Abstract
The blood-brain barrier of the neurovascular unit is a critical organ for normal brain function. It is continuously exposed to mechanical stress both from the peripheral circulation and plasma osmolarity changes. Barrier integrity is regulated by a number of mechanisms, including influx of calcium ions and activation of calcium-sensitive signaling pathways. This review addresses the molecular identity of the channels underlying mechanosensitive calcium influx, and hypothesizes a central role for transient receptor potential channels in mechanosensitive regulation of blood-brain barrier endothelial cell function.
Access provided by Autonomous University of Puebla. Download to read the full chapter text
Chapter PDF
Similar content being viewed by others
Keywords
References
Abbott NJ, Ronnback L and Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7(1):41–53.
Abbruscato TJ and Davis TP (1999) Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity. J Pharmacol Exp Ther 289(2):668–675.
Adler S, Verbalis JG, Meyers S, Simplaceanu E and Williams DS (2000) Changes in cerebral blood flow and distribution associated with acute increases in plasma sodium and osmolality of chronic hyponatremic rats. Exp Neurol 163(1):63–71.
Adler S, Verbalis JG and Williams DS (1995) Effect of rapid correction of hyponatremia on the blood-brain barrier of rats. Brain Res 679(1):135–143.
Adler S, Williams DS and Verbalis JG (1993) Effect of acute and chronic hyponatremia on blood-brain barrier function in the rat. NMR Biomed 6(2):119–124.
Ahmmed GU, Mehta D, Vogel S, Holinstat M, Paria BC, Tiruppathi C and Malik AB (2004) Protein kinase C alpha phosphorylates the TRPC1 channel and regulates store-operated Ca2+ entry in endothelial cells. J Biol Chem 279(20):20941–20949.
Al-Sarraf H, Ghaaedi F and 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.
Albert JL, Boyle JP, Roberts JA, Challiss RA, Gubby SE and Boarder MR (1997) Regulation of brain capillary endothelial cells by P2Y receptors coupled to Ca2+, phospholipase C and mitogen-activated protein kinase. Br J Pharmacol 122(5):935–941.
Andreeva A, Krause E, Muller E, Blasig IE and Utepbergenov D (2001) Protein kinase C regulates the phosphorylation and cellular localization of occludin. J Biol Chem 276(42):38480–38486.
Aschner JL, Lum H, Fletcher PW and 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.
Baker E, Tian Y, Adler S and Verbalis JG (2000) Blood-brain barrier disruption and complement activation in the brain following rapid correction of chronic hyponatremia. Exp Neurol 165(2):221–230.
Ballabh P, Braun A and Nedergaard M (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 16(1):1–13.
Barres BA, Chun LL and Corey DP (1989) Calcium current in cortical astrocytes: induction by cAMP and neurotransmitters and permissive effect of serum factors. J Neurosci 9(9):3169–3175.
Bartha K, Domotor E, Lanza F, Adam-Vizi V and Machovich R (2000) Identification of thrombin receptors in rat brain capillary endothelial cells. J Cereb Blood Flow Metab 20(1):175–182.
Bazzoni G and Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84(3):869–901.
Beech DJ (2005) TRPC1: store-operated channel and more. Pflugers Arch 451(1):53–60.
Beresewicz A, Czarnowska E and Maczewski M (1998) Ischemic preconditioning and superoxide dismutase protect against endothelial dysfunction and endothelium glycocalyx disruption in the postischemic guinea-pig hearts. Mol Cell Biochem 186(1–2): 87–97.
Berkels R, Mueller A, Roesen R and Klaus W (1999) Nifedipine and Bay K 8644 Induce an increase of [Ca(2alpha)](i) and Nitric Oxide in Endothelial Cells. J Cardiovasc Pharmacol Ther 4(3):175–181.
Berna N, Arnould T, Remacle J and Michiels C (2001) Hypoxia-induced increase in intracellular calcium concentration in endothelial cells: role of the Na+-glucose cotransporter. J Cell Biochem 84(1):115–131.
Birder L, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai A, Wang E, Ruiz G, de Groat W, Apodaca G, Watkins S and Caterina M (2002) Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5:856–860.
