Anatomical evidence of photoreceptor degeneration induced by iodoacetic acid in the porcine eye

Experimental Eye Research

Volumn 93, Issue 4, 2011, Pages 513-527

  Scott, Patrick A ^a   Kaplan, Henry J ^b   Sandell, Julie H ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Confocal microscopy; Electron microscopy; Immunohistochemistry; Iodoacetic acid; Porcine eye; Retina; Retinal degeneration; Retinitis pigmentosa

Indexed keywords

IODOACETIC ACID; VISUAL PIGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL SURVIVAL; CLINICAL FEATURE; CONTROLLED STUDY; DRUG EFFECT; EYE DISEASE; IMMUNOHISTOCHEMISTRY; MUELLER CELL; NONHUMAN; OPTIC DISK; PHOTORECEPTOR; PHOTORECEPTOR DEGENERATION; PRIORITY JOURNAL; RETINA CONE; RETINA OUTER MOLECULAR LAYER; RETINA ROD; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL COUNT; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAVENOUS; IODOACETIC ACID; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEIN KINASE C-ALPHA; RETINAL DEGENERATION; RHODOPSIN; SUS SCROFA; VIMENTIN;

EID: 80055028972     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2011.06.017     Document Type: Article

References (76)

1. Acland G.M., Aguirre G.D., Ray J., Zhang Q., Aleman T.S., Cideciyan A.V., Pearce-Kelling S.E., Anand V., Zeng Y., Maguire A.M., Jacobson S.G., Hauswirth W.W., Bennett J. Gene therapy restores vision in a canine model of childhood blindness. Nat. Genet. 2001, 28:92-95.
2. Aguirre G.D., Rubin L.F. Pathology of hemeralopia in the Alaskan malamute dog. Invest. Ophthalmol. Vis. Sci. 1974, 13:231-235.
3. Alm A., Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus), a study with radioactively labeled microspheres including flow determinations in brain and some other tissues. Exp. Eye Res. 1973, 15:15-29.
4. Barhoum R., Martínez-Navarrete G., Corrochano S., Germain F., Fernandez- Sanchez L., de La Rosa E.J., de La Villa P., Cuenca N. Functional and structural modifications during retinal degeneration in the rd10 mouse. Neuroscience 2008, 155:698-713.
5. Beauchemin M.L. The fine structure of the pig's retina. Graefes Arch. Clin. Exp. Ophthalmol. 1974, 190:27-45.
6. Braekvelt C.R. Fine structure of the retinal rods and cones in the domestic pig. Graefes Arch. Clin. Exp. Ophthalmol. 1983, 220:273-278.
7. Chader G.J. Animal models in research on retinal degenerations: past progress and future hope. Vis. Res. 2002, 42:393-399.
8. Chandler M.J., Smith P.J., Samuelson D.A., Mackay E.O. Photoreceptor density of the domestic pig retina. Vet. Ophthalmol. 1999, 2:179-184.
9. Chang G.Q., Hao Y., Wong F. Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron 1993, 11:595-605.
10. Cuenca N., Pinilla I., Sauvé Y., Lund R. Early changes in synaptic connectivity following progressive photoreceptor degeneration in RCS rats. Eur. J. Neurosci. 2005, 22:1057-1072.
11. D'Cruz P.M., Yasumura D., Weir J., Matthes M.T., Abderrahim H., LaVail M.M., Vollrath D. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum. Mol. Genet. 2000, 9:645-651.
12. De Schaepdrijver L., Simoens P., Pollet L., Lauwers H., De Laey J.J. Morphological and clinical study of the retinal circulation in the miniature pig. B: fluorescein angiography of the retina. Exp. Eye Res. 1992, 54:975-985.
13. Farber D.B., Souza D.W., Chase D.G. Cone visual cell degeneration in ground squirrel retina: disruption of morphology and cyclic nucleotide metabolism by iodoacetic acid. Invest. Ophthalmol. Vis. Sci. 1983, 24:1236-1249.
14. Farber D.B., Lolley R.N. Cyclic guanosine monophosphate: elevation in degenerating photoreceptor cells of the C3H mouse retina. Science 1974, 186:449-451.
