Is the pial microvessel a good model for blood-brain barrier studies?

Brain Research Reviews

Volumn 24, Issue 1, 1997, Pages 67-76

  Allt, G ^a,b   Lawrenson, J G ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b CITY UNIVERSITY   (United Kingdom)

Author keywords

Astrocyte function; Blood brain barrier; Cerebral microvessel; Electrical resistance; Electron dense tracer; Molecular characteristics; Pial microvessel; Ultrastructure

Indexed keywords

ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN MICROCIRCULATION; ELECTROPHYSIOLOGY; MICROVASCULATURE; NONHUMAN; PIA ARTERY; PRIORITY JOURNAL; REVIEW; TIGHT JUNCTION; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARIES; CEREBRAL VEINS; HUMANS;

EID: 0030848142     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0173(97)00011-8     Document Type: Review

References (78)

1. Abbott, N.J., Revest, P.A. and Romero, I.A., Astrocyte-endothelial interaction: physiology and pathology, Neuropathol. Appl. Neurobiol., 18 (1992) 424-433.
2. Andersen, D.R., Ultrastructure of meningeal sheaths. Normal human and monkey optic nerves, Arch. Ophthalmol., 82 (1969) 659-674.
3. Anderson, D.R. and Hoyt, W.F., Ultrastructure of intraorbital portion of human and monkey optic nerve, Arch. Ophthalmol., 82 (1969) 506-530.
4. Antonelli-Orlidge, A., Saunders, K.B., Smith, S.R. and D'Amore, P.A., An activated form of transforming growth factor is produced by cocultures of endothelial cells and pericytes, Proc. Natl. Acad. Sci. USA, 86 (1989) 4544-4548.
5. Bouldin, T.W. and Krigman, M.R., Differential permeability of cerebral capillary and choroid plexus to lanthanum ion, Brain Res., 99 (1975) 444-448.
6. Bradbury, M.W.B., The blood-brain barrier, Exp. Physiol., 78 (1993) 453-472.
7. Brightman, M.W., Ultrastructure of brain endothelium. In M.W.B. Bradbury (Ed.), Physiology and Pharmacology of the Blood-Brain Barrier, Springer-Verlag, Berlin, 1992, pp. 1-22.
8. Brightman, M.W., Anders, J.J. and Rosenstein, J.M., Specializations of nonneuronal cell membranes in the vertebrate nervous system, Adv. Cell. Neurobiol., 1 (1980) 3-29.
9. Brightman, M.W. and Reese, T.S., Junctions between intimately apposed cell membranes in the vertebrate brain, J. Cell Biol., 40 (1969) 648-677.
10. Brightman, M.W. and Tao-Cheng, J.H., Tight junctions of brain endothelium and epithelium. In W.M. Pardridge (Ed.), The Blood-Brain Barrier. Cellular and Molecular Biology, Raven Press, New York, 1993, pp. 107-125.
11. Broadwell, R.D., Transcytosis of macromolecules through the blood-brain barrier: a cell biological perspective and critical appraisal, Acta Neuropathol. (Berl.), 79 (1989) 117-128.
12. Bundgaard, M., Ultrastructure of frog cerebral and pial microvessels and their impermeability to lanthanum ions, Brain Res., 241 (1982) 57-65.
13. Butt, A.M. and Jones, H.C., Effect of histamine and antagonists on electrical resistance across the blood-brain barrier in rat brain-surface microvessels, Brain Res., 569 (1992) 100-105.
14. Butt, A.M., Jones, H.C. and Abbott, N.J., Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study, J. Physiol., 429 (1990) 47-62.
15. Cancilla, P.A., Bready, J. and Berliner, J., Brain endothelial-astrocyte interactions. In W.M. Pardridge (Ed.), The Blood-Brain Barrier. Cellular and Molecular Biology, Raven Press, New York, 1993, pp. 25-46.
16. Cassella, J.P., Lawrenson, J.G., Allt, G. and Firth, J.A., Ontogeny of four blood-brain barrier markers: an immunocytochemical compari-son of pial and cerebral cortical microvessels, J. Anat., 189 (1996) 407-415.
