The Blood Retinal Interface: Similarities and Contrasts with the Blood-Brain Interface

Blood-Brain Barriers: From Ontogeny to Artificial Interfaces

Volumn 1, Issue , 2007, Pages 701-724

  Chan Ling, Tailoi ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Blood retinal interface; BRB properties; Choroidal vasculature; Claudin 1; Clinical determination of blood retinal barrier; Disease related response; Experimental determination of blood retinal barrier; Inner BRB (blood retinal barrier); Intraretinal blood vessels; Membrane proteins; Occluding; Outer BRB; Pericytes; Tight junctions

Indexed keywords

BRAIN INTERFACES;

BLOOD;

EID: 33847281015     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527611225.ch28     Document Type: Chapter

References (117)

1. Adams, C.W. 1977, Pathology of multiple sclerosis: progression of the lesion (review), Br. Med. Bull. 33, 15-20.
2. Alm, A., Bill, A. 1973, Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues, Exp. Eye Res. 15, 15-29.
3. Antonetti, D.A., Barber, A. J., et al. 1998, Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells, Diabetes 47, 1953-1959.
4. Ashton, N. 1970, Retinal angiogenesis in the human embryo, Brit. Med. Bull. 26, 103-106.
5. Balda, M.S., Whitney, J. A., et al. 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, J. Cell Biol. 134, 1031-1049.
6. Bauer, H., Stelzhammer, W., et al. 1999, Astrocytes and neurons express the tight junction-specific protein occludin in vitro, Exp. Cell Res. 250, 434-438.
7. Beck, D.W., Vinters, H.V., et al. 1984, Glial cells influence polarity of the bloodbrain barrier. J. Neuropathol. Exp. Neurol. 43, 219-224.
8. Beck, D.W., Roberts, R.L., et al. 1986, Glial cells influence membrane-associated enzyme activity at the blood-brain barrier, Brain Res. 381, 131-137.
9. Bellhorn, R. 1980, Permeability of the blood-ocular barriers of neonatal and adult cats to sodium fluorescein. Invest. Ophth. Vis. Sci. 1980, 870-877.
10. Bill, A., Nilsson S. 1982, The blood supply of the eye and its regulation, in Basic Aspects of Glaucoma Research, ed. E. Lutjen-Drecoll, Schattaller, Stuttgart, p. 39-48.
11. Bill, A., Nilsson S. 1985, Control of ocular blood flow, J. Cardiovasc. Pharmacol. 7[Suppl 3], S96-S102.
12. Bill, A., Sperber, G. 1990, Control of retinal and choroidal blood flow, Eye 4, 319-325.
13. Bill, A., Tornquist, P. et al. 1980, Permeability of the intraocular blood vessels, Trans. Ophth. Soc. UK 100, 332-336.
14. Bill, A., Sperber, G., et al. 1983, Physiology of the choroidal vascular bed, Int. Ophth. 6, 101-107.
15. Bolton, S. J., Anthony, D. C., et al. 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.
16. Bouchard, B. A., Shatos, M.A., et al. 1997, Human brain pericytes differentially regulate expression of procoagulant enzyme complexes comprising the extrinsic pathway of blood coagulation, Neuroscience 85, 1-9.
17. Bouchard, C., Lebert, M., et al. 1989, Are close contacts between astrocytes and endothelial cells a prerequisite condition of a blood brain barrier - the rat subfornical organ as an example, Biol. Cell 67, 159-165.
18. Brightman, M.W. 1989, The anatomic basis of the blood-brain barrier, in Implications of the Blood-Brain Barrier and its Manipulation, vol. 1, ed. E. A. Neuwelt, Plenum Medical, New York, p. 53-78.
19. Brightman, M.W., Reese, T. S. 1969, Junctions between intimately opposed cell membranes in the vertebrate brain, J. Cell Biol. 40, 648-677.
20. Brightman, M.W., Tao-Cheng, J.H. 1993, Tight junctions of brain endothelium and epithelium, in The Blood-Brain Barrier, Cellular and Molecular Biology, ed. W.M. Pardridge, Raven Press, New York, p. 107-125.
21. Broadwell, R. D. 1989, Transcytosis of macromolecules through the blood-brain barrier: a cell biological perspective and critical appraisal, Acta Neuropathol. 79, 117-128.