Borbiev T, Verin AD, Birukova A, Liu F, Crow M and 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.
Borbiev T, Verin AD, Shi S, Feng L and 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.
Brown R, Wu L, Hicks K and O'Neil RG (2008) Regulation of blood-brain barrier permeability by transient receptor potential type C and type V calcium-permeable channels. Microcirculation in press.
Brown RC and 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.
Brown RC, Egleton RD and 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.
Brown RC, Mark KS, Egleton RD and Davis TP (2004b) Protection against hypoxia-induced blood-brain barrier disruption: changes in intracellular calcium. Am J Physiol Cell Physiol 286(5): C1045–C1052.
Brown RC, Mark KS, Egleton RD, Huber JD, Burroughs A and Davis TP (2003) Protection against hypoxia-induced increase in blood-brain barrier permeability: role of tight junction proteins and NFκB. J Cell Sci 116(Pt 4): 693–700.
Burnstock G (2006) Purinergic signaling--an overview. Novartis Found Symp 276:26–48; discussion 48–57, 275–81.
Busse R and Fleming I (2006) Vascular endothelium and blood flow. Handb Exp Pharmacol (176 Pt 2): 43–78.
Busse R and Mulsch A (1990) Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Lett 265:133–136.
Caterina M, Schumacher M, Tominaga M, Rosen T, Levine J and Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824.
Catterall WA (1998) Structure and function of neuronal Ca2+ channels and their role in neurotransmitter release. Cell Calcium 24(5–6): 307–323.
Chishty M, Begley D, Abbott JN and Reichel A (2003) Functional characteristics of nucleoside transport in rat brain endothelial cells. Neuroreport 14(7):1087–1090.
Ciura S and Bourque CW (2006) Transient receptor potential vanilloid 1 is required for intrinsic osmoreception in organum vasculosum lamina terminalis neurons and for normal thirst responses to systemic hyperosmolality. J Neurosci 26(35):9069–9075.
Coleman HA, Tare M and Parkington HC (2004) Endothelial potassium channels, endothelium-dependent hyperpolarization and the regulation of vascular tone in health and disease. Clin Exp Pharmacol Physiol 31(9):641–649.
Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Geleoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D and Zhang DS (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432(7018):723–730.
Delmas P (2005) Polycystins: polymodal receptor/ion-channel cellular sensors. Pflugers Arch 451(1):264–276.
Dermietzel R and Krause D (1991) Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry. Int Rev Cytol 127:57–109.
Dietrich A, Kalwa H, Storch U, Mederos YSM, Salanova B, Pinkenburg O, Dubrovska G, Essin K, Gollasch M, Birnbaumer L and Gudermann T (2007) Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch 455(3):465–477.
Duchene AD and Takeda K (1997) P2Y- and P2U-mediated increases in internal calcium in single bovine aortic endothelial cells in primary culture. Endothelium 5(4):277–286.
Dundas B, Harris M and Narasimhan M (2007) Psychogenic polydipsia review: etiology, differential, and treatment. Curr Psychiatry Rep 9(3):236–241.
Easton A and 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.
Fatehi M, Gerhart D, Myers T and Drewes L (1987) Characterization of the blood-brain barrier: glycoconjugate receptors of 14 lectins in canine brain, cultured endothelial cells, and blotted membrane proteins. Brain Res 415(1):30–39.
Fischer S, Wiesnet M, Marti HH, Renz D and Schaper W (2004) Simultaneous activation of several second messengers in hypoxia-induced hyperpermeability of brain derived endothelial cells. J Cell Physiol 198:359–369.
Fischer S, Wobben M, Marti HH, Renz D and 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.
Fleegal M, Hom S, Borg L and 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.
Forman JR, Qamar S, Paci E, Sandford RN and Clarke J (2005) The remarkable mechanical strength of polycystin-1 supports a direct role in mechanotransduction. J Mol Biol 349(4):861–871.
Gao X, Wu L and 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.
Garigan TP and Ristedt DE (1999) Death from hyponatremia as a result of acute water intoxication in an Army basic trainee. Mil Med 164(3):234–238.
Gautam M, Gojova A and Barakat AI (2006) Flow-activated ion channels in vascular endothelium. Cell Biochem Biophys 46(3):277–284.
