Skip to main content
SpringerLink
Log in

Stroke Induced Blood-Brain Barrier Disruption

  • Chapter
  • First Online:
Advancement in the Pathophysiology of Cerebral Stroke

Abstract

Blood-brain barrier (BBB) is highly ultra-synchronized, structural and biochemical barrier between the peripheral blood circulation and the central nervous system (CNS) coordinate entry of blood-borne entities into the CNS. BBB anatomy is comprised of microvascular endothelium, pericytes, astrocytes and neuronal cells that constitute a neurovascular unit (NVU), participating a crucial role in proper functioning of the CNS. Every cell of NVU forms an indispensable contribution to BBB integrity. BBB functions are mainly controlled by tight and adherens junctional (TJ and AJ) protein complexes. These restrictive angioarchitectures at BBB reduce the paracellular diffusion of molecules, whereas carrier proteins determine which substance can cross the transcellular barrier. Under normal condition, BBB prevents extravasation of blood-borne cell, solute, ions and molecules. However, its disruption can lead to change in paracellular and transcellular permeability and extravasation of leukocytes into brain tissue, contributing oedema formation in neuropathological disorder including brain stroke. This chapter emphasized recently gained information on BBB anatomy and its neuropathogenetic alteration in an ischemic cerebral injury.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AJ:

Adherens junction

BBB:

Blood-brain barrier

CNS:

Central nervous system

CSF:

Cerebrospinal fluid

JAM:

Junctional adhesion molecule

MAGUK:

Membrane-associated guanylate kinase

MS:

Multiple sclerosis

NMO:

Neuromyelitis optica

NPSLE:

Neuropsychiatric systemic lupus erythematosus

NVU:

Neurovascular unit

TBI:

Traumatic brain injury

TEMPOL:

4-hydroxy-2,2,6,6-tetramethylpiperidine-N-oxyl

TJ:

Tight junction

References

  1. Lewandowsky, M. (1900). Zur lehre von der cerebrospinalflussigkeit. Zeitschrift für Klinische Medizin, 40(480), 19.

    Google Scholar 

  2. Goldmann, E. E. (1909). Diessere und innere Sekretion des gesunden und kranken Organismus m Lichte der ‘vitalen Farbung’. Beiträge zur Klinischen Chirurgie, 64, 192–265.

    Google Scholar 

  3. Goldmann, E. E. (1913). Vitalfarbung am Zentralnervensystem. Abhandlungan Preussischen Akademii Wissenschaften Physics-Mathematics, 1, 1–60.

    Google Scholar 

  4. Zlokovic, B. V. (2008). The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron, 57, 178–201.

    Article  CAS  PubMed  Google Scholar 

  5. Reese, T. S., & Karnovsky, M. J. (1967). Fine structural localization of a blood-brain barrier to exogenous peroxidase. The Journal of Cell Biology, 34(1), 207–217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., Das, S. R., de Ferranti, S., Despres, J. P., Fullerton, H. J., Howard, V. J., Huffman, M. D., Isasi, C. R., Jimenez, M. C., Judd, S. E., Kissela, B. M., Lichtman, J. H., Lisabeth, L. D., Liu, S., Mackey, R. H., Magid, D. J., McGuire, D. K., Mohler, E. R., 3rd, Moy, C. S., Muntner, P., Mussolino, M. E., Nasir, K., Neumar, R. W., Nichol, G., Palaniappan, L., Pandey, D. K., Reeves, M. J., Rodriguez, C. J., Rosamond, W., Sorlie, P. D., Stein, J., Towfighi, A., Turan, T. N., Virani, S. S., Woo, D., Yeh, R. W., Turner, M. B., American Heart Association Statistic, C, & Stroke Statistics, S. (2016). Heart disease and stroke statistics-2016 update: A report from the American Heart Association. Circulation, 133, e38–e360.

    PubMed  Google Scholar 

  7. Keaney, J., & Campbell, M. (2015). The dynamic blood-brain barrier. The FEBS Journal, 282, 4067–4079.

    Article  CAS  PubMed  Google Scholar 

  8. Petty, M. A., & Wettstein, J. G. (2001). Elements of cerebral microvascular ischaemia. Brain Research Reviews, 36(1), 23–34.

    Article  CAS  PubMed  Google Scholar 

  9. Oldendorf, W. H., Cornford, M. E., & Brown, W. J. (1977). The large apparent work capability of the blood-brain barrier: A study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Annals of Neurology, 1(5), 409–417.

    Article  CAS  PubMed  Google Scholar 

  10. Fenstermacher, J., Gross, P., Sposito, N., Acuff, V., Pettersen, S., & Gruber, K. (1988). Structural and functional variations in capillary systems within the brain. Annals of the New York Academy of Sciences, 529(1), 21–30.

