Inflammation and breakdown of the blood-retinal barrier during "physiological aging" in the rat retina: A model for CNS aging

Microcirculation

Volumn 14, Issue 1, 2007, Pages 63-76

  Chan Ling, Tailoi ^a   Hughes, Suzanne ^a   Baxter, Louise ^a   Rosinova, Emelia ^a   McGregor, Iain ^a   Morcos, Yvette ^a   van Nieuwenhuyzen, Petra ^a   Hu, Ping ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Antigen presentation; Blood brain barrier; Blood retinal barrier; Inflammation; Microglia; Neurodegeneration; Retina

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OCCLUDIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BLOOD RETINA BARRIER; CENTRAL NERVOUS SYSTEM; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MALE; MICROGLIA; MONOCYTE; NONHUMAN; PATHOGENESIS; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT; RAT STRAIN; RETINA; SHORT TERM MEMORY; T LYMPHOCYTE ACTIVATION; TISSUE SECTION;

AGING; ANIMALS; ANTIBODIES; BLOOD-BRAIN BARRIER; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; ECTODYSPLASINS; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HORSERADISH PEROXIDASE; INDICATORS AND REAGENTS; INDOLES; INFLAMMATION; MALE; MEMBRANE PROTEINS; MICROCIRCULATION; MICROGLIA; MONOCYTES; ORGANOMETALLIC COMPOUNDS; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RETINAL VESSELS; T-LYMPHOCYTES; TIGHT JUNCTIONS;

RATTUS; RATTUS NORVEGICUS;

EID: 33847284576     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1080/10739680601073451     Document Type: Article

References (77)