Gottlieb P, Folgering J, Maroto R, Raso A, Wood TG, Kurosky A, Bowman C, Bichet D, Patel A, Sachs F, Martinac B, Hamill OP and Honore E (2007) Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflugers Arch.
Grammas P, Moore P, Cashman RE and Floyd RA (1998) Anoxic injury of endothelial cells causes divergent changes in protein kinase C and protein kinase A signaling pathways. Mol Chem Neuropathol 33(2):113–124.
Greenwood J (1991) Mechanisms of blood-brain barrier breakdown. Neuroradiology 33(2):95–100.
Gumbiner B and Simons K (1987) The role of uvomorulin in the formation of epithelial occluding junctions. Ciba Found Symp 125:168–86.
Gumbiner B, Stevenson B and Grimaldi A (1988) The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol 107(4):1575–1587.
Gumerlock MK, Belshe BD, Madsen R and Watts C (1992) Osmotic blood-brain barrier disruption and chemotherapy in the treatment of high grade malignant glioma: patient series and literature review. J Neurooncol 12(1):33–46.
Gunduz D, Hirche F, Hartel F, Rodewald C, Schafer M, Pfitzer G, Piper H and Noll T (2003) ATP antagonism of thrombin-induced endothelial barrier permeability. Cardiovasc Res 59(2):470–480.
Hanaoka K, Qian F, Boletta A, Bhunia A, Piontek K, Tsiokas L, Sukhatme VP, Guggino W and Germino G (2000) Co-assembly of polycistin-1 and -2 produces unique cation-permeable currents. Nature 408(6815):990–994.
Haorah J, Heilman D, Knipe B, Chrastil J, Leibhart J, Ghorpade A, Miller DW and 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.
Harrington LS, Evans RJ, Wray J, Norling L, Swales KE, Vial C, Ali F, Carrier MJ and Mitchell JA (2007) Purinergic 2X1 receptors mediate endothelial dependent vasodilation to ATP. Mol Pharmacol 72(5):1132–1136.
Hawkins BT and Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57(2):173–185.
Hempel A, Lindschau C, Maasch C, Mahn M, Bychkov R, Noll T, Luft FC and Haller H (1999) Calcium antagonists ameliorate ischemia-induced endothelial cell permeability by inhibiting protein kinase C. Circulation 99(19):2523–2529.
Henry C and Duling B (2000) TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 279(6): H2815–H2823.
Hom S, Egleton RD, Huber JD and Davis TP (2001) Effect of reduced flow on blood-brain barrier transport systems. Brain Res 890(1):38–48.
Hom S, Fleegal M, Egleton RD, Campos CR, Hawkins BT and Davis TP (2007) Comparative changes in the blood-brain barrier and cerebral infarction of SHR and WKY rats. Am J Physiol Regul Integr Comp Physiol 292(5): R1881–R1892.
Ikeda K, Nagashima T, Wu S, Yamaguchi M and Tamaki N (1997) The role of calcium ion in anoxia/reoxygenation damage of cultured brain capillary endothelial cells. Acta Neurochir Suppl 70:4–7.
Ishizaki T, Chiba H, Kojima T, Fujibe M, Soma T, Miyajima H, Nagasawa K, Wada I and Sawada N (2003) Cyclic AMP induces phosphorylation of claudin-5 immunoprecipitates and expression of claudin-5 gene in blood-brain barrier endothelial cells via protein kinase A-dependent and -independent pathways. Exp Cell Res 290(2):275–288.
Jolliet-Riant P and Tillement JP (1999) Drug transfer across the blood-brain barrier and improvement of brain delivery. Fundam Clin Pharmacol 13(1):16–26.
Kale G, Naren A, Sheth P and 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.
Kamouchi M, Kitazono T, Ago T, Wakisaka M, Ooboshi H, Ibayashi S and Iida M (2004) Calcium influx pathways in rat CNS pericytes. Brain Res Mol Brain Res 126(2):114–20.
Keep RF, Xiang J and Betz AL (1993) Potassium transport at the blood-brain and blood-CSF barriers. Adv Exp Med Biol 331:43–54.