    Article  CAS  PubMed  Google Scholar 

  11. Sedlakova, R., Shivers, R. R., & Del Maestro, R. F. (1999). Ultrastructure of the blood-brain barrier in the rabbit. Journal of Submicroscopic Cytology and Pathology, 31(1), 149–161.

    CAS  PubMed  Google Scholar 

  12. Klingler, C., Kniesel, U., Bamforth, S. D., Wolburg, H., Engelhardt, B., & Risau, W. (2000). Disruption of epithelial tight junctions is prevented by cyclic nucleotide-dependent protein kinase inhibitors. Histochemistry and Cell Biology, 113(5), 349–361.

    CAS  PubMed  Google Scholar 

  13. Tagami, M., Nara, Y., Kubota, A., Fujino, H., & Yamori, Y. (1990). Ultrastructural changes in cerebral pericytes and astrocytes of stroke-prone spontaneously hypertensive rats. Stroke, 21(7), 1064–1071.

    Article  CAS  PubMed  Google Scholar 

  14. Bandopadhyay, R., Orte, C., Lawrenson, J. G., Reid, A. R., De Silva, S., & Allt, G. (2001). Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. Journal of Neurocytology, 30(1), 35–44.

    Article  CAS  PubMed  Google Scholar 

  15. Gonul, E., Duz, B., Kahraman, S., Kayali, H., Kubar, A., & Timurkaynak, E. (2002). Early pericyte response to brain hypoxia in cats: An ultrastructural study. Microvascular Research, 64(1), 116–119.

    Article  PubMed  Google Scholar 

  16. Dore-Duffy, P., Owen, C., Balabanov, R., Murphy, S., Beaumont, T., & Rafols, J. A. (2000). Pericyte migration from the vascular wall in response to traumatic brain injury. Microvascular Research, 60(1), 55–69.

    Article  CAS  PubMed  Google Scholar 

  17. Hori, S., Ohtsuki, S., Hosoya, K. I., Nakashima, E., & Terasaki, T. (2004). A pericyte-derived angiopoietin-1 multimeric complex induces occludin gene expression in brain capillary endothelial cells through Tie-2 activation in vitro. Journal of Neurochemistry, 89(2), 503–513.

    Article  CAS  PubMed  Google Scholar 

  18. Sofroniew, M. V. (2015). Astrocyte barriers to neurotoxic inflammation. Nature reviews. Neuroscience, 16(5), 249.

    CAS  PubMed  Google Scholar 

  19. Ballabh, P., Braun, A., & Nedergaard, M. (2004). The blood–brain barrier: An overview: Structure, regulation, and clinical implications. Neurobiology of Disease, 16(1), 1–13.

    Article  CAS  PubMed  Google Scholar 

  20. Braet, K., Paemeleire, K., D'herde, K., Sanderson, M. J., & Leybaert, L. (2001). Astrocyte–endothelial cell calcium signals conveyed by two signalling pathways. European Journal of Neuroscience, 13(1), 79–91.

    CAS  PubMed  Google Scholar 

  21. Zonta, M., Angulo, M. C., Gobbo, S., Rosengarten, B., Hossmann, K. A., Pozzan, T., & Carmignoto, G. (2003). Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nature Neuroscience, 6(1), 43–50.

    Article  CAS  PubMed  Google Scholar 

  22. Asgari, N., Berg, C. T., Mørch, M., Khorooshi, R. M., & Owens, T. (2016). Cerebrospinal fluid aquaporin-4-immunoglobulin G induces blood brain barrier breakdown. Annals of Clinical and Translational Neurology.

    Google Scholar 

  23. Hatashita, S., & Hoff, J. T. (1990). Brain edema and cerebrovascular permeability during cerebral ischemia in rats. Stroke, 21(4), 582–588.

    Article  CAS  PubMed  Google Scholar 

  24. Lee, E. J., Hung, Y. C., & Lee, M. Y. (1999). Early alterations in cerebral hemodynamics, brain metabolism, and blood-brain barrier permeability in experimental intracerebral hemorrhage. Journal of Neurosurgery, 91(6), 1013–1019.

    Article  CAS  PubMed  Google Scholar 

  25. Ben-Menachem, E., Johansson, B. B., & Svensson, T. H. (1982). Increased vulnerability of the blood-brain barrier to acute hypertension following depletion of brain noradrenaline. Journal of Neural Transmission, 53(2), 159–167.

    Article  CAS  PubMed  Google Scholar 

  26. Cohen, Z., Molinatti, G., & Hamel, E. (1997). Astroglial and vascular interactions of noradrenaline terminals in the rat cerebral cortex. Journal of Cerebral Blood Flow & Metabolism, 17(8), 894–904.