17. Cassella, J.P., Lawrenson, J.G. and Firth, J.A., Rat pial microvasculature: the incomplete expression of a blood-brain barrier? Ann. Anat., 178 (Suppl.) (1996) 54-55.
18. Cassella, J.P., Lawrenson, J.G., Lawrence, L. and Firth, J.A., Differential distribution of an endothelial barrier antigen between the pial and cortical microvessels of the rat, Brain Res., 744 (1997) 335-338.
19. Cervós-Navarro, J., Betz, E., Matakas, F. and Wüllenweber, R. (Eds.), The Cerebral Vessel Wall, Raven Press, New York, 1976, pp. 100-134, 149-156, 197-206.
20. Claude, P. and Goodenough, D.A., Fracture faces of zonulae occludentes from 'tight' and 'leaky' epithelia, J. Cell Biol., 58 (1973) 390-400.
21. Coomber, B.L. and Stewart, P.A., Morphometric analysis of CNS microvascular endothelium, Microvasc. Res., 30 (1985) 99-115.
22. Crone, C. and Olesen, S.P., Electrical resistance of brain microvascular endothelium, Brain Res., 241 (1982) 49-55.
23. Dehouck, M.-P., Méresse, S., Delorme, P., Fruchart, J.-C. and Cecchelli, R., An easier, reproducible, and mass production method to study the blood-brain barrier in vitro, J. Neurochem., 54 (1990) 1798-1801.
24. Dermietzel, R., Junctions in the central nervous system of the cat. IV. Interendothelial junctions of cerebral blood vessels from selected areas of the brain, Cell Tiss. Res., 164 (1975) 45-62.
25. Dermietzel, R. and Krause, D., Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry, Intern. Rev. Cytol., 127 (1991) 57-109.
26. Easton, A.S. and Fräser, P.A., Variable restriction of albumin diffusion across inflamed cerebral microvessels of the anaesthetized rat, J. Physiol. (Lond.), 475 (1994) 147-157.
27. Engelhardt, B. and Risau, W., Development of the blood-brain barrier. In J. Greenwood, D.J. Begley and M.B. Segal (Eds.), New Concepts of a Blood-Brain Barrier, Plenum Press, New York, 1995, pp. 11-31.
28. Fujimoto, K., Pericyte-endothelial gap junctions in developing rat cerebral capillaries: a fine structural study, Anat. Rec., 242 (1995) 562-565.
29. Goldstein, G.W., Endothelial cell-astrocyte interactions. A cellular model of the blood-brain barrier, Ann. NY Acad. Sci., 529 (1988) 31-39.
30. Goldstein, G.W. and Betz, A.L., The blood-brain barrier, Sci. Am., 255 (3) 70-79.
31. Heistad, D.D. and Kontos, H.A., Cerebral circulation. In J.T. Shepherd and F.M. Abboud (Eds.), Handbook of Physiology, Section 2: The Cardiovascular System, Vol. III, Peripheral Circulation and Organ Blood Flow, Part I, American Physiological Society, Bethesda, 1983, pp. 137-182.
32. Herman, I.M., Microvascular pericytes in development and disease. In W.M. Pardridge (Ed.), The Blood-Brain Barrier. Cellular and Molecular Biology, Raven Press, New York, 1993, pp. 127-135.
33. Janzer, R.C. and Raff, M.C., Astrocytes induce blood-brain barrier properties in endothelial cells, Nature, 325 (1987) 253-257.
34. Joó, F., Isolated brain microvessels and cultured cerebral endothelial cells in blood-brain barrier research: 20 years on. In J. Greenwood, D.J. Begley and M.B. Segal (Eds.), New Concepts of a Blood - Brain Barrier, Plenum Press, New York, 1995, pp. 229-237.
35. Kniesel, U., Reichenbach, A., Risau, W. and Wolburg, H., Quantification of tight junction complexity by means of fractal analysis, Tissue Cell, 26 (1994) 901-912.
36. Kunz, J., Krause, D., Kremer, M. and Dermietzel, R., The 140-kDa protein of blood-brain barrier-associated pericytes is identical to aminopeptidase N. J. Neurochem., 62 (1994) 2375-2386.
37. Larson, D.M., Carson, M.P. and Haudenschild, C.C., Junctional transfer of small molecules in cultured bovine brain microvascular endothelial cells and pericytes, Microvasc. Res., 38 (1987) 184-199.