Kim Y, Di Cello F, Hillaire C and Kim K (2004) Differential Ca2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am J Physiol Cell Physiol 286(1): C31–C42.
Kimura C, Oike M and Ito Y (2000) Hypoxia-induced alterations in Ca2+ mobilization in brain microvascular endothelial cells. Am J Physiol Heart Circ Physiol 279(5): H2310–H2318.
Kohler R, Heyken WT, Heinau P, Schubert R, Si H, Kacik M, Busch C, Grgic I, Maier T and Hoyer J (2006) Evidence for a functional role of endothelial transient receptor potential V4 in shear stress-induced vasodilatation. Arterioscler Thromb Vasc Biol 26(7):1495–1502.
Kraft R, Grimm C, Grosse K, Hoffmann A, Sauerbruch S, Kettenmann H, Schultz G and Harteneck C (2004) Hydrogen peroxide and ADP-ribose induce TRPM2-mediated calcium influx and cation currents in microglia. Am J Physiol Cell Physiol 286(1): C129–C137.
Krizanac-Bengez L, Kapural M, Parkinson F, Cucullo L, Hossain M, Mayberg MR and 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.
Krizbai I, Bauer H, Bresgen N, Eckl P, Farkas A, Szatmari E, Traweger A, Wejksza K and Bauer H (2005) Effect of oxidative stress on the junctional proteins of cultured cerebral endothelial cells. Cell Mol Neurobiol 25(1):129–139.
Kuroiwa T, Shibutani M and Okeda R (1988) Blood-brain barrier disruption and exacerbation of ischemic brain edema after restoration of blood flow in experimental focal cerebral ischemia. Acta Neuropathol 76(1):62–70.
Lawrenson J, Cassella J, Hayes A, Firth JA and Allt G (2000) Endothelial glycoconjugates: a comparative lectin study of the brain, retina and myocardium. J Anat 196:55–60.
Lee H, Iida T, Mizuno A, Suzuki M and Caterina M (2005) Altered thermal selection behavior in mice lacking transient receptor potential vanilloid 4. J Neurosci 25(5):1304–1310.
Lerner R (1994) Changes of cytosolic calcium ion concentrations in human endothelial cells in response to thrombin, platelet-activating factor, and leukotriene B4. J Lab Clin Med 124(5):723–729.
Levine JD and Alessandri-Haber N (2007) TRP channels: targets for the relief of pain. Biochim Biophys Acta 1772(8):989–1003.
Li L, Bressler B, Prameya R, Dorovini-Zis K and Van Breemen C (1999) Agonist-stimulated calcium entry in primary cultures of human cerebral microvascular endothelial cells. Microvasc Res 57(3):211–226.
Li S, Jiang Q and Stys PK (2000) Important role of reverse Na+/Ca2+ exchange in spinal cord white matter injury at physiological temperature. J Neurophysiol 84(2):1116–1119.
Liedtke W, Choe Y, Marti-Renom M, Bell A, Denis C, Sali A, Hudspeth A, Friedman JM and Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103(3):525–535.
Liedtke W and Friedman JM (2003) Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci USA 100(23):13698–13703.
Lin SY and Corey DP (2005) TRP channels in mechanosensation. Curr Opin Neurobiol 15(3):350–357.
Mark KS, Brown RC, Hom S and Davis TP (2001) Hypoxia-induced changes in permeability and tight junctional protein localization of brain microvessel endothelial cells. Society for Neuroscience Abstracts 434.3.
Mark KS, Burroughs A, Brown RC, Huber JD and Davis TP (2004) Nitric oxide mediates hypoxia-induced changes in paracellular permeability of cerebral microvasculature. Am J Physiol Heart Circ Physiol 286: H174–H180.
Mark KS and 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.
Maroto R, Raso A, Wood T, Kurosky A, Martinac B and Hamill O (2005) TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7(2):179–185.
Marrelli SP, O'Neil RG, Brown RC and Bryan RM Jr (2007) PLA2 and TRPV4 channels regulate endothelial calcium in cerebral arteries. Am J Physiol Heart Circ Physiol 292(3): H1390–H1397.
