  CAS  Google Scholar 

  • Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101(1):396–401

    PubMed  CAS  Google Scholar 

  • Waldmann R, Lazdunski M (1998) H+-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol 8(3):418–424

    PubMed  CAS  Google Scholar 

  • Waldmann R, Champigny G, Lingueglia E, de Weille J, Heurteaux C, Lazdunski M (1999) H+-gated cation channels. Ann N Y Acad Sci 868:67–76

    PubMed  CAS  Google Scholar 

  • Wang Y, Liu Y (2009) Bradykinin selectively modulates the blood-tumor barrier via calcium-induced calcium release. J Neurosci Res 87(3):660–667

    PubMed  CAS  Google Scholar 

  • Wang CX, Shuaib A (2007) Critical role of microvasculature basal lamina in ischemic brain injury. Prog Neurobiol 83(3):140–148

    PubMed  CAS  Google Scholar 

  • Wang XX, Pluznick JL, Wei PL, Padanilam BJ, Sansom SC (2004) TRPC4 forms store-operated Ca2+ channels in mouse mesangial cells. Am J Physiol Cell Physiol 287(2):C357–C364

    PubMed  CAS  Google Scholar 

  • Wang J, Weigand L, Lu W, Sylvester JT, Semenza GL, Shimoda LA (2006) Hypoxia inducible factor 1 mediates hypoxia-induced TRPC expression and elevated intracellular Ca2+ in pulmonary arterial smooth muscle cells. Circ Res 98(12):1528–1537

    PubMed  CAS  Google Scholar 

  • Wang HP, Pu XY, Wang XH (2007) Distribution profiles of transient receptor potential melastatin-related and vanilloid-related channels in prostatic tissue in rat. Asian J Androl 9(5):634–640

    PubMed  Google Scholar 

  • Wang Z, Ginnan R, Abdullaev IF, Trebak M, Vincent PA, Singer HA (2010) Calcium/Calmodulin-dependent protein kinase II delta 6 (CaMKIIdelta6) and RhoA involvement in thrombin-induced endothelial barrier dysfunction. J Biol Chem 285(28):21303–21312

    PubMed  CAS  Google Scholar 

  • Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277(49):47044–47051

    PubMed  CAS  Google Scholar 

  • Webb AA, Muir GD (2000) The blood-brain barrier and its role in inflammation. J Vet Intern Med 14(4):399–411

    PubMed  CAS  Google Scholar 

  • Wei Z, Al-Mehdi AB, Fisher AB (2001) Signaling pathway for nitric oxide generation with simulated ischemia in flow-adapted endothelial cells. Am J Physiol Heart Circ Physiol 281:H2226–H2232

    PubMed  CAS  Google Scholar 

  • Weiler F, Marbe T, Scheppach W, Schauber J (2005) Influence of protein kinase C on transcription of the tight junction elements ZO-1 and occludin. J Cell Physiol 204(1):83–86

    PubMed  CAS  Google Scholar 

  • Weiss N, Miller F, Cazaubon S, Couraud P (2009) The blood-brain barrier in brain hoemostasis and neurological diseases. Biochim Biophys Acta 1788(4):842–857

    PubMed  CAS  Google Scholar 

  • Weyerbrock A, Walbridge S, Saavedra JE, Keefer LK, Oldfield EH (2011) Differential effects of nitric oxide on blood-brain barrier integrity and cerebral blood flow in intracerebral C6 gliomas. Neuro Oncol 13(2):203–211

    PubMed  CAS  Google Scholar 

  • White PF (2008) Red-hot chili peppers: a spicy new approach to preventing postoperative pain. Anesth Analg 107(1):6–8

    PubMed  Google Scholar 

  • Wilhelm I, Farkas AE, Nagyoszi P, Varo G, Balint Z, Vegh GA, Couraud PO, Romero IA, Weksler B, Krizbai IA (2007) Regulation of cerebral endothelial cell morphology by extracellular ­calcium. Phys Med Biol 52(20):6261–6274

    PubMed  CAS  Google Scholar 

  • Wittchen ES, Haskins J, Stevenson BR (1999) Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J Biol Chem 274(49):35179–35185