15. Fariss R.N., Li Z.Y., Milam A.H. Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. Am. J. Ophthalmol. 2000, 129:215-223.
16. Fauser S., Luberichs J., Schuttauf F. Genetic animal models for retinal degeneration. Surv. Ophthalmol. 2002, 47:357-367.
17. Fei Y. Cone neurite sprouting: an early onset abnormality of the cone photoreceptors in the retinal degeneration mouse. Mol. Vis. 2002, 8:306-314.
18. Fisher S.K., Lewis G.P. Müller cell neuronal remodeling in retinal detachment and reattachment and their potential consequences for visual recovery: a review and reconsideration of recent data. Vis. Res. 2003, 43:887-897.
19. Gargini C., Terzibasi E., Mazzoni F., Strettoi E. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J. Comp. Neurol. 2007, 500:222-238.
20. Gerke C.G., Hao Y., Wong F. Topography of rods and cones in the retina of the domestic pig. Hong Kong Med. J. 1995, 1:302-308.
21. Graymore C., Tansley K. Iodoacetate poisoning of the rat retina. I. Production of retinal degeneration. Br. J. Ophthalmol. 1959, 43:177-185.
22. Hoang Q.V., Linsenmeier R.A., Chung C.K., Curcio C.A. Photoreceptor inner segments in monkey and human retina: mitochondrial density, optics, and regional variation. Vis. Neurosci. 2002, 19:395-407.
23. Hughes A. Topographical relationships between anatomy and physiology of the rabbit visual system. Doc. Ophthalmol. 1971, 30:30-159.
24. Humayun M., Sato Y., Propst R., de Juan E. Can potentials from the visual cortex be elicited electrically despite severe retinal degeneration and a markedly reduced electroretinogram?. Ger. J. Ophthalmol. 1995, 4:57-64.
25. Humayun M.S., Prince M., de Juan E.J., Barron Y., Moskowitz M., Klock I.B., Milam A.H. Morphometric analysis of the extramacular retina from postmortem eyes with retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 1999, 40:143-148.
26. Ivert L., Gouras P., Naeser P., Narfstrom K. Photoreceptor allografts in a feline model of retinal degeneration. Graefes Arch. Clin. Exp. Ophthalmol. 1998, 236:844-852.
27. Jaissle G.B., May C.A., Reinhard J., Kohler K., Fauser S., Lutjen-Drecoll E., Zrenner E., Seeliger M.W. Evaluation of the rhodopsin knockout mouse as a model of pure cone function. Invest. Ophthalmol. Vis. Sci. 2001, 42:506-513.
28. Johnson L.V., Hageman G.S., Blanks J.C. Interphotoreceptor matrix domains ensheath vertebrate cone photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 1986, 27:129-135.
29. Jones B.W., Watt C.B., Frederick J.M., Baehr W., Chen C.K., Levine E.M., Milam A.H., LaVail M.M., Marc R.E. Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol. 2003, 464:1-16.
30. Jones B.W., Marc R.E. Retinal remodeling during degeneration. Exp. Eye Res. 2005, 81:123-137.
31. Kim S., Sadda S., Pearlman J., Humayun M.S., de Juan E., Melia B.M., Green W.R. Morphometric analysis of the macula in eyes with disciform age-related macular degeneration. Retina 2002, 22:471-477.
32. Lachapelle P., Benoit J., Guite P., Tran C.N., Molotchnikoff S. The effect of iodoacetic acid on the electroretinogram and oscillatory potentials in rabbits. Doc. Ophthalmol. 1990, 75:7-14.
33. Lasansky A., De Robertis E. Submicroscopic changes in visual cells of the rabbit induced by iodoacetate. J. Biophys. Biochem. Cytol. 1959, 5:245-250.
34. Li Z.-Y., Kljavin I.J., Milam A.H. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J. Neurosci. 1995, 15:5429-5438.
35. Li T., Snyder W.K., Olsson J.E., Dryja T.P. Transgenic mice carrying the dominant rhodopsin mutation P347S: evidence for defective vectorial transport of rhodopsin to the outer segments. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:14176-14181.
