Evolving neurovascular relationships in the RCS rat with age

Current Eye Research

Volumn 27, Issue 3, 2003, Pages 183-196

  Wang, S ^a,b   Villegas Perez M P ^c   Holmes, T ^a,b   Lawrence, J M ^e   Vidal Sanz, M ^c   Hurtado Montalban N ^c   Lund, R D ^a,b,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF MURCIA   (Spain)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e NONE

Author keywords

Degeneration; Retinal ganglion cell; Retinal pigment epithelial cell; Retinitis pigmentosa; Vascular complex

Indexed keywords

NEUROFILAMENT PROTEIN; PEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL MIGRATION; CONTROLLED STUDY; DISEASE COURSE; HISTOCHEMISTRY; IMMUNOPEROXIDASE STAINING; NERVE FIBER DEGENERATION; NONHUMAN; OPTIC NERVE FIBER; PHOTORECEPTOR; PIGMENT CELL; PRIORITY JOURNAL; RAT; RETINA BLOOD VESSEL; RETINA GANGLION CELL; VASCULAR DISEASE;

AGING; ANIMALS; AXONS; CAPILLARY PERMEABILITY; CELL DEATH; HORSERADISH PEROXIDASE; NADPH DEHYDROGENASE; OPTIC NERVE; PHOTORECEPTORS, VERTEBRATE; RATS; RATS, MUTANT STRAINS; RETINAL DEGENERATION; RETINAL GANGLION CELLS; RETINAL VESSELS;

EID: 0141650582     PISSN: 02713683     EISSN: None     Source Type: Journal    
DOI: 10.1076/ceyr.27.3.183.16053     Document Type: Article

References (56)