38. Latker, C.H., Lynch, K.J. and Rapoport, S.I., The morphology of pial blood vessels of the frog, preserved by rapid freezing and freeze substitution, Brain Res., 375 (1986) 186-192.
39. Lawrenson, J.G., Cassella, J.P., Allt, G. and Firth, J.A., 1996, unpublished observations.
40. MacKenzie, M.L., Ghabriel, M.N. and Allt, G., Nodes of Ranvier and Schmidt-Lanterman incisures: an in vivo lanthanum tracer study, J. Neurocytol., 13 (1984) 1043-1055.
41. Martinez-Palomo, A. and Erlij, D., Structure of tight junctions in epithelia with different permeability, Proc. Natl Acad. Sci. USA, 72 (1975) 4487-4491.
42. Møllgård, K., Malinowska, D.H. and Saunders, N.R., Lack of correlation between tight junction morphology and permeability properties in developing choroid plexus. Nature, 264 (1976) 293-294.
43. Nabeshima, S., Reese, T.S., Landis, D.M.D. and Brightman, M.W., Junctions in the meninges and marginal glia, J. Comp. Neural, 164 (1975) 127-170.
44. Nagy, Z., Peters, H. and Hüttner, I., Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions, Lab. Invest., 50 (1984) 313-322.
45. Oldenorf, W.H., Cornford, M.E. and Brown, W.J., 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, Ann. Neurol, 1 (1977) 409-417.
46. Olesen, S.-P., Leakiness of rat brain microvessels to fluorescent probes following craniotomy, Acta Physiol Scand., 130 (1987) 63-68.
47. Pardridge, W.M., The Blood-Brain Barrier. Cellular and Molecular Biology, Raven Press, New York, 1993, 476 pp.
48. Pelligrino, D.A., Wang, Q., Koenig, H.M. and Albrecht, R.F., Role of nitric oxide, adenosine, N-methyl-D-aspartate receptors, and neuronal activation in hypoxia-induced pial arteriolar dilation in rats, Brain Res., 704 (1995) 61-70.
49. Rapoport, S.I., Blood-Brain Barrier in Physiology and Medicine, Raven Press, New York, 1976, pp. 101-106, 135-137.
50. Raub, T.J., Kuentzel, S.L. and Sawada, G.A., Permeability of bovine brain microvessel endothelial cells in vitro: barrier tightening by a factor released from astroglial cells, Exp. Cell Res., 199 (1992) 330-340.
51. Reese, T.S. and Karnovsky, M.J., Fine structural localization of a blood-brain barrier to exogenous peroxidase, J. Cell Biol., 34 (1967) 207-217.
52. Revest, P.A., Jones, H.C. and Abbott, N.J., Transendothelial electrical potential across pial vessels in anaesthetised rats: a study of ion permeability and transport at the blood-brain barrier, Brain Res., 652 (1994) 76-82.
53. Risau, W., Induction of blood-brain barrier endothelial cell differentiation. Ann. NY Acad. Sci., 633 (1991) 405-419.
54. Risau, W., Dingler, A., Albrecht, U., Dehouck, M.-P. and Cecchelli, R., Blood-brain barrier pericytes are the main source of γ-glutamyltranspeptidase activity in brain capillaries, J. Neurochem., 58 (1992) 667-672.
55. Rosenstein, J.M., Krum, J.M., Sternberger, L.A., Pulley, M.T. and Sternberger, N.H., Immunocytochemical expression of the endothelial barrier antigen (EBA) during brain angiogenesis, Dev. Brain Res., 66 (1992) 47-54.
56. Rubin, L.L., The blood-brain barrier in and out of cell culture, Curr. Opin. Neurobiol, 1 (1991) 360-363.
57. Rubin, L.L., Hall, D.E., Porter, S., Barbu, K., Cannon, C., Horner, H.C., Janatpour, M., Liaw, C.W., Manning, K., Morales, J., Tanner, L.I., Tomaselli, K.J. and Bard, F., A cell culture model of the blood-brain barrier, J. Cell Biol, 115 (1991) 1725-1735.
58. Sato, Y. and Rifkin, D.B., Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-β 1-like molecule by plasmin during co-culture, J. Cell Biol, 109 (1989) 309-315.