36. Li Z.Y., Wong F., Chang J.H., Possin D.E., Hao Y., Petters R.M., Milam A.H. Rhodopsin transgenic pigs as a model for human retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 1998, 39:808-819.
37. Liang L., Katagiri Y., Franco L.M., Yamauchi Y., Enzmann V., Kaplan H.J., Sandell J.H. Long-term cellular and regional specificity of the photoreceptor toxin, iodoacetic acid (IAA), in the rabbit retina. Vis. Neurosci. 2008, 25:1-11.
38. Lin B., Masland R.H., Strettoi E. Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp. Eye Res. 2009, 88:589-599.
39. Linberg K.A., Lewis G.P., Matsumoto B., Fisher S.K. Immunocytochemical evidence that rod connected horizontal cell axon terminals remodel in response to experimental retinal detachment in the cat. Mol. Vis. 2006, 12:1674-1686.
40. Lolley R.N., Farber D.B. Abnormal guanosine 3',5'-monophosphate during photoreceptor degeneration in the inherited retinal disorder of C3H/HeJ mice. Ann. Ophthalmol. 1976, 8:469-473.
41. Macaluso C., Onoe S., Niemeyer G. Changes in glucose level affect rod function more than cone function in the isolated, perfused cat eye. Invest. Ophthalmol. Vis. Sci. 1992, 33:2798-2808.
42. Marc R.E., Jones B.W., Watt C.B., Strettoi E. Neural remodeling in retinal degeneration. Prog. Ret. Eye Res. 2003, 22:607-655.
43. Marc R.E., Jones B.W., Watt C.B., Vazquez-Chona F., Vaughan D.K., Organisciak D.T. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol. Vis. 2008, 14:782-806.
44. Milam A.H., Li Z.-Y., Fariss R.N. Histopathology of the human retina in retinitis pigmentosa. Prog. Ret. Eye Res. 1998, 17:175-205.
45. Medeiros N.E., Curcio C.A. Preservation of ganglion cell layer neurons in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2001, 42:795-803.
46. Mohand-Said S., Deudon-Combe A., Hicks D., Fintz A.C., Simonutti M., Forster V., Leveillard T., Dreyfus H., Sahel J.-A. Normal rod photoreceptors increase cone survival in the retinal degeneration (rd) mouse. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8357-8362.
47. Musarella M.A., MacDonald I.M. Current concepts in the treatment of retinitis pigmentosa. J. Ophthalmol. 2011, 2011:1-8.
48. Nagar S., Krishnamoorthy V., Cherukuri P., Jain V., Dhingra N.K. Early remodeling in an inducible animal model of retinal degeneration. Neuroscience 2009, 160:517-529.
49. Nihira M., Anderson K., Gorin F.A., Burns M.S. Primate rod and cone photoreceptors may differ in glucose accessibility. Invest. Ophthalmol. Vis. Sci. 1995, 36:1259-1270.
50. Ninomiya H., Inomata T. Microvascular anatomy of the pig eye: scanning electron microscopy of vascular corrosion casts. J. Vet. Med. Sci. 2006, 68:1149-1154.
51. Noell W.K. The effect of iodoacetate on the vertebrate retina. J. Cell. Comp. Physiol. 1951, 37:283-307.
52. Noell W.K. The impairment of visual cell structure by iodoacetate. J. Cell. Comp. Physiol. 1952, 40:25-55.
53. Noell W.K. Experimentally induced toxic effects on structure and function of visual cells and pigment epithelium. Am. J. Ophthalmol. 1953, 36:103-116.
54. Nork T.M., Kim C.B., Shanmuganayagam D., Van Lysel M.S., Ver Hoeve J.N., Foltz J.D. Measurement of regional choroidal blood flow in rabbits and monkeys using fluorescent microspheres. Arch. Ophthalmol. 2006, 124:860-868.
55. Olsson J.E., Gorden J.W., Pawlyk B.S., Roof D., Hayes A., Molday R.S., Mukai S., Cowley G.S., Berson E.L., Dryja T.P. Transgenic mice with a rhodopsin mutation (Pro-23-His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron 1992, 9:815-830.
56. Orzalesi N., Calabria G.A., Grignolo A. Experimental degeneration of the rabbit retina induced by iodoacetic acid. A study of the ultrastructure, the rhodopsin cycle and the uptake of 14C-labeled iodoacetic acid. Exp. Eye Res. 1970, 9:246-253.