1. Chan-Ling T, Halasz P, Stone J. Development of retinal vasculature in the cat: Processes and mechanisms. Curr Eye Res. 1990;9:459-478.
2. Gariano RF, Iruela-Arispe ML, Sage EH, Hendrickson AE. Immunohistochemical characterization of developing and mature primate retinal blood vessels. Invest Ophthalmol Vis Sci. 1996;37:93-103.
3. Villegas Perez MP, Vidal Sanz M, Bray GM, Aguayo AJ. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci. 1988;8:265-280.
4. Maslim J, Stone J. Tissue oxygen is a factor in photoreceptor dystrophy: Evidence from the RCS rat. Invest Ophthalmol Vis Sci. 1996;37:144.
5. Dowling JE, Sidman RL. Inherited retinal dystrophy in the rat. J Cell Biol. 1962;14:73-107.
6. LaVail MM, Battelle BA. Influence of eye pigmentation and light deprivation on inherited retinal dystrophy in the rat. Exp Eye Res. 1975;21:167-192.
7. D'Cruz PM, Yasumura D, Weir J, Matthes MT, Abderrahim H, LaVail MM, Vollrath D. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet. 2000;9:645-651.
8. Bok D, Hall MO. The role of the pigment epithelium in the etiology of inherited retinal dystrophy in the rat. J Cell Biol. 1971;49:664-682.
9. Chaitin MH, Hall MO. The distribution of actin in cultured normal and dystrophic rat pigment epithelial cells during the phagocytosis of rod outer segments. Invest Ophthalmol Vis Sci. 1983;24:821-831.
10. Caldwell RB, Roque RS, Solomon SW. Increased vascular density and vitreo-retinal membranes accompany vascularization of the pigment epithelium in the dystrophic rat retina. Curr Eye Res. 1989;8:923-937.
11. El-Hifnawi E. Pathomorphology of the retina and its vasculature in hereditary retinal dystrophy in RCS rats. In: Zrenner E, Krastel H, Goebel H-H, eds. Research in Retinitis Pigmentosa. Advances in the Biosciences, Vol. 62. Oxford: Pergamon; 1987:417-434.
12. Essner E, Pino RM, Griewski RA. Permeability of retinal capillaries in rats with inherited retinal degeneration. Invest Ophthalmol Vis Sci. 1979;18:859-863.
13. Gerstein DD, Dantzker DR. Retinal vascular changes in hereditary visual cell degeneration. Arch Ophthalmol. 1969;81:99-105.
14. Matthes MT, Bok D. Blood vascular abnormalities in animals with inherited retinal degeneration. In: LaVail MM, Hollyfield JG, Anderson RE, eds., Retinal Degeneration: Experimental and Clinical studies. New York: Alan R. Lis; 1984:209-237.
15. Van Driel D, Provis JM, Billson FA. Morphology of intraretinal new vessels in the PETH rat. Grae Arch Clin Exp Ophthalmol. 1988;226:576-582.
16. Villegas-Perez MP, Lawrence JM, Vidal-Sanz M, LaVail MM, Lund RD. Ganglion cell loss in RCS rat retina: A result of compression of axons by contracting intraretinal vessels linked to the pigment epithelium. J Comp Neurol. 1998;392:58-77.
17. Villegas-Perez PM, Vidal SM, Lund RD. Mechanism of retinal ganglion cell loss in inherited retinal dystrophy. Neuroreport. 1996;7:1995-1999.
18. Li ZY, Possin DE, Milam AM. Histopathology of bone spicule pigmentation in retinitis pigmentosa. Ophthalmology. 1995;102:805-816.
19. Hartnett ME, Weiter JJ, Staurenghi G, Elsner AE. Deep retinal vascular anomalous complexes in advanced age-related macular degeneration. Ophthalmology. 1996;103:2042-2053.
20. Milam AH, Li ZY. Retinal pathology in retinitis pigmentosa: Considerations for therapy. In: Anderson RE, LaVail MM, Hollyfield JG, eds. Degenerative Diseases of the Retina. New York: Plenum Press; 1995:275-284.
21. Chakravarthy U, Stitt AW, McNally J, Bailie JR, Hoey EM, Duprex P. Nitric-oxide synthase activity and expression in retinal capillary. Curr Eye Res. 1995;14:285-294.
22. Provis JM, Leech J, Diaz CM, Penfold PL, Stone J, Keshet E. Development of the human retinal vasculature: Cellular relations and VEGF expression. Exp Eye Res. 1997;65:555-568.
23. Wang S, Villegas-Perez MP, Vidal-Sanz M, Lund RD. Progressive optic axon dystrophy and vacuslar changes in rd mice. Invest Ophthalmol Vis Sci. 2000;41:537-545.
24. Takemura M, Wakisaka S, Iwase K, Yabuta NH, Nakagawa S, Chen K, Bae YC, Yoshida A, Shigenaga Y. NADPH-diaphorase in the developing rat: Lower brainstem and cervical spinal cord, with special reference to the trigemino-solitary complex. J Comp Neurol. 1996;365:511-525.
25. Linden R, Perry VH. Massive retinotectal projection in rats. Brain Res. 1983;272:145-149.
26. Rexer M, May ChA, Lutjen-Drecoll E. Changes in the choroidal innervation in Royal College of Surgeons Rats with hereditary retina degeneration. Acta Anatomica. 1998;162:112-118.
27. Michaelson IC. Retinal circulation in man and animals. The Rat. Springfield, IL: Charles C. Thomas; 1954:64-73.
28. Dahl D, Bignami A. Neurofilament phosphorylation in the axonless horizontal cells of rat retina. Brain Res. 1991;553:163-166.