1. Akiyama, H., Barger, S., Barnum, S., Bradit, B., Bauer, J., Cole, G. M., Cooper, N. R., Eikelenboom, P., Emmerling, M., Fiebich, B. L., Finch, C. E., Frauutschy, S., Griffin, W ST, Hampel, H., Hull, M., Landreth, G., Lue, L. F., Mrak, R., Mackenzie, I. R., McGeer, P. L., O'Banion, M. K., Pachter, J., Pasinetti, G., Plata-Salaman, C., Rogers, J., Rydel, R., Shen, Y., Streit, W., Strohmeyer, R., Tooyoma, I., Van Muiswinkel, F. L., Veerhuis, R., Walker, D., Webster, S., Wegrzyniak, B., Wenk, G. and Wyss-Coray, T. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging, 21, pp. 383-421.
2. Alba, C., Vidal, L., Diaz, F., Villena, A. and de Vargas, I. P. (2004) Ultrastructural and quantitative age-related changes in capillaries of the dorsal lateral geniculate nucleus. Brain Res Bull, 64, pp. 145-153.
3. Alberghina, M., Lupo, G., Anfuso, C. and Moro, F. (1993) Palmitate transport through the blood-retina and blood-brain barrier of rat visual system during aging. Neurosci Lett, 150, pp. 17-20.
4. Beare, N. A., Southern, C., Chalira, C., Taylor, T. E., Molyneux, M. E. and Harding, S. P. (2004) Prognostic significance and course of retinopathy in children with severe malaria. Arch Ophthalmol, 122, pp. 1141-1147.
5. Beazley, L. D., Perry, V. H., Baker, B. and Darby, J. E. (1987) An investigation into the role of ganglion cells in the regulation of division and death of other retinal cells. Brain Res, 430, pp. 169-184.
6. Bhutto, I. A. and Amemiya, T. (1995) Retinal vascular changes during aging in Wistar Kyoto rats: Application of corrosion cast and scanning electron microscopy. Ophthalmic Res, 27, pp. 249-261.
7. Burns, E. M., Kruckeberg, T. W. and Gaetano, P. K. (1981) Changes with age in cerebral capillary morphology. Neurobiol Aging, 2, pp. 283-291.
8. Cagnin, A., Brooks, D. J., Kennedy, A. M., Gunn, R. N., Myers, R., Turkheimer, F. E., Jones, T. and Banati, R. B. (2001) In-vivo measurement of activated microglia in dementia. Lancet, 358, pp. 461-467.
9. Chan-Ling, T. (1997) Glial, vascular, and neuronal cytogenesis in whole-mounted cat retina. Microsc Res Tech, 36, pp. 1-16.
10. Chan-Ling, T. (2006) The blood-retinal interface: Similarities and contrasts with the blood-brain barrier. Blood-Brain Interfaces: From Ontogeny to Artificial Barriers, pp. 701-724. Wiley-VCH, Weinheim
11. Chan-Ling, T., Neill, A. L. and Hunt, N. H. (1992) Early microvascular changes in murine cerebral malaria detected in retinal wholemounts. Am J Pathol, 140, pp. 1121-1130.
12. Chan-Ling, T., Tout, S., Hollander, H. and Stone, J. (1992) Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci, 33, pp. 2128-2147.
13. Claudio, L. (1996) Ultrastructural features of the blood-brain barrier in biopsy tissue from Alzheimer's disease patients. Acta Neuropathol (Berl), 91, pp. 6-14.
14. Cullen, K. M., Kocsi, Z. and Stone, J. (2005) Pericapillary haem-rich deposits: Evidence for microhaemorrhages in aging human cerebral cortex. J Cereb Blood Flow Metab, 25, pp. 1656-1667.
15. Davies, D. C. and Hardy, J. A. (1988) Blood-brain barrier in ageing and Alzheimer's disease. Neurobiol Aging, 9, pp. 46-48.
16. de Jong, G. I., de Weerd, H., Schuurman, T., Traber, J. and Luiten, P. G. (1990) Microvascular changes in aged rat forebrain: Effects of chronic nimodipine treatment. Neurobiol Aging, 11, pp. 381-389.
17. Dermietzel, R., Spray, D. C. and Needergard, M. (2006) Blood-Brain Interfaces: From Ontogeny to Artificial Barriers, Wiley-VCH, Weinheim
18. Dijkstra, C. D., Dopp, E. A., Joling, P. and Kraal, G. (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: Distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology, 54, pp. 589-599.
19. Ennaceur, A. and Delacour, J. (1988) A new one-trial test for neurobiological studies of memory in rats, 1: Behavioral data. Behav Brain Res, 31, pp. 47-59.
20. Everitt, A. V. (2003) Food restriction, pituitary hormones and ageing. Biogerontology, 4, pp. 47-50.
21. Farkas, E. and Luiten, P. G. (2001) Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol, 64, pp. 575-611.
22. Felzien, L. K., McDonald, J. T., Gleason, S. M., Berman, N. E. and Klein, R. M. (2001) Increased chemokine gene expression during aging in the murine brain. Brain Res, 890, pp. 137-146.
23. Frank, M. G., Barrientos, R. M., Biedenkapp, J. C., Rudy, J. W., Watkins, L. R. and Maier, S. F. (2006) mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol Aging, 27, pp. 712-722.
24. Hartwig, M. (1995) Immune ageing and Alzheimer's disease. Neuroreport, 6, pp. 1274-1276.
25. Hassler, O. (1965) Vascular changes in senile brains: A micro-angiographic study. Acta Neuropathologica (Berl)., 5, pp. 40-53.
26. Hicks, P., Rolsten, C., Brizzee, D. and Samorajski, T. (1983) Age-related changes in rat brain capillaries. Neurobiol Aging, 4, pp. 69-75.
27. Hosokawa, M. and Ueno, M. (1999) Aging of blood-brain barrier and neuronal cells of eye and ear in SAM mice. Neurobiol Aging, 20, pp. 117-123.
