Inflammation and Breakdown of the Blood–Retinal Barrier During “Physiological Aging” in the Rat Retina: A Model for CNS Aging

REFERENCES

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