Publication: Macroglial and retinal changes in hypercholesterolemic rabbits after normalization of cholesterol levels
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2006-09-26
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Hoz Montañana, María Rosa de
Ruiz, Emilio
Tejerina Sánchez, Teresa
Ramirez Sebastian, Jose Manuel
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Elsevier
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Abstract
This study evaluates hypercholesterolemic rabbits, examining the retinal changes in Müller cells and astrocytes as well as their variations after a period of normal blood-cholesterol values induced by a standard diet. New Zealand rabbits were divided into three groups: G0, fed a standard diet; G1A, fed a 0.5% cholesterol-enriched diet for 8 months; and G1B, fed as G1A followed by standard diet for 6 months. Eyes were processed for transmission electron microscopy and immunohistochemistry (GFAP). While G1B resembled G0 more than did G1A, they shared alterations with G1A: a) as in G1A, Müller cells were GFAP+, filled spaces left by axonal degeneration, formed glial scars and their nuclei were displaced to the nerve-fibre layer. The area occupied by the astrocytes associated with the nerve-fibre bundles (AANFB) and by perivascular astrocytes (PVA) in G1A and G1B was significantly lower than in controls. However, no significant differences in PVA were found between G1A and G1B. In G1B, type I PVA was absent and replaced by hypertrophic type II cells; b) Bruch's membrane (BM) was thinner in G1B than in G1A; c) the retinal pigment epithelium (RPE) cytoplasm contained fewer lipids in G1B than in G1A; d) in G1A and G1B choriocapillaris and retinal vessel showed alterations with respect to G0; e) cell death and axonal degeneration in the retina were similar in G1A and G1B. The substitution of a hyperlipemic diet by a standard one normalizes blood-lipid levels. However, the persistence of damage at retinal vessels and BM-RPE could trigger chronic ischemia.
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Received 4 May 2006; accepted in revised form 22 July 2006
Available online 26 September 2006
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- Agardh, E., Bruun, A., Agardh, C.D., 2001. Retinal glial cell immunoreactivity and neuronal cell changes in rats with STZ-induced diabetes. Curr. Eye Res. 23, 276e284.
- Amaratunga, A., Abraham, C.R., Edwards, R.B., Sandell, J.H., Schreiber, B.M., Fine, R.E., 1996. Apolipoprotein E is synthesized in the retina by Mu¨ller glial cells, secreted into the vitreous, and rapidly transported into the optic nerve by retinal ganglion cells. J. Biol. Chem. 271, 5628e5632.
- Baskin, F., Smith, G.A., Fosmire, J.A., Rosenberg, R.N., 1997. Altered apolipoprotein E secretion in cytokine treated human astrocytes cultures. J. Neurol. Sci. 148, 15e18.
- Berring, E.E., Borrenpohl, K., Fliesler, S.J., Serfis, A.B., 2005. A comparison of the behavior of cholesterol and selected derivatives in mixed sterolphospholipid Langmuir monolayers: a fluorescence microscopy study. Chem. Phys. Lipids 136, 1e12.
- Bringmann, A., Uckermann, O., Pannicke, T., Iandiev, I., Reichenbach, A., Wiedemann, P., 2005. Neuronal versus glial cell swelling in the ischaemic retina. Acta Ophthalmol. Scan. 83, 528e538.
- Chan-Ling, T., Stone, J., 1992. Degeneration of astrocytes in feline retinopathy of prematurity causes failure of the blood-retinal barrier. Invest. Ophthalmol. Vis. Sci. 33, 2148e2159.
- Cook, D.R., Wisniewski, H.M., 1973. The role of the oligodendroglia and astroglia in wallerian degeneration of the optic nerve. Brain Res. 61, 191e206.
- Eisenfeld, A.J., Bunt-Milam, A.H., Sarthy, P.V., 1984. Mu¨ller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Invest. Ophthalmol. Vis. Sci. 25, 1321e1328.
- Erickson, P.A., Fisher, S.R., Guerin, C.J., Anderson, D.H., Kaska, D.D., 1987. Glial fibrillary acidic protein increases in Mu¨ller cells after retinal detachment. Exp. Eye Res. 44, 37e48.
- Fliesler, S.J., Richards, M.J., Peachey, N.S., Kauser, K., 2000. Hypercholesterolemia does not alter retinal sterol composition or compromise retinal structure or function in apolipoprotein E (ApoE)-knockout mice. Invest. Ophthalmol. Vis. Sci. 41 (4), S199.
- Gordon, W.C., Bazan, N.G., 1997. Retina. In: Harding, J.J. (Ed.), Biochemistry of the Eye, first ed. Chapman and Hall, London, pp. 144e275.
- Goritz, C., Mauch, D.H., Pfrieger, F.W., 2005. Multiple mechanisms mediate cholesterol-induced synaptogenesis in a CNS neurons. Mol. Cell. Neurosci. 29, 190e201.
- Guerin, C.J., Anderson, D.H., Fisher, S.K., 1990. Changes in intermediate filament immunolabeling occur in response to retinal detachment and reattachment in primates. Invest. Ophthalmol. Vis. Sci. 31, 1474e1482.