59. Schulze, C. and Firth, A.J., Interendothelial junctions during blood-brain barrier development in the rat: morphological changes at the level of individual tight junctional contacts, Dev. Brain Res., 69 (1992) 85-95.
60. Shivers, R.R., The blood-brain barrier of a reptile, Anolis caroli-nensis. A freeze-fracture study, Brain Res., 169 (1979) 221-230.
61. Shivers, R.R., Betz, A.L. and Goldstein, G.W., Isolated rat brain capillaries possess intact, structurally complex, interendothelial tight junctions; freeze-fracture verification of tight junction integrity, Brain Res., 324 (1984) 313-322.
62. Simionescu, M. and Simionescu, N. Ultrastructure of the microvas-cular wall: functional correlations. In: E.M. Renkin and C.C. Michel (Eds.), Handbook of Physiology, Section 2: The Cardiovascular System, Vol. IV, Microcirculation, Part I, American Physiological Society, Bethesda, 1984, pp. 41-101.
63. Smith, Q.R. and Rapoport, S.I., Cerebrovascular permeability coefficients to sodium, potassium, and chloride, J. Neurochem., 46 (1986) 1732-1742.
64. Sternberger, N.H. and Stemberger, L.A., Blood-brain barrier protein recognized by monoclonal antibody, Proc. Natl. Acad. Sci. USA, 84 (1987) 8169-8173.
65. Stewart, P.A. and Hayakawa, K., Early ultrastructural changes in blood-brain barrier vessels of the rat embryo, Dev. Brain Res., 78 (1994) 25-34.
66. Stewart, P.A., Hayakama, K. and Farrell, C.L., Quantitation of blood-brain barrier ultrastructure, Microsc. Res. Tech., 27 (1994) 516-527.
67. Tani, E., Yamagata, S. and Ito, Y., Freeze-fracture of capillary endothelium in rat brain, Cell Tiss. Res., 176 (1977) 157-165.
68. Tao-Cheng, J.-H., Nagy, Z. and Brightman, M.W, Tight junctions of brain endothelium in vitro are enhanced by astroglia, J. Neurosci., 7 (1987) 3293-3299.
69. Tao-Cheng, J.-H., Nagy, Z. and Brightman, M.W., Astrocytic or-thogonal arrays of intramembranous particle assemblies are modulated by brain endothelial cells in vitro, J. Neurocytol., 19 (1990) 143-153.
70. Tontsch, U. and Bauer, H.-C., Glial cells and neurons induce blood-brain barrier related enzymes in cultured cerebral endothelial cells. Brain Res., 539 (1991) 247-253.
71. Vorbrodt, A.W., Ultrastructural cytochemistry of blood-brain barrier endothelia, Prog. Histochem. Cytochem., 18 (1988) 1-99.
72. Vorbrodt, A.W., Morphological evidence of the functional polarization of brain microvascular endothelium. In: W.M. Pardridge (Ed.), The Blood-Brain Barrier. Cellular and Molecular Biology, Raven Press, New York, (1993), pp. 137-164.
73. Vorbrodt, A.W., Glycoconjugates and anionic sites in the bloodbrain barrier. In: M. Nicolini and P.F. Zatta (Eds.), Glycobiology and the Brain, Pergamon Press, Oxford, 1994, pp. 37-62.
74. Vorbrodt, A.W., Lassmann, H., Wisniewski, H.M. and Lossinsky, A.S., Ultracytochemical studies of the blood-meningeal barrier (BMB) in rat spinal cord, Acta Neuropathol. (Berl), 55 (1981) 113-123.
75. Westergaard, E., Enhanced vesicular transport of exogenous peroxidase across cerebral vessels, induced by serotonin, Acta Neuropath. (Berl.), 32 (1975) 27-42.
76. Westergaard, E., Transport of microperoxidase across segments of cerebral arterioles under normal conditions, Neuropathol. Appl. Neurobiol., 6 (1980) 267-277.
77. Westergaard, E. and Brightman, M.W., Transport of proteins across normal cerebral arterioles, J Comp. Neurol., 152 (1973) 17-44.
78. Wolburg, H., Neuhaus, J., Kniesel, U., Krauss, B., Schmid, E.-M, Öcalan, M., Farrell, C. and Risau, W., Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes, J. Cell Sci., 107 (1994) 1347-1357.