22. Bussow, H. 1980, The astrocytes in the retina and optic nerve head of mammals: a special glia for the ganglion cell axons, Cell Tissue Res. 206, 367-378.
23. Chan-Ling, T. 1994, Glial, neuronal and vascular interactions in the mammalian retina, in Progress in Retinal Research, vol. 13, eds. N. Osborne, G. Chader, Pergamon Press, Oxford, p. 357-389.
24. Chan-Ling, T. 1997, Glial, vascular, and neuronal cytogenesis in whole-mounted cat retina, Microsc. Res. Tech. 36, 1-16.
25. Chan-Ling, T., Stone, J. 1992, Degeneration of astrocytes in feline retinopathy of prematurity causes failure of the blood-retinal barrier, Invest. Ophth. Vis. Sci. 33, 2148-2159.
26. Chan-Ling, T., Stone, J. 1993, Retinopathy of prematurity: origins in the architecture of the retina, Prog. Retinal Res. 12, 155-177.
27. Chan-Ling, T., Halasz, P., et al. 1990, Development of retinal vasculature in the cat: processes and mechanisms, Curr. Eye Res. 9, 459-478.
28. Chan-Ling, T., Neill, A. L., et al. 1992, Early microvascular changes in murine cerebral malaria detected in retinal wholemounts, Am. J. Pathol. 140, 1121-1130.
29. Chan-Ling, T., Tout, S., et al. 1992, Vascular changes and their mechanisms in the feline model of retinopathy of prematurity, Invest. Ophth. Vis. Sci. 33, 2128-2147.
30. Chan-Ling, T., Gock, B., et al. 1995, The effect of oxygen on vasoformative cell division: evidence that physiological hypoxia is the stimulus for normal retinal vasculogenesis, Invest. Ophth. Vis. Sci. 36, 1201-1214.
31. Chan-Ling, T., McLeod, D.S., et al. 2004a, Astrocyte-endothelial cell relationships during human retinal vascular development, Invest. Ophth. Vis. Sci. 46, 2020-2032.
32. Chan-Ling, T., Page, M.P., et al. 2004b, Desmin ensheathment ratio as an indicator of vessel stability: evidence in normal development and in retinopathy of prematurity, Am. J. Pathol. 165, 1301-1313.
33. Chan-Ling, T., Hughes, S., et al. 2005, Inflammation and breakdown of the blood-retinal barrier during physiological aging in the rat retina, Neurobiol. Aging, in press.
34. Chen, Y.-H., Merzdorf, C., et al. 1997, COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos, J. Cell Biol. 138, 891-899.
35. Chu, Y., Hughes, S., et al. 2001, Differentiation and migration of astrocyte precursor cells and astrocytes in human fetal retina: relevance to optic nerve coloboma, FASEB J. 15, 2013-2015.
36. Cunha-Vaz, J. G. 1976, The blood-retinal barriers, Doc. Ophth. 41, 287-327.
37. Dehouck, M.P., Meresse, S., et al. 1990, An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro, J. Neurochem. 54, 1798-1801.
38. Dohgu, S., Takata, F., et al. 2005, Brain pericytes contribute to the induction and up-regulation of blood-brain barrier functions through transforming growth factor-beta production, Am. J. Pathol. 166, 208-215.
39. Ergun, S., Bruns, T., et al. 1997, Angioarchitecture of the human spermatic cord, Adv. Exp. Med. Biol. 424, 183-184.
40. Flage, T. 1977, Permeability properties of the tissues in the optic nerve head region in the rabbit and the monkey: an ultrastructural study, Acta Ophth. 55, 652-664.
41. Flower, R.W. 1990, Perinatal ocular physiology and ROP in the experimental animal model, Doc. Ophth. 74, 153-162.
42. Flower, R.W., Klein, G. J. 1990, Pulsatile flow in the choroidal circulation: a preliminary investigation, Eye 4, 310-318.
43. Forrester, J.V., McMenamin, P. G., et al. 1994, Localization and characterization of major histocompatibility complex class II - positive cells in the posterior segment of the eye: implications for induction of autoimmune uveoretinitis, Invest. Ophth. Vis. Sci. 35, 64-77.
44. Frank, R. N., Dutta, S., et al. 1987, Pericyte coverage is greater in the retinal than in the cerebral capillaries of the rat, J. Cell Sci. 1987, 1086-1091.
45. Frank, R. N., Turczyn, T. J., et al. 1990, Pericyte coverage of retinal and cerebral capillaries, Invest. Ophth. Vis. Sci. 31, 999-1007.