- Guidry, C., Medeiros, N.E., Curcio, C.A., 2002. Phenotypic variation of retinal pigment epithelium in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 43, 267e273.
- Haddad, A., Ramírez, A.I., Laicine, E.M., Salazar, J.J., Triviño, A., Ramírez, J.M., 2001. Immmunohistochemistry in association with scanning electron microscopy for the morphological characterization and location of astrocytes of the rabbit retina. J. Neurosci. Methods 106, 131e137.
- Haddad, A., Salazar, J.J., Laicine, E.M., Ramírez, A.I., Ramírez, J.M., Triviño, A., 2003. A direct contact between astrocyte and vitreous body is possible in the rabbit eye due to discontinuities in the basement membrane of the retinal inner limiting membrane. Braz. J. Med. Biol. Res. 36, 207e211.
- Iadecola, C., 1999. Mechanisms of cerebral ischemic damage. In: Walz, W. (Ed.), Cerebral Ischemia: Molecular and Cellular Pathophysiology. Humana Press Inc, Totowa, pp. 3e32.
- Johnson, N.F., 1974. Effects of acute ischaemia on the structure of the rabbit retina. Trans. Ophthalmol. Soc. UK 94, 394e405.
- Kettenmann, H., Faissner, A., Trotter, J., 1996. Neuron-glia interactions in homeostasis and degeneration. In: Greger, R.,Windhorst, U. (Eds.), Comprehensive Human Physiology. From Cellular Mechanisms to Integration. Springer-Verlag, Berlin, pp. 533e543.
- Landis, D.M.D., 1994. The early reactions of non-neuronal cells to brain injury. Annu. Rev. Neurosci. 17, 133e151.
- Laping, N.J., Teter, B., Nichols, N.R., Rozovsky, I., Finch, C.E., 1994. Glial fi- brillary acidic protein: regulation by hormones, cytokines, and growth factors. Brain Pathol 1, 259e275.
- Lewis, G.P., Guerin, C.J., Anderson, D.H., Matsumoto, B., Fisher, S.K., 1994. Rapid changes in the expression of glial cell proteins caused by experimental retinal detachment. Am. J. Ophthalmol. 118, 368e376.
- Lindsey, R.M., 1986. Reactive gliosis. In: Fedoroff, S., Vernadakis, A. (Eds.), Astrocytes, vol. 3. Academic Press, Orlando, pp. 231e262.
- Liu, D., Smith, C.L., Barone, F.C., Ellison, J.A., Lysco, P.G., Li, K., Simpson, I.A., 1999. Astrocytic demise precedes delayed neuronal death in focal ischemic rat brain. Mol. Brain Res. 68, 29e41.
- Madigan, M.C., Penfold, P.L., Provis, J.M., Balind, T.K., Billson, F.A., 1994. Intermediate filament expression in human retinal macroglia. Histopathologic changes associated with age-related macular degeneration. Retina 14, 65e74.
- Mahley, R.W., 1988. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622e630.
- Mano, T., Puro, D.G., 1990. Phagocytosis by human retinal glial cells in culture. Invest. Ophthalmol. Vis. Sci. 31, 1047e1055.
- Marshall, J., Hussain, A.A., Starita, C., Moore, D.J., Patmore, A.L., 1998. Aging and Bruch’s membrane. In: Marmor, M.F., Wolfnsberger, T.J. (Eds.), The Retinal Pigment Epithelium. Oxford University, New York, pp. 669e692.
- Mizutani, M., Gerhardinger, C., Lorenzi, M., 1998. Mu¨ller cell changes in human diabetic retinopathy. Diabetes 47, 445e449.
- Murabe, Y., Ibata, Y., Sano, Y., 1982. Morphological studies on neuroglia. IV. Proliferative response of non-neuronal elements in the hippocampus of the rat to kainic acid-induced lesions. Cell. Tissue Res. 222, 223e226.
- Nieto-Sampedro, M., Verdu´, E., 1998. Lesiones del sistema nervioso: respuesta neuronal y reparacio´n. In: Delgado, J.M., Ferru´s, A., Mora, F., Rubia, F.J. (Eds.), Manual de neurociencia. Editorial Sı´ntesis S.A., Madrid, pp. 929e969.
- Norton, W.T., Aquino, D.A., Hozumi, I., Chiu, F.-C., Brosnan, C.F., 1992. Quantitative aspects of reactive gliosis: a review. Neurochem. Res. 17, 877e885.
- Okada, M., Matsumura, M., Ogino, N., Honda, Y., 1990. Mu¨ller cells in detached human retina express glial fibrillary acidic protein and vimentin. Graef. Arch. Clin. Exp. Ophthalmol. 228, 467e474.
- Ong, J.M., Zorapapel, N.C., Rich, K.A., Wagstaff, R.E., Lambert, R.W., Rosenberg, S.E., Moghaddas, F., Pirouzmanesh, A., Aoki, A.M., Kenney, C., 2001. Effects of cholesterol and Apolipoprotein E on retinal abnormalities in ApoE-deficient mice. Invest. Ophthalmol. Vis. Sci. 42, 1891e1900.