    Article  CAS  Google Scholar 

  27. Cohen, Z. V. I., Bonvento, G., Lacombe, P., & Hamel, E. (1996). Serotonin in the regulation of brain microcirculation. Progress in Neurobiology, 50(4), 335–362.

    Article  CAS  PubMed  Google Scholar 

  28. Vaucher, E., & Hamel, E. (1995). Cholinergic basal forebrain neurons project to cortical microvessels in the rat: Electron microscopic study with anterogradely transported Phaseolus vulgaris leucoagglutinin and choline acetyltransferase immunocytochemistry. Journal of Neuroscience, 15(11), 7427–7441.

    Article  CAS  PubMed  Google Scholar 

  29. Tong, X. K., & Hamel, E. (1999). Regional cholinergic denervation of cortical microvessels and nitric oxide synthase-containing neurons in Alzheimer’s disease. Neuroscience, 92(1), 163–175.

    Article  CAS  PubMed  Google Scholar 

  30. Vaucher, E., Tong, X. K., Cholet, N., Lantin, S., & Hamel, E. (2000). GABA neurons provide a rich input to microvessels but not nitric oxide neurons in the rat cerebral cortex: A means for direct regulation of local cerebral blood flow. Journal of Comparative Neurology, 421(2), 161–171.

    Article  CAS  PubMed  Google Scholar 

  31. Kobayashi, H., Magnoni, M. S., Govoni, S., Izumi, F., Wada, A., & Trabucchi, M. (1985). Neuronal control of brain microvessel function. Experientia, 41(4), 427–434.

    Article  CAS  PubMed  Google Scholar 

  32. Rosenberg, G. A., Estrada, E., Kelley, R. O., & Kornfeld, M. (1993). Bacterial collagenase disrupts extracellular matrix and opens blood-brain barrier in rat. Neuroscience Letters, 160(1), 117–119.

    Article  CAS  PubMed  Google Scholar 

  33. Rascher, G., Fischmann, A., Kröger, S., Duffner, F., Grote, E. H., & Wolburg, H. (2002). Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: Spatial segregation of tenascin and agrin. Acta Neuropathologica, 104(1), 85–91.

    Article  CAS  PubMed  Google Scholar 

  34. Hynes, R. O. (1992). Integrins: Versatility, modulation, and signaling in cell adhesion. Cell, 69(1), 11–25.

    Article  CAS  PubMed  Google Scholar 

  35. Tilling, T., Korte, D., Hoheisel, D., & Galla, H. J. (1998). Basement membrane proteins influence brain capillary endothelial barrier function in vitro. Journal of Neurochemistry, 71(3), 1151–1157.

    Article  CAS  PubMed  Google Scholar 

  36. Savettieri, G., Di Liegro, I., Catania, C., Licata, L., Pitarresi, G. L., D'agostino, S., Schiera, G., De Caro, V., Giandalia, G., Giannola, L. I., & Cestelli, A. (2000). Neurons and ECM regulate occludin localization in brain endothelial cells. Neuroreport, 11(5), 1081–1084.

    Article  CAS  PubMed  Google Scholar 

  37. Schulze, C., & Firth, J. A. (1993). Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat. Journal of Cell Science, 104(3), 773–782.

    PubMed  Google Scholar 

  38. Wolburg, H., & Lippoldt, A. (2002). Tight junctions of the blood–brain barrier: Development, composition and regulation. Vascular Pharmacology, 38(6), 323–337.

    Article  CAS  PubMed  Google Scholar 

  39. Bazzoni, G., & Dejana, E. (2004). Endothelial cell-to-cell junctions: Molecular organization and role in vascular homeostasis. Physiological Reviews, 84(3), 869–901.

    Article  CAS  PubMed  Google Scholar 

  40. Brown, R. C., & Davis, T. P. (2002). Calcium modulation of adherens and tight junction function. Stroke, 33(6), 1706–1711.

    Article  CAS  PubMed  Google Scholar 

  41. Vorbrodt, A. W., & Dobrogowska, D. H. (2003). Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers: Electron microscopist’s view. Brain Research Reviews, 42(3), 221–242.

    Article  CAS  PubMed  Google Scholar 

  42. Van Meer, G., & Simons, K. (1986). The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells. The EMBO Journal, 5, 1455–1464.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Nag, S. (2003). Morphology and molecular properties of cellular components of normal cerebral vessels. Methods in Molecular Medicine, 89, 3–36.

    CAS  PubMed  Google Scholar 

  44. Del Maschio, A., De Luigi, A., Martin-Padura, I., Brockhaus, M., Bartfai, T., Fruscella, P., et al. (1999). Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). The Journal of Experimental Medicine, 190, 1351–1356.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Tao-Cheng, J. H., Nagy, Z., & Brightman, M. W. (1987). Tight junctions of brain endothelium in vitro are enhanced by astroglia. Journal of Neuroscience, 7(10), 3293–3299.