Miyagi Y, Kobayashi S, Nishimura J, Fukui M and Kanaide H (1996) P2U receptor is linked to cytosolic Ca2+ transient and release of vasorelaxing factor in bovine endothelial cells in situ. J Physiol 492 (Pt 3): 751–761.
Mizuno A, Matsumoto N, Imai M and Suzuki M (2003) Impaired osmotic sensation in mice lacking TRPV4. Am J Physiol Cell Physiol 285(1): C96–C101.
Mooradian AD (1988) Effect of aging on the blood-brain barrier. Neurobiol Aging 9(1):31–39.
Mott R and Helmke B (2007) Mapping the dynamics of shear stress-induced structural changes in endothelial cells. Am J Physiol Cell Physiol 293(5): C1616–C1626.
Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M and Imaizumi Y (2003) TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93:829–838.
Nagashima T, Ikeda K, Wu S, Kondo T, Yamaguchi M and Tamaki N (1997). The mechanism of reversible osmotic opening of the blood-brain barrier: role of intracellular calcium ion in capillary endothelial cells. Acta Neurochir Suppl 70:231–233.
Nagashima T, Shijing W, Mizoguchi A and Tamaki N (1994) A possible role of calcium ion in osmotic opening of blood-brain barrier. J Auton Nerv Sys 49: S145–S149.
Nagy Z, Pappius HM, Mathieson G and Huttner I (1979). Opening of tight junctions in cerebral endothelium. I. Effect of hyperosmolar mannitol infused through the internal carotid artery. J Comp Neurol 185(3):569–578.
Nauli S, Alenghat F, Luo Y, Williams E, Vassilev P, Li X, Elia A, Lu W, Brown E, Quinn S, Ingber D and Zhou J (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33(2):129–137.
Neuhaus W, Lauer R, Oelzant S, Fringeli UP, Ecker GF and Noe CR (2006) A novel flow based hollow-fiber blood-brain barrier in vitro model with immortalised cell line PBMEC/C1-2. J Biotechnol 125(1):127–141.
Neuwelt EA, Maravilla KR, Frenkel EP, Rapaport SI, Hill SA and Barnett PA (1979) Osmotic blood-brain barrier disruption. Computerized tomographic monitoring of chemotherapeutic agent delivery. J Clin Invest 64(2):684–688.
Nilius B, Droogmans G and Wondergem R (2003) Transient receptor potential channels in endothelium: solving the calcium entry puzzle? Endothelium 10:5–15.
Nilius B and Voets T (2004) Diversity of TRP channel activation. Novartis Found Symp 258:140–149; discussion 149–59, 263–266.
Noakes T (2002) Hyponatremia in distance runners: fluid and sodium balance during exercise. Curr Sports Med Rep 1(4):197–207.
Noakes T (2003). Fluid replacement during marathon running. Clin J Sport Med 13(5):309–318.
Nobles M, Revest PA, Couraud PO and Abbott NJ (1995) Characteristics of nucleotide receptors that cause elevation of cytoplasmic calcium in immortalized rat brain endothelial cells (RBE4) and in primary cultures. Br J Pharmacol 115(7):1245–1252.
O'Donnell ME, Martinez A and Sun D (1995) Cerebral microvascular endothelial cell Na-K-Cl cotransport: regulation by astrocyte-conditioned medium. Am J Physiol 268(3 Pt 1): C747–C754.
O'Neil RG and Heller S (2005) The mechanosensitive nature of TRPV channels. Pflugers Arch 451(1):193–203.
Ohtake K, Maeno T, Ueda H, Ogihara M, Natsume H and Morimoto Y (2003) Poly-L-arginine enhances paracellular permeability via serine/threonine phosphorylation of ZO-1 and tyrosine dephosphorylation of occludin in rabbit nasal epithelium. Pharm Res 20(11):1838–1845.
Oster J and Singer I (1999) Hyponatremia, hyposmolality and hypotonicity: tables and fables. Arch Intern Med 159(4):333–336.
Paemeleire K, de Hemptinne A and 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.
Paltauf-Doburzynska J, Frieden M, Spitaler M and 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.