57. Park S.J., Kim I.B., Choi K.R., Moon J.I., Oh S.J., Chung J.W., Chun M.H. Reorganization of horizontal cell processes in the developing FVB/N mouse retina. Cell Tissue Res. 2001, 306:341-346.
58. Peichl L., Bolz J. Kainic acid induces sprouting of retinal neurons. Science 1984, 223:503-504.
59. Perkins G.A., Ellisman M.H., Fox D.A. Three-dimensional analysis of mouse rod and cone mitochondria architecture: bioenergetic and functional implications. Mol. Vis. 2003, 9:60-73.
60. Petters R.M., Alexander C.A., Wells K.D., Collins E.B., Sommer J.R., Blanton M.R., Rojas G., Hao Y., Flowers W.L., Banin E., Cideciyan A.V., Jacobson S.G., Wong F. Genetically engineered large animal model for studying cone photoreceptor survival and degeneration in retinitis pigmentosa. Nat. Biotechnol. 1997, 15:965-970.
61. Pignatelli V., Cepko C.L., Strettoi E. Inner retinal abnormalities in a mouse model of Leber's congenital amaurosis. J. Comp. Neurol. 2004, 469:351-359.
62. Roof D.J., Adamian M., Hayes A. Rhodopsin accumulation at abnormal sites in retinas of mice with a human P23H rhodopsin transgene. Invest. Ophthalmol. Vis. Sci. 1994, 35:4049-4062.
63. Santos A., Humayun M.S., de Juan E.J., Greenburg R.J., Marsh M.J., Klock I.B., Milam A.H. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch. Ophthalmol. 1997, 115:511-515.
64. Sharma R.K., Ehinger B. Management of hereditary retinal degenerations: present status and future directions. Surv. Ophthalmol. 1999, 43:427-444.
65. Simoens P., De Schaepdrijver L., Lauwers H. Morphologic and clinical study of the retinal circulation in the miniature pig. A: morphology of the retinal microvasculature. Exp. Eye Res. 1992, 54:965-973.
66. Stone J.L., Barlow W.E., Humayun M.S., de Juan E.J., Milam A.H. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch. Ophthalmol. 1992, 110:1634-1639.
67. Strauss O., Stumpff F., Mergler S., Wienrich M., Wiederholt M. The Royal College of Surgeons rat: an animal model for inherited retinal degeneration with a still unknown genetic defect. Acta Anat. (Basel) 1998, 162:101-111.
68. Strettoi E., Pignatelli V. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11020-11025.
69. Strettoi E., Porciatti V., Falsini B., Pignatelli V., Rossi C. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J. Neurosci. 2002, 22:5492-5504.
70. Strettoi E., Pignatelli V., Rossi C., Porciatti V., Falsini B. Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vis. Res. 2003, 43:867-877.
71. Sullivan R.K.P., Wolde Mussie E., Pow D.V. Dendritic and synaptic plasticity of neurons in the human age-related macular degeneration retina. Invest. Ophthalmol. Vis. Sci. 2007, 48:2782-2791.
72. Sung C.H., Makino C., Baylor D., Nathans J. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment. J. Neurosci. 1994, 14:5818-5833.
73. Törnquist P., Alm A., Bill A. Studies on ocular blood flow and retinal capillary permeability to sodium in pigs. Acta Physiol. Scand. 1979, 106:343-350.
74. Tso M.O.M., Li W.W.Y., Zhang C., Lam T.T., Hao Y., Petters R.M., Wong F. A pathologic study of degeneration of the rod and cone populations of the rhodopsin PRO347LEU transgenic pigs. Trans. Am. Ophthalmol. Soc. 1997, 95:467-483.
75. Wikler K.C., Williams R.W., Rakic P. Photoreceptor mosaic: number and distribution of rods and cones in the rhesus monkey retina. J. Comp. Neurol. 1990, 297:499-508.
76. Winkler B.S., Sauer M.W., Starnes C.A. Modulation of the Pasteur effect in retinal cells: implications for understanding compensatory metabolic mechanisms. Exp. Eye Res. 2003, 76:715-723.