    Article  CAS  PubMed  Google Scholar 

  46. Kojima, T., Yamamoto, T., Murata, M., Chiba, H., Kokai, Y., & Sawada, N. (2003). Regulation of the blood–biliary barrier: Interaction between gap and tight junctions in hepatocytes. Medical Electron Microscopy, 36(3), 157–164.

    Article  PubMed  Google Scholar 

  47. Simard, M., Arcuino, G., Takano, T., Liu, Q. S., & Nedergaard, M. (2003). Signaling at the gliovascular interface. Journal of Neuroscience, 23(27), 9254–9262.

    Article  CAS  PubMed  Google Scholar 

  48. Lampugnani, M. G., Corada, M., Caveda, L., Breviario, F., Ayalon, O., Geiger, B., et al. (1995). The molecular organization of endothelial cell to cell junctions: Differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). The Journal of Cell Biology, 129, 203–217.

    Article  CAS  PubMed  Google Scholar 

  49. Watabe-Uchida, M., Uchida, N., Imamura, Y., Nagafuchi, A., Fujimoto, K., Uemura, T., et al. (1998). alpha-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. Journal of Cellular Biochemistry, 142, 847–857.

    CAS  Google Scholar 

  50. Abbruscato, T. J., & Davis, T. P. (1998). Protein expression of brain endothelial cell E-cadherin after hypoxia/aglycemia: Influence of astrocyte contact. Brain Research, 842, 277–286.

    Article  Google Scholar 

  51. Farquhar, M. G., & Palade, G. E. (1963). Junctional complexes in various epithelia. The Journal of Cell Biology, 17, 375–412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., Tsukita, S., et al. (1993). Occludin: A novel integral membrane protein localizing at tight junctions. Journal of Cellular Biochemistry, 123, 1777–1788.

    CAS  Google Scholar 

  53. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K., & Tsukita, S. (1998). Claudin-1 and -2: Novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. The Journal of Cell Biology, 141, 1539.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Morita, K., Sasaki, H., Fujimoto, K., Furuse, M., & Tsukita, S. (1999). Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. The Journal of Cell Biology, 145, 579–588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Liebner, S., Fischmann, A., Rascher, G., Duffner, F., Grote, E.-H., Kalbacher, H., et al. (2000). Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathologica, 100, 323–331.

    Article  CAS  PubMed  Google Scholar 

  56. Liebner, S., Kniesel, U., Kalbacher, H., & Wolburg, H. (2000). Correlation of tight junction morphology with the expression of tight junction proteins in blood-brain barrier endothelial cells. European Journal of Cell Biology, 79, 707–717.

    Article  CAS  PubMed  Google Scholar 

  57. Lippoldt, A., Kniesel, U., Liebner, S., Kalbacher, H., Kirsch, T., Wolburg, H., et al. (2000). Structural alterations of tight junctions are associated with loss of polarity in stroke-prone spontaneously hypertensive rat blood-brain barrier endothelial cells. Brain Research, 885, 251–261.

    Article  CAS  PubMed  Google Scholar 

  58. Hirase, T., Staddon, J. M., Saitou, M., Ando-Akatsuka, Y., Itoh, M., Furuse, M., et al. (1997). Occludin as a possible determinant of tight junction permeability in endothelial cells. Journal of Cell Science, 110(Pt 14), 1603–1613.

    CAS  PubMed  Google Scholar 

  59. Dejana, E., Lampugnani, M. G., Martinez-Estrada, O., & Bazzoni, G. (2000). The molecular organization of endothelial junctions and their functional role in vascular morphogenesis and permeability. The International Journal of Developmental Biology, 44, 743–748.

    CAS  PubMed  Google Scholar 

  60. Jia, W., Martin, T. A., Zhang, G., & Jiang, W. G. (2013). Junctional adhesion molecules in cerebral endothelial tight junction and brain metastasis. Anticancer Research, 33(6), 2353–2359.

    PubMed  Google Scholar 

  61. Bauer, H. C., & Traweger Auer, H. (2004). 1-proteins of the tight junction in the blood-brain barrier. In Blood-spinal cord brain barriers health disease (pp. 1–10). San Diego: Academic.

    Google Scholar 

  62. Ando-Akatsuka, Y., Saitou, M., Hirase, T., Kishi, M., Sakakibara, A., Itoh, M., et al. (1996). Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. The Journal of Cell Biology, 133, 43–47.