46. Frey, A., Meckelein, B., et al. 1991, Pericytes of the brain microvasculature express gamma-glutamyl transpeptidase, J. Cell Sci. 1991, 421-429.
47. Fujimoto, K. 1995, Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins: application to the immunogold labeling of intercellular junctional complexes, J. Cell Sci. 108, 3443-3449.
48. Furuse, M., Fujimoto, K., et al. 1996, Overexpression of occludin, a tight junction-associated integral membrane protein, induces the formation of intracellular multilamellar bodies bearing tight junction-like structures, J. Cell Sci. 109, 429-435.
49. Furuse, M., Fujita, K., et al. 1998, Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin, J. Cell Biol. 141, 1539-1550.
50. Furuse, M., Hirase, T., et al. 1993, Occludin: a novel integral membrane protein localizing at tight junctions [see comments], J. Cell Biol. 123, 1777-1788.
51. Furuse, M., Sasaki, H., et al. 1998, A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts, J. Cell Biol. 143, 391-401.
52. Gardner, T.W., Lieth, E., et al. 1997, Astrocytes increase barrier properties and ZO-1 expression in retinal vascular endothelial cells, Invest. Ophth. Vis. Sci. 38, 2423-2427.
53. Guy, J., Rao, N. A. 1984, Acute and chronic experimental optic neuritis: alteration in the blood-nerve barrier, Arch. Ophth. 102, 450-454.
54. Hellstrom, M., Gerhardt, H., et al. 2001, Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis, J. Cell Biol. 153, 543-553.
55. Hirase, T., Staddon, J. M., et al. 1997, Occludin as a possible determinant of tight junction permeability in endothelial cells, J. Cell Sci. 110, 1603-1613.
56. Hollander, H., Makarov, F., et al. 1991, Structure of the macroglia of the retina: sharing and division of labour between astrocytes and Muller cells, J. Comp. Neurol. 313, 587-603.
57. Hori, S., Ohtsuki, S., et al. 2004, A pericyte-derived angiopoietin-1 multimeric complex induces occludin gene expression in brain capillary endothelial cells through Tie-2 activation in vitro, J. Neurochem. 89, 503-513.
58. Hu, P., Pollard, J., et al. 1998a, Microvascular and cellular responses in the retina of rats with acute experimental allergic encephalomyelitis (EAE), Brain Pathol. 8, 487-498.
59. Hu, P., Pollard, J., et al. 1998b, Microvascular and cellular responses in the optic nerve of rats with acute experimental allergic encephalomyelitis (EAE), Brain Pathol. 8, 475-486.
60. Hu, P., Pollard, J. D., et al. 2000, Breakdown of the blood-retinal barrier induced by activated T cells of nonneural specificity, Am. J. Pathol. 156, 1139-1149.
61. Hughes, S., Chan-Ling, T. 2000, Roles of endothelial cell migration and apoptosis in vascular remodeling during development of the central nervous system, Microcirculation 7, 317-333.
62. Hughes, S., Chan-Ling, T. 2004, Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo, Invest. Ophth. Vis. Sci. 45, 2795-2806.
63. Hughes, S., Yang, H., et al. 2000, Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis, Invest. Ophth. Vis. Sci. 41, 1217-1228.
64. Janzer, R. C., Raff, M.C. 1987, Astrocytes induce blood-brain barrier properties in endothelial cells, Nature 325, 253-257.
65. Jiang, B., Bezhadian, M.A., et al. 1995, Astrocytes modulate retinal vasculogenesis: effects on endothelial cell differentiation, Glia 15, 1-10.
66. Kondo, H., Takahashi, H., et al. 1984, Immunohistochemical study of S-100 protein in the postnatal development of Muller cells and astrocytes in the rat retina, Cell Tissue Res. 238, 503-508.
67. Kunz, J., Krause, D., et al. 1994, The 140-kDa protein of blood-brain barrierassociated pericytes is identical to aminopeptidase N, Cell Tissue Res. 248, 2375-2386.
68. Lassmann, H., Rinner, W., et al. 1994, Differential role of hematogenous macrophages, resident microglia and astrocytes in antigen presentation and tissue damage during autoimmune encephalomyelitis, Neuropathol. Appl. Neurobiol. 20, 195-196.