29. Peichl L, Gonzalez-Soriano J. Unexpected presence of neurofilaments in axon-bearing horizontal cells of the mammalian retina. J Neurosci. 1993;13:4091-4100.
30. Roth S. Role of nitric oxide in retinal cell death. Clin Neurosci. 1997;4:216-223.
31. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest. 1998;101:731-736.
32. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest. 1998;101:2567-2578.
33. Iwashina M, Shichiri M, Marumo F, Hirata Y. Transfection of inducible nitric oxide synthese gene causes apoptosis in vascular smooth muscle cells. Circulation. 1998;98:1212-1218.
34. Lopez-Farre A, Rodriguez-Feo JA, Sanchez-de ML, Rico L, Casado S. Role of nitric oxide in the control of apoptosis in the microvasculature. Int J Biochem and Cell Biol. 1998;30:1095-1106.
35. Bourne MC, Campbell DA, Tansley K. Hereditary degeneration of the rat retina. Br J Ophthalmol. 1938;2:613-623.
36. Burns MS, Tyler NK. Selective neovascularization of the retinal pigment epithelium in rat photoreceptor degeneration in vivo. Curr Eye Res. 1990;9:1061-1075.
37. Roque RS, Caldwell RB. Muller cell changes precede vascularization of the pigment epithelium in the dystrophic rat retina. Glia. 1990;3:464-475.
38. Weber ML, Mancini MA, Frank RN. Retinovitreal neovascularization in the Royal College of Surgeons rat. Curr Eye Res. 1989;8:61-74.
39. Frank RN, Das A, Weber ML. A model of subretinal neovascularization in the pigmented rat. Curr Eye Res. 1989;8:239-247.
40. Bowes C, Li T, Danciger M, Baxter LC, Applebury L, Farber DB. Retinal degeneration in the rd mouse is caused by a defect in the B subunit of rod cGMP-phosphodiesterase. Nature. 1990;347:677-680.
41. Schmidt SY, Lolley RN. Cyclic-nucleotide phosphodiesterase: an early defect in inherited retinal degeneration of C3H mice. Journal of Cell Biology. 1973;57:117-123.
42. Nishikawa S, LaVail MM. Neovascularization of the RPE: temporal differences in mice with rod photoreceptor gene defects. Exp Eye Res. 1998;67:509-515.
43. Bellhorn RW, Burns M, Friedman AH. Urethane-induced retinopathy in pigmented rats. Invest Ophthalmol Vis Sci. 1973;12:65-76.
44. Bellhorn RW, Burns MS, Benjamin JV. Retinal vessel abnormalities of phototoxic retinopathy in rats. Invest Ophthalmol Vis Sci. 1980;19:584-595.
45. Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet. 2000;26:270-271.
46. Gu SM, Thompson DA, Srikumari CR, Lorenz B, Finckh U, Nicoletti A, Murthy KR, Rathmann M, Kumaramanickavel G, Denton MJ, Gal A. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat Genet. 1997;17:194-197.
47. Santos A, Humayun MS, de Juan EJr, Greenburg RJ, Marsh MJ, Klock IB, Milam AH. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch Ophthalmol. 1997;115:511-515.
48. Stone JL, Barlow WE, Humayun MS, de Juan E Jr, Milam AH. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch Ophthalmol. 1992;110:1634-1639.
49. Falsini B, Iarossi G, Porciatti V, Merendino E, Fadda A, Cermola S, Buzzonetti L. Postreceptoral contribution to macular dysfunction in retinitis pigmentosa. Invest Ophthalmol Vis Sci. 1994;35:4282-4290.
50. Hood DC, Birch DG. Assessing abnormal rod photoreceptor activity with the a-wave of the electroretinogram: applications and methods. Doc Ophthalmol. 1996;92:253-267.
51. Coffey PJ, Girman S, Wang SM, Hetherington L, Keegan DJ, Adamson P, Greenwood J, Lund RD. Long-term preservation of cortically dependent visual function in RCS rats by transplantation. Nat Neurosci. 2002;5:53-56.
52. LaVail MM, Li L, Turner JE, Yasumura D. Retinal pigment epithelial cell transplantation in RCS rats: Normal metabolism in rescued photoreceptors. Exp Eye Res. 1992;55:555-562.
53. Lawrence JM, Sauve Y, Keegan DJ, Coffey PJ, Hetherington L, Girman S, Whiteley SJ, Kwan AS, Pheby T, Lund RD. Schwann cell grafting into the retina of the dystrophic RCS rat limits functional deterioration. Royal College of Surgeons. Invest Ophthalmol Vis Sci. 2000;41:518-528.
54. Lund RD, Adamson P, Sauve Y, Keegan DJ, Girman SV, Wang S, Winton H, Kanuga N, Kwan AS, Beauchene L, Zerbib A, Hetherington L, Couraud PO, Coffey P, Greenwood J. Subretinal transplantation of genetically modified human cell lines attenuates loss of visual function in dystrophic rats. Proc Natl Acad Sci U.S.A. 2001;98:9942-9947.
55. Holmes TM, Lawrence JM, Butt RP, Lund RD. Development of Retinal Vascular Complexes in the Royal College of Surgeons (RCS) rat and the Effects of Pharmaceutical Intervention With Pigment epothelial Derived Factor (PEDF) and Echistatin. Invest Ophthalmol Vis Sci. 2002: E-Abstract 3486.
56. Holmes TM, Lu B, Lund RD. Human RPE cell transplants retard the secondary vascular events of RCS rat retinal degeneration. Invest Ophthalmol Vis Sci. 2003: E-Abstract 4972.