    Article  CAS  PubMed  Google Scholar 

  63. Furuse, M., Sasaki, H., & Tsukita, S. (1999). Manner of interaction of heterogeneous claudin species within and between tight junction strands. The Journal of Cell Biology, 147, 891–903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. McCarthy, K. M., Skare, I. B., Stankewich, M. C., Furuse, M., Tsukita, S., Rogers, R. A., et al. (1996). Occludin is a functional component of the tight junction. Journal of Cell Science, 109(Pt 9), 2287–2298.

    CAS  PubMed  Google Scholar 

  65. Balda, M. S., Whitney, J. A., Flores, C., Gonzalez, S., Cereijido, M., & Matter, K. (1996). Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. The Journal of Cell Biology, 134, 1031–1049.

    Article  CAS  PubMed  Google Scholar 

  66. Matter, K., & Balda, M. S. (2003). Signalling to and from tight junctions. Nature Reviews. Molecular Cell Biology 2003, 4, 225–236.

    Article  CAS  PubMed  Google Scholar 

  67. Sonoda, N., Furuse, M., Sasaki, H., Yonemura, S., Katahira, J., Horiguchi, Y., et al. (1999). Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier. The Journal of Cell Biology, 147, 195–204.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Bolton, S. J., Anthony, D. C., & Perry, V. H. (1998). Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience, 86, 1245–1257.

    Article  CAS  PubMed  Google Scholar 

  69. Huber, J. D., Hau, V. S., Borg, L., Campos, C. R., Egleton, R. D., & Davis, T. P. (2002). Blood-brain barrier tight junctions are altered during a 72-h exposure to lambda-carrageenan-induced inflammatory pain. American Journal of Physiology. Heart and Circulatory Physiology, 283, H1531–H1537. https://doi.org/10.1152/ajpheart.00027.2002.

    Article  CAS  PubMed  Google Scholar 

  70. Brown, R. C., & Davis, T. P. (2005). Hypoxia/aglycemia alters expression of occludin and actin in brain endothelial cells. Biochemical and Biophysical Research Communications, 327, 1114–1123.

    Article  CAS  PubMed  Google Scholar 

  71. Heiskala, M., Peterson, P. A., & Yang, Y. (2001). The roles of claudin superfamily proteins in paracellular transport. Traffic, 2, 93–98.

    Article  CAS  PubMed  Google Scholar 

  72. Tam, S. J., & Watts, R. J. (2010). Connecting vascular and nervous system development: Angiogenesis and the blood-brain barrier. Annual Review of Neuroscience, 33, 379–408.

    Article  CAS  PubMed  Google Scholar 

  73. Nitta, T., Hata, M., Gotoh, S., Seo, Y., Sasaki, H., Hashimoto, N., Furuse, M., & Tsukita, S. (2003). Size-selective loosening of the blood-brain barrier in claudin-5–deficient mice. The Journal of Cell Biology, 161(3), 653–660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kubota, K., Furuse, M., Sasaki, H., Sonoda, N., Fujita, K., Nagafuchi, A., et al. (1999). Ca(2+)-independent cell-adhesion activity of claudins, a family of integral membrane proteins localized at tight junctions. Current Biology: CB, 9, 1035–1038.

    Article  CAS  PubMed  Google Scholar 

  75. Shin, H., Hsueh, Y. P., Yang, F. C., Kim, E., & Sheng, M. (2000). An intramolecular interaction between Src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 20, 3580–3587.

    Article  CAS  Google Scholar 

  76. Stevenson, B. R., Siliciano, J. D., Mooseker, M. S., & Goodenough, D. A. (1986). Identification of ZO-1: A high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. The Journal of Cell Biology, 103, 755–766.

    Article  CAS  PubMed  Google Scholar 

  77. Howarth, A. G., Hughes, M. R., & Stevenson, B. R. (1992). Detection of the tight junction-associated protein ZO-1 in astrocytes and other nonepithelial cell types. The American Journal of Physiology, 262, C461–C469.

    Article  CAS  PubMed  Google Scholar 

  78. Islas, S., Vega, J., Ponce, L., & Gonzalez-Mariscal, L. (2002). Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Experimental Cell Research, 274, 138–148. https://doi.org/10.1006/excr.2001.5457.

    Article  CAS  PubMed  Google Scholar 

  79. Traweger, A., Fuchs, R., Krizbai, I. A., Weiger, T. M., Bauer, H.-C., & Bauer, H. (2003). The tight junction protein ZO-2 localizes to the nucleus and interacts with the heterogeneous nuclear ribonucleoprotein scaffold attachment factor-B. The Journal of Biological Chemistry, 278, 2692–2700.

    Article  CAS  PubMed  Google Scholar 

  80. Abbruscato, T. J., Lopez, S. P., Mark, K. S., Hawkins, B. T., & Davis, T. P. (2002). Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. Journal of Pharmaceutical Sciences, 91, 2525–2538. https://doi.org/10.1002/jps.10256.