69. Laterra, J., Guerin, C., et al. 1990, Astrocytes induce neural microvascular endothelial cells to form capillary-like structures in vitro, J. Cell. Physiol. 144, 204-215.
70. Laties, A. M., Rapoport, S. I., et al. 1979, Hypertensive breakdown of cerebral but not of retinal blood vessels in rhesus monkey, Cell Tissue Res. 233, 1511-1514.
71. Liebner, S., Fischmann, A., et al. 2000, Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme, Acta Neuropathol. 100, 323-331.
72. Ling, T., Mitrofanis, J., et al. 1989, Origin of retinal astrocytes in the rat: evidence of migration from the optic nerve, J. Comp. Neurol. 286, 345-352.
73. Ling, T. L., Stone, J. 1988, The development of astrocytes in the cat retina: evidence of migration from the optic nerve, Brain Res. Dev. Brain Res. 44, 73-85.
74. Madara, J. L. 1998, Regulation of the movement of solutes across tight junctions, Annu. Rev. Physiol. 60, 143-159.
75. Maxwell, K., Berliner, J. A., et al. 1987, Induction of gamma-glutamyl transpeptidase in cultured cerebral endothelial cells by a product released by astrocytes, Brain Res. 410, 309-314.
76. McCarthy, K. M., Skare, I. B., et al. 1996, Occludin is a functional component of the tight junction, J. Cell Sci. 109, 2287-2298.
77. Mi, H., Haeberle, H., et al. 2001, Induction of astrocyte differentiation by endothelial cells, J. Neurosci. 21, 1538-1547.
78. Michaelson, I. C. 1954, Retinal Circulation in Man and Animals, Charles C. Thomas, New York.
79. Mitic, L. L., Van Itallie, C. M., et al. 2000, Molecular physiology and pathophysiology of tight junctions I, tight junction structure and function: lessons from mutant animals and proteins, Am. J. Physiol. Gastroint. Liver Physiol. 279, G250-G254.
80. Molleston, M.C., Thomas, M.L., et al. 1993, Novel major histocompatibility complex expression by microglia and site-specific experimental allergic encephalomyelitis lesions in the rat central nervous system after optic nerve transection, Adv. Neurol. 59, 337-348.
81. 4+ oligodendrocyte precursors and astrocytes to the glial ensheathment of vessels in the rabbit myelinated streak, Glia 27, 1-14.
82. Morcos, Y., Hosie, M.J., et al. 2001, Immunolocalization of occludin and claudin-1 to tight junctions in intact CNS vessels of mammalian retina, J. Neurocytol. 30, 107-123.
83. Morita, K., Sasaki, H., et al. 1999a, Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis, J. Cell Biol. 145, 579-588.
84. Morita, K., Sasaki, H., et al. 1999b, Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells, J. Cell Biol. 147, 185-194.
85. Neill, A. L., Hunt, N.H. 1992, Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice, Parasitology 105, 165-175.
86. Olson, L., Seiger, A., et al. 1983, Intraocular transplantation in rodents: a detailed account of the procedure and examples of its use in neurobiology with special reference to brain tissue grafting, Adv. Cell. Neurobiol. 4, 407-442.
87. Penfold, P. L., Provis, J. M., et al. 1990, Angiogenesis in normal human retinal development: the involvement of astrocytes and macrophages, Arch. Clin. Exp. Ophth. 228, 255-263.
88. Pettersson, C. A. 1993, Sheaths of the spinal nerve roots: permeability and structural characteristics of dorsal and ventral spinal nerve roots of the rat, Acta Neuropathol. 85, 129-137.
89. Pollard, J. D., McCombe, P. A., et al. 1986, Class II antigen expression and T lymphocyte subsets in chronic inflammatory demyelinating polyneuropathy, J. Neuroimmunol. 13, 123-134.
90. Radius, R. L., Anderson, D.R., 1980, Distribution of albumin in the normal monkey eye as revealed by Evans Blue fluorescence microscopy, Invest. Ophth. Vis. Sci. 19, 238-243.
91. Raub, T. J., Kuentzel, S. L., et al. 1992, Permeability of bovine brain microvessel endothelial cells in vitro: barrier tightening by a factor released from astroglioma cells, Exp. Cell Res. 199, 330-340.