Paria BC, Vogel SM, Ahmmed GU, Alamgir S, Shroff J, Malik AB and Tiruppathi C (2004) Tumor necrosis factor-alpha-induced TRPC1 expression amplifies store-operated Ca2+ influx and endothelial permeability. Am J Physiol Lung Cell Mol Physiol 287(6): L1303–L1313.
Petty MA and Wettstein JG (2001) Elements of cerebral microvascular ischaemia. Brain Res Brain Res Rev 36(1):23–34.
Pizzo P, Burgo A, Pozzan T and Fasolato C (2001) Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. J Neurochem 79(1):98–109.
Plateel M, Teissier E and Cecchelli R (1997) Hypoxia dramatically increases the nonspecific transport of blood-borne proteins to the brain. J Neurochem 68(2):874–877.
Preston E and Webster J (2002) Differential passage of [14C]sucrose and [3H]inulin across rat blood-brain barrier after cerebral ischemia. Acta Neuropathol 103(3):237–242.
Ramirez AN and Kunze DL (2002) P2X purinergic receptor channel expression and function in bovine aortic endothelium. Am J Physiol Heart Circ Physiol 282(6): H2106–H2116.
Rapoport SI (1970) Effect of concentrated solutions on the blood-brain barrier. Am J Physiol 219(1):270–274.
Rapoport SI, Hori M and Klatzo I (1971). Reversible osmotic opening of the blood-brain barrier. Science 173(4001):1026–1028.
Riesen FK, Rothen-Rutishauser B and Wunderli-Allenspach H (2002) A ZO1-GFP fusion protein to study the dynamics of tight junctions in living cells. Histochem Cell Biol 117(4):307–315.
Rubin LL and Staddon JM (1999) The cell biology of the blood-brain barrier. Annu Rev Neurosci 22:11–28.
Sahagun G, Moore S and Hart M (1990) Permeability of neutral vs. anionic dextrans in cultured brain microvascular endothelium. Am J Physiol 259(1 Pt 2): H162–H166.
Sedova M and Blatter LA (1999) Dynamic regulation of [Ca2+]i by plasma membrane Ca2+-ATPase and Na+/Ca2+ exchange during capacitative Ca2+ entry in bovine vascular endothelial cells. Cell Calcium 25(5):333–343.
Sharif Naeini R, Witty MF, Seguela P and Bourque CW (2006) An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nat Neurosci 9(1):93–98.
Sipos I, Domotor E, Abbott NJ and Adam-Vizi V (2000) The pharmacology of nucleotide receptors on primary rat brain endothelial cells grown on a biological extracellular matrix: effects on intracellular calcium concentration. Br J Pharmacol 131(6):1195–1203.
Sotomayor M, Corey DP and Schulten K (2005) In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 13(4):669–682.
Spassova MA, Hewavitharana T, Xu W, Soboloff J and Gill DL (2006) A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci USA 103(44):16586–16591.
Speedy DB, Faris JG, Hamlin M, Gallagher PG and Campbell RG (1997) Hyponatremia and weight changes in an ultradistance triathlon. Clin J Sport Med 7(3):180–184.
Stanimirovic DB, Nikodijevic B, Nikodijevic-Kedeva D, McCarron RM and Spatz M (1994) Signal transduction and Ca2+ uptake activated by endothelins in rat brain endothelial cells. Eur J Pharmacol 288(1):1–8.
Stanness KA, Westrum LE, Fornaciari E, Mascagni P, Nelson JA, Stenglein SG, Myers T and Janigro D (1997). Morphological and functional characterization of an in vitro blood-brain barrier model. Brain Res 771(2):329–342.
Stuart RO, Sun A, Panichas M, Hebert SC, Brenner BM and Nigam SK (1994) Critical role for intracellular calcium in tight junction biogenesis. J Cell Physiol 159(3):423–433.
Suzuki M, Mizuno A, Kodaira K and Imai M (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278(25):22664–22668.
Tanaka N, Kawasaki K, Nejime N, Kubota Y, Nakamura K, Kunitomo M, Takahashi K, Hashimoto M and Shinozuka K (2004) P2Y receptor-mediated Ca2+ signaling increases human vascular endothelial cell permeability. J Pharmacol Sci 95(2):174–180.