    Article  CAS  PubMed  Google Scholar 

  81. Fischer, S., Wobben, M., Marti, H. H., Renz, D., & Schaper, W. (2002). Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves. Microvascular Research, 63, 70–80.

    Article  CAS  PubMed  Google Scholar 

  82. Mark, K. S., & Davis, T. P. (2002). Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. American Journal of Physiology - Heart and Circulatory Physiology, 282, H1485.

    Article  CAS  PubMed  Google Scholar 

  83. Gottardi, C. J., Arpin, M., Fanning, A. S., & Louvard, D. (1996). The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proceedings of the National Academy of Sciences, 93, 10779–10784.

    Article  CAS  Google Scholar 

  84. Riesen, F. K., Rothen-Rutishauser, B., & Wunderli-Allenspach, H. (2002). A ZO1-GFP fusion protein to study the dynamics of tight junctions in living cells. Histochemistry and Cell Biology, 117, 307–315.

    Article  CAS  PubMed  Google Scholar 

  85. Hawkins, B. T., Abbruscato, T. J., Egleton, R. D., Brown, R. C., Huber, J. D., Campos, C. R., et al. (2004). Nicotine increases in vivo blood-brain barrier permeability and alters cerebral microvascular tight junction protein distribution. Brain Research, 1027, 48–58.

    Article  CAS  PubMed  Google Scholar 

  86. Balda, M. S., & Matter, K. (2000). The tight junction protein ZO-1 and an interacting transcription factor regulate ErbB-2 expression. The EMBO Journal, 19, 2024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Meyer, T. N., Schwesinger, C., & Denker, B. M. (2002). Zonula occludens-1 is a scaffolding protein for signaling molecules: Gα12 directly binds to the src homology 3 domain and regulates paracellular permeability in epithelial cells. The Journal of Biological Chemistry, 277, 24855–24858.

    Article  CAS  PubMed  Google Scholar 

  88. Gumbiner, B., Lowenkopf, T., & Apatira, D. (1991). Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proceedings of the National Academy of Sciences, 88, 3460–3464.

    Article  CAS  Google Scholar 

  89. Betanzos, A., Huerta, M., Lopez-Bayghen, E., Azuara, E., Amerena, J., & Gonzalez-Mariscal, L. (2004). The tight junction protein ZO-2 associates with Jun, Fos and C/EBP transcription factors in epithelial cells. Experimental Cell Research, 292, 51–66.

    Article  CAS  PubMed  Google Scholar 

  90. Umeda, K., Matsui, T., Nakayama, M., Furuse, K., Sasaki, H., Furuse, M., et al. (2004). Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. The Journal of Biological Chemistry, 279, 44785–44794.

    Article  CAS  PubMed  Google Scholar 

  91. Inoko, A., Itoh, M., Tamura, A., Matsuda, M., Furuse, M., & Tsukita, S. (2003). Expression and distribution of ZO-3, a tight junction MAGUK protein, in mouse tissues. Genes to Cells: Devoted to Molecular & Cellular Mechanisms, 8, 837–845.

    Article  CAS  Google Scholar 

  92. Yamamoto, T., Harada, N., Kawano, Y., Taya, S., & Kaibuchi, K. (1999). In vivo interaction of AF-6 with activated Ras and ZO-1. Biochemical and Biophysical Research Communications, 259, 103–107.

    Article  CAS  PubMed  Google Scholar 

  93. Zhong, Y., Enomoto, K., Tobioka, H., Konishi, Y., Satoh, M., & Mori, M. (1994). Sequential decrease in tight junctions as revealed by 7H6 tight junction-associated protein during rat hepatocarcinogenesis. Japanese Journal of Cancer Research, 85, 351–356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Fischer, S., Wiesnet, M., Marti, H. H., Renz, D., & Schaper, W. (2004). Simultaneous activation of several second messengers in hypoxia-induced hyperpermeability of brain derived endothelial cells. Journal of Cellular Physiology, 198(3), 359–369.

    Article  CAS  PubMed  Google Scholar 

  95. Thomas, F. C., Sheth, B., Eckert, J. J., Bazzoni, G., Dejana, E., & Fleming, T. P. (2004). Contribution of JAM-1 to epithelial differentiation and tight-junction biogenesis in the mouse preimplantation embryo. Journal of Cell Science, 117(23), 5599–5608.

    Article  CAS  PubMed  Google Scholar 

  96. Nagy, Z., Szabo, M., & Hüttner, I. (1985). Blood-brain barrier impairment by low pH buffer perfusion via the internal carotid artery in rat. Acta Neuropathologica, 68(2), 160–163.