92. Rucker, H. K., Wynder, H. J ., et al. 2000, Cellular mechanisms of CNS pericytes. Exp. Cell Res. 207, 363-369.
93. Sakagami, K., Wu, D. M., et al. 1999, Physiology of rat retinal pericytes: modulation of ion channel activity by serum-derived molecules, J. Physiol. 521, 637-650.
94. Sandercoe, T. M., Madigan, M.C., et al. 1999, Astrocyte proliferation during development of the human retinal vasculature, Exp. Eye Res. 69, 511-523.
95. Schnitzer, J. 1988, Astrocytes in mammalian retina, in Progress in Retinal Research, ed. C. Osbourne, Pergamon Press, New York, p. 209-231.
96. Shin, T., Kojima, T., et al. 1995, The subarachnoid space as a site for precursor T cell proliferation and effector T cell selection in experimental autoimmune encephalomyelitis, J. Neuroimmunol. 56, 171-178.
97. 2+ resorption [see comment], J. Neuroimmunol. 60, 103-106.
98. Stewart, P. A., Coomber, B.L. 1986, Astrocytes and the blood-brain barrier, Astrocytes 1, 311-327.
99. Stewart, P. A., Hayakawa, E.M. 1987, Interendothelial junctional changes underlie the developmental 'tightening' of the blood-brain barrier, Brain Res. 429, 271-281.
100. Stewart, P. A., Tuor, U. I. 1994, Blood-eye barriers in the rat: correlation of ultrastructure with function, J. Comp. Neurol. 340, 566-576.
101. Stewart, P. A., Wiley, M. J. 1981, Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras, Dev. Biol. 84, 183-192.
102. Stone, J., Dreher, Z. 1987, Relationship between astrocytes, ganglion cells, and vasculature of the retina, J. Comp. Neurol. 255, 35-49.
103. Tao-Cheng, J. H., Brightman, M.W. 1988, Development of membrane interactions between brain endothelial cells and astrocytes in vitro, Int. J. Dev. Neurosci. 6, 25-37.
104. Tao-Cheng, J. H., Nagy, Z., et al. 1987, Tight junctions of brain endothelium in vitro are enhanced by astroglia, J. Neurosci. 7, 3293-3299.
105. Tilton, R. G., Miller, E. J., et al. 1985, Pericyte form and distribution in rat retinal and uveal capillaries, J. Neurosci. 9, 68-73.
106. Tontsch, U., Bauer, H.C. 1991, Glial cells and neurons induce blood-brain barrier related enzymes in cultured cerebral endothelial cells, Brain Res. 539, 247-253.
107. Tout, S., Chan-Ling, T., et al. 1993, The role of Muller cells in the formation of the blood-retinal barrier, Neuroscience 55, 291-301.
108. Tso, M.O., Shih, C.Y., et al. 1975, Is there a blood-brain barrier at the optic nerve head? Arch. Ophth. 93, 815-825.
109. Tsukita, S., Furuse, M. 1999, Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol. 9, 268-273.
110. Tsukita, S., Furuse, M. 2000, Pores in the wall: claudins constitute tight junction strands containing aqueous pores, J. Cell Biol. 149, 13-16.
111. Tyler, N. K., Burns, M.S. 1991, Comparison of lectin reactivity in the vessel beds of the rat eye, Curr. Eye Res. 10, 801-810.
112. Vorbrodt, A.W. 1993, Morphological evidence of the functional polarization of brain microvascular endothelium, in The Blood Brain Barrier, Cellular and Molecular biology, ed. W.M. Pardridge, Raven Press, New York, p. 137-164.
113. Wolburg, H., Neuhaus, J., et al. 1994, Modulation of tight junction structure in blood-brain barrier endothelial cells: effects of tissue culture, second messengers and cocultured astrocytes, J. Cell Sci. 107, 1347-1357.
114. Wolman, M., Klatzo, I., et al. 1981, Evaluation of the dye-protein tracers in pathophysiology of the blood-brain barrier, Acta Neuropathol. 54, 55-61.
115. Wong, V., Gumbiner, B.M. 1997, A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier, J. Cell Biol. 136, 399-409.
116. Wu, P., Gong, H., et al. 2000, Localization of occludin, ZO-1, and pan-cadherin in rabbit ciliary epithelium and iris vascular endothelium, Histochem. Cell Biol. 114, 303-310.
117. Yamamoto, F., Steinberg, R.H. 1992, Effects of systemic hypoxia on pH outside rod photoreceptors in the cat retina, Exp. Eye Res. 54, 699-709.