28. Pollard, J., Hunt, N. and Chan-Ling, T. (1998) Microvascular and cellular responses in the retina of rats with acute experimental allergic encephalomyelitis (EAE). Brain Pathol, 8, pp. 487-498.
29. Pollard, J., Hunt, N., Taylor, J. and Chan-Ling, T. (1998) Microvascular and cellular responses in the optic nerve of rats with acute experimental allergic encephalomyelitis (EAE). Brain Pathol, 8, pp. 475-486.
30. Pollard, J. D. and Chan-Ling, T. (2000) Breakdown of the blood-retinal barrier induced by activated T cells of nonneural specificity. Am J Pathol, 156, pp. 1139-1149.
31. Hughes, S. and Chan-Ling, T. (2000) Roles of endothelial cell migration and apoptosis in vascular remodeling during development of the central nervous system. Microcirculation, 7, pp. 317-333.
32. Hughes, S., Gardiner, T., Baxter, L., Rosinova, E. and Chan-ling, T. (2006) Altered pericyte-endothelial relations in the rat retina during aging: Implications for vessel stability. Neurobiol Aging, 27, pp. 1838-1847.
33. Hunig, T., Wallny, H. J., Hartley, J. K., Lawetzky, A. and Tiefenthaler, G. (1989) A monoclonal antibody to a constant determinant of the rat T cell antigen receptor that induces T cell activation: Differential reactivity with subsets of immature and mature T lymphocytes. J Exp Med, 169, pp. 73-86.
34. Lai, Y. L., Jacoby, R. O. and Jonas, A. M. (1978) Age-related and light-associated retinal changes in Fischer rats. Invest Ophthalmol Vis Sci, 17, pp. 634-638.
35. Leuenberger, P. M. (1973) Ultrastructure of the ageing retinal vascular system, with special reference to quantitative and qualitative changes of capillary basement membranes. Gerontologia., 19, pp. 1-15.
36. Ling, T. L. and Stone, J. (1988) The development of astrocytes in the cat retina: Evidence of migration from the optic nerve. Brain Res Dev Brain Res, 44, pp. 73-85.
37. Lukaszewska, I. and Radulska, A. (1994) Object recognition is not impaired in old rats. Acta Neurobiol Exp (Warsz), 54, pp. 143-150.
38. Mackic, J. B., Bading, J., Ghiso, J., Walker, L., Wisniewski, T., Frangione, B. and Zlokovic, B. V. (2002) Circulating amyloid-beta peptide crosses the blood-brain barrier in aged monkeys and contributes to Alzheimer's disease lesions. Vascul Pharmacol, 38, pp. 303-313.
39. McGeer, E. G. and McGeer, P. L. (2003) Inflammatory processes in Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry, 27, pp. 741-749.
40. McMenamin, P. G. and Forrester, J. V. (2001) Dendritic cells in the eye. Dendritic Cells, pp. 398-409. Academic Press, San Diego
41. Michel, C. C. and Curry, F. E. (1999) Microvascular permeability. Physiol Rev, 79, pp. 703-761.
42. Mitchell, P., Wang, J. J., Wong, T. Y., Smith, W., Klein, R. and Leeder, S. R. (2005) Retinal microvascular signs and risk of stroke and stroke mortality. Neurology, 65, pp. 1005-1009.
43. Moody, D. M., Santamore, W. P. and Bell, M. A. (1991) Does tortuosity in cerebral arterioles impair down-autoregulation in hypertensives and elderly normotensives? A hypothesis and computer model. Clin Neurosurg, 37, pp. 372-387.
44. Mooradian, A. D. (1994) Potential mechanisms of the age-related changes in the blood-brain barrier. Neurobiol Aging, 15, pp. 751-755.
45. Mooradian, A. D., Grabau, G. and Uko-eninn, A. (1993) In situ quantitative estimates of the age-related and diabetes-related changes in cerebral endothelial barrier antigen. Brain Res, 609, pp. 41-44.
46. Mooradian, A. D., Haas, M. and Chehade, J. (2003) Age-related changes in rat cerebral occludin and zonula occludens-1 (ZO-1). Mech Ageing Dev, 124, pp. 143-146.
47. Mooradian, A. D. and McCuskey, R. S. (1992) In vivo microscopic studies of age-related changes in the structure and the reactivity of cerebral microvessels. Mech Ageing Dev, 64, pp. 247-254.
48. Morcos, Y., Hosie, M. J., Bauer, H. C. and Chan-Ling, T. (2001) Immunolocalization of occludin and claudin-1 to tight junctions in intact CNS vessels of mammalian retina. J Neurocytol, 30, pp. 107-123.
49. Morley, K. C., Gallate, J. E., Hunt, G. E., Mallet, P. E. and McGregor, I. S. (2001) Increased anxiety and impaired memory in rats 3 months after administration of 3,4-methylenedioxymethamphetamine ("ecstasy"). Eur J Pharmacol, 43, pp. 91-99.
50. Nagata, M., Katz, M. and Robinson, W. J. (1986) Age-related thickening of retinal capillary basement membranes. Invest Ophthalmol Vis Sci, 27, pp. 437-440.
51. Neill, A. L., Chan, L. T. and Hunt, N. H. (1993) Comparisons between microvascular changes in cerebral and non-cerebral malaria in mice, using the retinal whole-mount technique. Parasitology, 107, pp. 477-487.
52. Neill, A. L. and Hunt, N. H. (1992) Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice. Parasitology, 105, pp. 165-175.
53. Ogura, K., Ogawa, M. and Yoshida, M. (1994) Effects of ageing on microglia in the normal rat brain: Immunohistochemical observations. Neuroreport, 5, pp. 1224-1226.