    Article  CAS  PubMed  Google Scholar 

  97. Abbott, N. J., & Revest, P. A. (1991). Control of brain endothelial permeability. Cerebrovascular and Brain Metabolism Reviews, 3(1), 39–72.

    CAS  PubMed  Google Scholar 

  98. Balda, M. S., Gonzalez-Mariscal, L., Matter, K., Cereijido, M., & Anderson, J. M. (1993). Assembly of the tight junction: The role of diacylglycerol. The Journal of Cell Biology, 123(2), 293–302.

    Article  CAS  PubMed  Google Scholar 

  99. Stewart, M. P., Cabanas, C., & Hogg, N. (1996). T cell adhesion to intercellular adhesion molecule-1 (ICAM-1) is controlled by cell spreading and the activation of integrin LFA-1. The Journal of Immunology, 156(5), 1810–1817.

    CAS  PubMed  Google Scholar 

  100. Pun, P. B., Lu, J. I., & Moochhala, S. (2009). Involvement of ROS in BBB dysfunction. Free Radical Research, 43(4), 348–364.

    Article  CAS  PubMed  Google Scholar 

  101. Hawkins, B. T., & Davis, T. P. (2005). The blood-brain barrier/neurovascular unit in health and disease. Pharmacological Reviews, 57(2), 173–185.

    Article  CAS  PubMed  Google Scholar 

  102. Staddon, J. M., Herrenknecht, K., Smales, C., & Rubin, L. L. (1995). Evidence that tyrosine phosphorylation may increase tight junction permeability. Journal of Cell Science, 108(2), 609–619.

    CAS  PubMed  Google Scholar 

  103. Morita, K., Sakakibara, A., Kitayama, S., Kumagai, K., Tanne, K., & Dohi, T. (2002). Pituitary adenylate cyclase-activating polypeptide induces a sustained increase in intracellular free Ca2+ concentration and catecholamine release by activating Ca2+ influx via receptor-stimulated Ca2+ entry, independent of store-operated Ca2+ channels, and voltage-dependent Ca2+ channels in bovine adrenal medullary chromaffin cells. Journal of Pharmacology and Experimental Therapeutics, 302(3), 972–982.

    Article  CAS  PubMed  Google Scholar 

  104. Brown, R. C., Morris, A. P., & O’Neil, R. G. (2007). Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Research, 1130, 17–30.

    Article  CAS  PubMed  Google Scholar 

  105. Farshori, P., & Kachar, B. (1999). Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells. The Journal of Membrane Biology, 170(2), 147–156.

    Article  CAS  PubMed  Google Scholar 

  106. Tsukamoto, T., & Nigam, S. K. (1999). Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. American Journal of Physiology-Renal Physiology, 276(5), F737–F750.

    Article  CAS  Google Scholar 

  107. Ishizaki, T., Chiba, H., Kojima, T., Fujibe, M., Soma, T., Miyajima, H., Nagasawa, K., Wada, I., & 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. Experimental Cell Research, 290(2), 275–288.

    Article  CAS  PubMed  Google Scholar 

  108. Stevenson, M. H., & Gray, R. (1989). Effect of irradiation dose, storage time and temperature on the ESR signal in irradiated chicken bone. Journal of the Science of Food and Agriculture, 48(3), 269–274.

    Article  CAS  Google Scholar 

  109. Kurihara, H. I., Anderson, J. M., & Farquhar, M. G. (1995). Increased Tyr phosphorylation of ZO-1 during modification of tight junctions between glomerular foot processes. American Journal of Physiology-Renal Physiology, 268(3), F514–F524.

    Article  CAS  Google Scholar 

  110. Sakakibara, A., Furuse, M., Saitou, M., Ando-Akatsuka, Y., & Tsukita, S. (1997). Possible involvement of phosphorylation of occludin in tight junction formation. The Journal of Cell Biology, 137(6), 1393–1401.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Ilzecka, J. (1996). The structure and function of blood-brain barrier in ischaemic brain stroke process. In Annales Universitatis Mariae Curie-Sklodowska. Sectio D: Medicina (Vol. 51, pp. 123–127). Lublin: Uniwersytet Marii Curie-Skłodowskiej.

    Google Scholar 

  112. Morganti-Kossmann, M. C., Rancan, M., Stahel, P. F., & Kossmann, T. (2002). Inflammatory response in acute traumatic brain injury: A double-edged sword. Current Opinion in Critical Care, 8(2), 101–105.

    Article  PubMed  Google Scholar 

  113. Minagar, A., & Alexander, J. S. (2003). Blood-brain barrier disruption in multiple sclerosis. Multiple Sclerosis Journal, 9(6), 540–549.