    PubMed  CAS  Google Scholar 

  • Wong V (1997) Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am J Physiol 273(6 Pt 1):C1859–C1867

    PubMed  CAS  Google Scholar 

  • Wong D, Dorovini-Zis K, Vincent SR (2004) Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp Neurol 190(2):446–455

    PubMed  CAS  Google Scholar 

  • Wu L, Gao X, Brown RC, Heller S, O’Neil RG (2007) Dual role of TRPV4 channel as a sensor of flow and osmolality in renal epithelial cells. Am J Physiol Renal Physiol 293(5):F1699–F1713

    PubMed  CAS  Google Scholar 

  • Xiong Z, Zhu X, Chu X, Minami M, Hey J, Wei W, MacDonald J, Wemmie J, Price M, Welsh M, Simon R (2004) Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118(6):687–698

    PubMed  CAS  Google Scholar 

  • Xiong ZG, Pignataro G, Li M, Chang SY, Simon RP (2008) Acid-sensing ion channels (ASICs) as pharmacological targets for neurodegenerative diseases. Curr Opin Pharmacol 8(1):25–32

    PubMed  CAS  Google Scholar 

  • Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y, DiStefano PS, Curtis R, Clapham DE (2002) TRPV3 is a calcium-permeable temperature-­sensitive cation channel. Nature 418(6894):181–186

    PubMed  CAS  Google Scholar 

  • Xu H, Blair NT, Clapham DE (2005) Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J Neurosci 25(39):8924–8937

    PubMed  CAS  Google Scholar 

  • Yamaji R, Fujita K, Takahashi S, Yoneda H, Nagao K, Masuda W, Naito M, Tsuruo T, Miyatake K, Inui H, Nakano Y (2003) Hypoxia up-regulates glyceraldehyde-3-phosphate dehydrogenase in mouse brain capillary endothelial cells: involvement of Na+/Ca2+ exchanger. Biochim Biophys Acta 1593(2–3):269–276

    PubMed  CAS  Google Scholar 

  • Yang T, Roder KE, Abbruscato TJ (2007) Evaluation of bEnd5 cell line as an in vitro model for the blood-brain barrier under normal and hypoxic/aglycemic conditions. J Pharm Sci 96(12):3196–3213

    PubMed  CAS  Google Scholar 

  • Yuan SY (2000) Signal transduction pathways in enhanced microvascular permeability. Microcirculation 7(6 Pt 1):395–403

    PubMed  CAS  Google Scholar 

  • Yuan JP, Zeng WZ, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9(6):636–645

    PubMed  CAS  Google Scholar 

  • Zhang DX, Gutterman DD (2011) Transient receptor potential channel activation and endothelium-dependent dilation in the systemic circulation. J Cardiovasc Pharmacol 57(2):133–139

    PubMed  CAS  Google Scholar 

  • Zhao H, Steinberg GK, Sapolsky RM (2007) General versus specific actions of mild-moderate hypothermia in attenuating cerebral ischemic damage. J Cereb Blood Flow Metab 27(12):1879–1894

    PubMed  CAS  Google Scholar 

  • Zhu MX (2005) Multiple roles of calmodulin and other Ca(2+)-binding proteins in the functional regulation of TRP channels. Pflugers Arch 451(1):105–115

    PubMed  CAS  Google Scholar 

  • Zunkeler B, Carson RE, Olson J, Blasberg RG, DeVroom H, Lutz RJ, Saris SC, Wright DC, Kammerer W, Patronas NJ, Dedrick RL, Herscovitch P, Oldfield EH (1996) Quantification and pharmacokinetics of blood-brain barrier disruption in humans. J Neurosurg 85(6):1056–1065

    PubMed  CAS  Google Scholar 

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Correspondence to Rachel C. Brown .

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© 2012 Springer Science+Business Media New York

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Brown, R.C. (2012). Calcium Signaling at the Blood–Brain Barrier in Stroke. In: Li, Y., Zhang, J. (eds) Metal Ion in Stroke. Springer Series in Translational Stroke Research. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-9663-3_6

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