54. Patton, N., Aslam, T., MacGillivray, T., Pattie, A., Deary, I. J. and Dhillon, B. (2005) Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: A rationale based on homology between cerebral and retinal microvasculatures. J Anat, 206, pp. 319-348.
55. Peinado, M. A., Quesada, A., Pedrosa, J. A., Torres, M. I., Martinez, M., Esteban, F. J., Moral, M L del, Hernandez, R., Rodrigo, J. and Peinado, J. M. (1998) Quantitative and ultrastructural changes in glia and pericytes in the parietal cortex of the aging rat. Microsc Res Tech, 43, pp. 34-42.
56. Perry, E. and Kay, D. W. (1997) Some developments in brain ageing and dementia. Br J Biomed Sci, 54, pp. 201-215.
57. Perry, V. H., Matyszak, M. K. and Fearn, S. (1993) Altered antigen expression of microglia in the aged rodent CNS. Glia, 7, pp. 60-67.
58. Peyman, G. and Bok, D. (1972) Peroxidase diffusion in the normal and laser-coagulated primate retina. Invest Ophthalmol Vis Sci, 11, pp. 35-45.
59. Prickaerts, J., de Vente, J., Honig, W., Steinbusch, H. W. and Blokland, A. (2002) CGMP, but not cAMP, in rat hippocampus is involved in early stages of object memory consolidation. Eur J Pharmacol, 436, pp. 83-87.
60. Rapoport, S. I., Ohno, K. and Pettigrew, K. D. (1979) Blood-brain barrier permeability in senescent rats. J Gerontology, 34, pp. 162-169.
61. Rudick, R. A. and Buell, S. J. (1983) Integrity of blood-brain barrier to peroxidase in senescent mice. Neurobiol Aging, 4, pp. 283-287.
62. Schellini, S. A., Gregorio, E. A., Padovani, C. R., Spadella, C. T. and Moraes-Silva, M. A. (1997) Ultrastructural and morphometric aspects of ageing in the retinal capillaries of rats. J Submicrosc Cytol Pathol, 29, pp. 275-280.
63. Shakib, M. and Cunha-Vaz, J. G. (1966) Studies on the permeability of the blood-retinal barrier, IV: Junctional complexes of the retinal vessels and their role in the permeability of the blood-retinal barrier. Exp Eye Res, 5, pp. 229-234.
64. Sheffield, L. G. and Berman, N. E. (1998) Microglial expression of MHC class II increases in normal aging of nonhuman primates. Neurobiol Aging, 19, pp. 47-55.
65. Skoog, I., Wallin, A., Fredman, P., Hesse, C., Aevarsson, O., Karlsson, I., Gottfries, C. G. and Blennow, K. (1998) A population study on blood-brain barrier function in 85-year-olds: Relation to Alzheimer's disease and vascular dementia. Neurology, 50, pp. 966-971.
66. Stewart, P. A., Hayakawa, K., Akers, M. A. and Vinters, H. V. (1992) A morphometric study of the blood-brain barrier in Alzheimer's disease. Lab Invest, 67, pp. 734-742.
67. Stewart, P. A., Magliocco, M., Hayakawa, K., Farrellk, C. L., Maestro, R F Del, Girvin, J., Kaufmann, J CE, Vinters, H. V. and Gilbert, J. (1987) A quantitative analysis of blood-brain barrier ultrastructure in the aging human. Microvasc Res, 33, pp. 270-282.
68. Styren, S. D., Civin, W. H. and Rogers, J. (1990) Molecular, cellular, and pathologic characterization of HLA-DR immunoreactivity in normal elderly and Alzheimer's disease brain. Exp Neurol, 110, pp. 93-104.
69. Terao, A., Apte-Deshpande, A., Dousman, L., Morairty, S., Eynon, B., Kilduff, T. and Freund, Y. (2002) Immune response gene expression increases in the aging murine hippocampus. J Neuroimmunol, 132, pp. 99-112.
70. Thumwood, C. M., Hunt, N. H., Clark, I. A. and Cowden, W. B. (1988) Breakdown of the blood-brain barrier in murine cerebral malaria. Parasitology, 96, pp. 579-589.
71. Topple, A., Fifkova, E., Baumgardner, D. and Cullen-Dockstader, K. (1991) Effect of age on blood vessels and neurovascular appositions in the CA1 region of the rat hippocampus. Neurobiol Aging, 12, pp. 211-217.
72. Topple, A., Fifkova, E. and Cullen-Dockstader, K. (1990) Effect of age on blood vessels and neurovascular appositions in the rat dentate fascia. Neurobiol Aging, 11, pp. 371-380.
73. Vannucchi, M. G., Scali, C., Kopf, S. R., Pepeu, G. and Casamenti, F. (1997) Selective muscarinic antagonists differentially affect in vivo acetylcholine release and memory performances of young and aged rats. Neuroscience, 79, pp. 837-846.
74. Vorbrodt, A. W. and Dobrogowska, D. H. (1994) Immunocytochemical evaluation of blood-brain barrier to endogenous albumin in adult, newborn and aged mice. Folia Histochem Cytobiol, pp. 63-70.
75. Weisse, I. (1995) Changes in the aging rat retina. Ophthalmic Res, 27, pp. 154-163.
76. Willig, F., Palacios, A., Monmaur, P., M'Harzi, M., Laurent, J. and Delacour, J. (1987) Short-term memory, exploration and locomotor activity in aged rats. Neurobiol Aging, 8, pp. 393-402.
77. Wong, T. Y., Klein, R., Sharrett, A. R., Nieto, F. J., Boland, L. L., Couper, D. J., Mosley, T. H., Klein, B. E., Hubbard, L. D. and Szklo, M. (2002) Retinal microvascular abnormalities and cognitive impairment in middle-aged persons: The Atherosclerosis Risk in Communities Study. Stroke., 33, pp. 1487-1492.