Taniguchi J, Tsuruoka S, Mizuno A, Sato J, Fujimura A and Suzuki M (2007) TRPV4 as a flow sensor in flow-dependent K+ secretion from the cortical collecting duct. Am J Physiol Renal Physiol 292(2): F667–F673.
Tarbell J and Pahakis M (2006) Mechanotransduction and the glycocalyx. J Int Med 259(4):339–350.
Thiel VE and Audus KL (2001) Nitric oxide and blood-brain barrier integrity. Antioxid Redox Signal 3(2):273–278.
Tiruppathi C, Minshall RD, Paria BC, Vogel SM and Malik AB (2002) Role of Ca2+ signaling in the regulation of endothelial permeability. Vascul Pharmacol 39(4–5): 173–185.
Ueno M, Sakamoto H, Liao Y, Onodera M, Huang C, Miyanaka H and Nakagawa T (2004) Blood-brain barrier disruption in the hypothalamus of young adult spontaneously hypertensive rats. Histochem Cell Biol 122(2):131–137.
Vanhauwe JF, Thomas TO, Minshall RD, Tiruppathi C, Li A, Gilchrist A, Yoon EJ, Malik AB and Hamm HE (2002) Thrombin receptors activate G(o) proteins in endothelial cells to regulate intracellular calcium and cell shape changes. J Biol Chem 277(37):34143–34149.
Vannucci SJ, Maher F and Simpson IA (1997) Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 21(1):2–21.
Venkatachalam K and Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417.
Vogel J, Sperandio M, Pries A, Linderkamp O, Gaehtgens P and Kuschinsky W (2000) Influence of the endothelial glycocalyx on cerebral blood flow in mice. J Cereb Blood Flow Metab 20(11):1571–1578.
Vriens J, Owsianik G, Fisslthaler B, Suzuki M, Janssens A, Voets T, Morisseau C, Hammock BD, Fleming I, Busse, R and Nilius B (2005) Modulation of the Ca2+ permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res 97(9):908–915.
Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T and Nilius B (2004). Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A 101(1):396–401.
Wei Z, Manevich Y, Al-Mehdi A, Chatterjee S and Fisher A (2004) Ca2+ flux through voltage-gated channels with flow cessation in pulmonary microvascular endothelial cells. Microcirculation 11(6):517–526.
Weinbaum S, Tarbell J and Damiano E (2007) The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9:121–167.
Westenbroek RE, Bausch SB, Lin RC, Franck JE, Noebels JL and Catterall WA (1998). Upregulation of L-type Ca2+ channels in reactive astrocytes after brain injury, hypomyelination, and ischemia. J Neurosci 18(7):2321–2334.
White TA, Xue A, Chini EN, Thompson M, Sieck GC and Wylam ME (2006) Role of TRPC3 in Tumor Necrosis Factor-alpha Enhanced Calcium Influx in Human Airway Myocytes. Am J Respir Cell Mol Biol.
Wu L, Gao X, Brown RC, Heller S and O'Neil RG (2007) Dual role of TRPV4 channel as a sensor of flow and osmlolality in renal epithelial cells. Am J Physiol Renal Physiol 293(5): F1699–F1713.
Yakubu MA and Leffler CW (2002) L-type voltage-dependent Ca2+ channels in cerebral microvascular endothelial cells and ET-1 biosynthesis. Am J Physiol Cell Physiol 283(6): C1687–C1695.
Yao X and Garland CJ (2005) Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 97(9):853–863.
Ye J, Tsukamoto T, Sun A and Nigam SK (1999) A role for intracellular calcium in tight junction reassembly after ATP depletion-repletion. Am J Physiol Renal Physiol 277(4 Pt 2): F524-F532.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Brown, R.C., O’Neil, R.G. (2009). Mechanosensitive Calcium Fluxes in the Neurovascular Unit: TRP Channel Regulation of the Blood-Brain Barrier. In: Kamkim, A., Kiseleva, I. (eds) Mechanosensitivity of the Nervous System. Mechanosensitivity in Cells and Tissues, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8716-5_15
Download citation
DOI: https://doi.org/10.1007/978-1-4020-8716-5_15
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-8715-8
Online ISBN: 978-1-4020-8716-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)