    Article  CAS  PubMed  Google Scholar 

  114. Floris, S., Blezer, E. L., Schreibelt, G., Döpp, E., Van der Pol, S. M., Schadee-Eestermans, I. L., Nicolay, K., Dijkstra, C. D., & De Vries, H. E. (2004). Blood–brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis: A quantitative MRI study. Brain, 127(3), 616–627.

    Article  CAS  PubMed  Google Scholar 

  115. Wardlaw, J. M., Sandercock, P. A., Dennis, M. S., & Starr, J. (2003). Is breakdown of the blood-brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia? Stroke, 34(3), 806–812.

    Article  CAS  PubMed  Google Scholar 

  116. Del Zoppo, G. J., & Hallenbeck, J. M. (2000). Advances in the vascular pathophysiology of ischemic stroke. Thrombosis Research, 98(3), 73–81.

    Article  PubMed  Google Scholar 

  117. O’Donnell, M. E., Lam, T. I., Tran, L., & Anderson, S. E. (2004). The role of the blood-brain barrier Na-K-2Cl cotransporter in stroke. In Cell volume and signaling (pp. 67–75). Boston: Springer.

    Google Scholar 

  118. Heo, J. H., Han, S. W., & Lee, S. K. (2005). Free radicals as triggers of brain edema formation after stroke. Free Radical Biology & Medicine, 39(1), 51–70.

    Article  CAS  Google Scholar 

  119. Lochhead, J. J., McCaffrey, G., Sanchez-Covarrubias, L., Finch, J. D., DeMarco, K. M., Quigley, C. E., Davis, T. P., & Ronaldson, P. T. (2011). Tempol modulates changes in xenobiotic permeability and occludin oligomeric assemblies at the blood-brain barrier during inflammatory pain. American Journal of Physiology-Heart and Circulatory Physiology, 302(3), H582–H593.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Cuzzocrea, S., McDonald, M. C., Mazzon, E., Siriwardena, D., Costantino, G., Fulia, F., Cucinotta, G., Gitto, E., Cordaro, S., Barberi, I., & De Sarro, A. (2000). Effects of tempol, a membrane-permeable radical scavenger, in a gerbil model of brain injury. Brain Research, 875(1–2), 96–106.

    Article  CAS  PubMed  Google Scholar 

  121. Stamatovic, S. M., Keep, R. F., & Andjelkovic, A. V. (2008). Brain endothelial cell-cell junctions: How to “open” the blood brain barrier. Current Neuropharmacology, 6(3), 179–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Panahpour, H., Farhoudi, M., Omidi, Y., & Mahmoudi, J. (2018). An in vivo assessment of blood-brain barrier disruption in a rat model of ischemic stroke. Journal of Visualized Experiments, (133).

    Google Scholar 

  123. Gordon, Y., Partovi, S., Müller-Eschner, M., Amarteifio, E., Bäuerle, T., Weber, M. A., Kauczor, H. U., & Rengier, F. (2014). Dynamic contrast-enhanced magnetic resonance imaging: Fundamentals and application to the evaluation of the peripheral perfusion. Cardiovascular Diagnosis and Therapy, 4(2), 147.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgement

AKT gratefully acknowledges the financial support provided by the Department of Science and Technology-Science Engineering Research Board (PDF/2016/002996/LS), New Delhi, India, and Indian Institute of Technology (Banaras Hindu University), Varanasi, Uttar Pradesh for providing facility and support.

Author information

Authors and Affiliations

  1. School of Biomedical Engineering, Indian Institute of Technology (Banaras Hindu University), Varanasi, Uttar Pradesh, India

    Amit Kumar Tripathi

  2. Department of Internal Medicine, University of Iowa, Iowa City, IA, USA

    Nirav Dhanesha

  3. Department of Chemistry, University of Coimbra, Coimbra, Portugal

    Santosh Kumar

Authors
  1. Amit Kumar Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nirav Dhanesha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santosh Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. School of Biomedical Engineering, Indian Institute of Technology (Banaras Hindu University), Varanasi, Uttar Pradesh, India

    Ranjana Patnaik

  2. School of Biomedical Engineering, Indian Institute of Technology (Banaras Hindu University), Varanasi, Uttar Pradesh, India

    Amit Kumar Tripathi

  3. Department of Zoology, Banaras Hindu University, Varanasi, Uttar Pradesh, India

    Ashish Dwivedi

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Tripathi, A.K., Dhanesha, N., Kumar, S. (2019). Stroke Induced Blood-Brain Barrier Disruption. In: Patnaik, R., Tripathi, A., Dwivedi, A. (eds) Advancement in the Pathophysiology of Cerebral Stroke. Springer, Singapore. https://doi.org/10.1007/978-981-13-1453-7_3

Download citation

Publish with us

Policies and ethics

Search

Navigation