- Pannicke, T., Uckermann, O., Iandiev, I., Wiedemann, P., Reichenbach, A., Bringmann, A., 2005. Ocular inflammation alters swelling and membrane characteristic of rat Mu¨ller glial cells. J. Neuroimmunol. 161, 145e154.
- Penfold, P.L., Provis, J.M., 1986. Cell death in the development of the human retina: phagocitosis of pyknotic and apoptotic bodies by retinal cells. Graef. Arch. Clin. Exp. 228, 255e263.
- Ramírez, J.M., Triviño, A., Ramírez, A.I., Salazar, J.J., García-Sánchez, J., 1994. Immunohistochemical study of human retinal astroglia. Vis. Res. 34, 1935e1946.
- Ramírez, J.M., Triviño, A., Ramírez, A.I., Salazar, J.J., García-Sánchez, J., 1996. Structural specializations of human retinal glial cells. Vis. Res. 36, 2029e2036.
- Ramírez, J.M., Ramírez, A.I., Salazar, J.J., De Hoz, R., Triviño, A., 2001. Changes of astrocytes in retinal ageing and age-related macular degeneration. Exp. Eye Res. 73, 601e615.
- Reier, P.J., 1986. Gliosis following CNS injury: the anatomy of astrocytic scars and their influences on axonal elongation. In: Fedoroff, S., Vernadakis, A. (Eds.), Astrocytes, Vol. 3. Academic. Press, Orlando, pp. 263e324.
- Reynolds, E.S., 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell. Biol. 17, 208e212.
- Ridet, J.L., Malhotra, S.K., Privat, A., Gage, F.H., 1997. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20, 570e577.
- Rivard, A., Fabre, J.-E., Silver, M., Chen, D., Murohara, T., Kearney, M., Magner, M., Asahara, T., Isner, J.M., 1999. Age-dependent impairment of angiogenesis. Circulation 99, 111e120.
- Rungger-Bra¨ndle, E., Leuenberger, P.M., 1997. Senile retinal deficiencies in astrocytes and blood vessels. In: LaVail, M.M., Hollyfield, J.G., Anderson, R.E. (Eds.), Degenerative Retinal Diseases. Plenum Press, New York, pp. 409e415.
- Rungger-Brändle, E., Dosso, A.A., Leuenberger, P.M., 2000. Glial reactivity, an early feature of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 41, 1971e1980.
- SanGiovanni, J.P., Chew, E.Y., 2005. The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog. Ret. Eye Res. 24, 87e138.
- Sarthy, V., Brodjian, S.J., Smith, S., 1997. Ciliary neurotrophic factor (CNTF) induces reactive gliosis and GFAP gene expression in Mu¨ller cells. Invest. Ophthalmol. Vis. Sci. 38, S590.
- Sarthy, P.V., Fu, M., 1989. Transcriptional activation of an intermediate filament protein gene in mice with retinal dystrophy. DNA J. Mol. Cell. Biol. 8, 437e446.
- Sarthy, V., Ripps, H., 2001. The Retinal Mu¨ller Cell: Structure and Function. Kluwer Academic/Plenum Publishers, New York.
- Stone, J., Dreher, Z., 1987. Relationship between astrocytes, ganglion cells and vasculature of the retina. J. Comp. Neurol. 255, 35e49.
- Tanihara, H., Hangai, M., Sawaguchi, S., Abe, H., Kageyama, M., Nakazawa, F., Shirasawa, E., Honda, Y., 1997. Up-regulation of glial fibrillary acidic protein in the retina of primate eyes with experimental glaucoma. Arch. Ophthalmol. 115, 752e756.
- Triviño, A., Ramírez, J.M., Ramírez, A.I., Salazar, J.J., García Sánchez, J., 1992. Retinal perivascular astroglia: an immunoperoxidase study. Vis. Res. 32, 1601e1607.
- Triviño, A., Ramírez, J.M., Ramírez, A.I., Salazar, J.J., García-Sánchez, J., 1997. Comparative study of astrocytes in human and rabbit retinae. Vis. Res. 37, 1707e1711.
- Triviño, A., Ramírez, A.I., Salazar, J.J., De Hoz, R., Rojas, B., Padilla, E., Tejerina, T., Ramírez, J.M., 2006. A cholesterol-enriched diet induces ultrastructural changes in retinal and macroglial rabbit cells. Exp. Eye Res. 83, 357e366.
- Tyler, N.K., Burns, M.S., 1991. Alterations in glial cells morphology and glial fibrillary acidic protein expression in urethane-induced retinopathy. Invest. Ophthalmol. Vis. Sci. 32, 246e256.
- Wilson, J.X., 1997. Antioxidant defense of the brain: a role for astrocytes. Can. J. Physiol. Pharmacol. 75, 1149e1163.
- Winkler, B.S., Boulton, M.E., Gottsch, J.D., Sternberg, P., 1999. Oxidative damage and age-related macular degeneration. Mol. Vis. 5, 32.