Age-related changes in visual function in cystathionine-beta-synthase mutant mice, a model of hyperhomocysteinemia

Experimental Eye Research

Volumn 96, Issue 1, 2012, Pages 124-131

  Yu, Minzhong ^a   Sturgill Short, Gwen ^a,b   Ganapathy, Preethi ^c   Tawfik, Amany ^c   Peachey, Neal S ^a,b,d   Smith, Sylvia B ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

Author keywords

Electrophysiology; Electroretinogram; Mouse; Optic nerve; Retina; Retinal degeneration; Retinal function; Visual evoked potential

Indexed keywords

CYSTATHIONINE BETA SYNTHASE; HOMOCYSTEINE;

A WAVE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; CELL LOSS; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRORETINOGRAPHY; EVOKED VISUAL RESPONSE; GROUPS BY AGE; HISTOPATHOLOGY; HYPERHOMOCYSTEINEMIA; MOUSE; NONHUMAN; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RESPONSE TIME; RETINA DISEASE; RETINA GANGLION CELL; VISUAL CORTEX; WILD TYPE;

AGING; ANIMALS; CYSTATHIONINE BETA-SYNTHASE; DARK ADAPTATION; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; EVOKED POTENTIALS, VISUAL; HOMOCYSTEINE; HYPERHOMOCYSTEINEMIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; RETINA; RETINAL PIGMENT EPITHELIUM; VISUAL ACUITY; VISUAL CORTEX;

EID: 84862803353     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2011.12.011     Document Type: Article

References (37)

1. Axer-Siegel R., Bourla D., Ehrlich R., et al. Association of neovascular age-related macular degeneration and hyperhomocysteinemia. Am. J. Ophthalmol. 2004, 137:84-89.
2. Aydemir O., Türkçüoĝlu P., Güler M., Celiker U., Ustündaĝ B., Yilmaz T., Metin K. Plasma and vitreous homocysteine concentrations in patients with proliferative diabetic retinopathy. Retina 2008, 28:741-743.
3. Bleich S., Jünemann A., Von Ahsen N., et al. Homocysteine and risk of open-angle glaucoma. J. Neural Transm. 2002, 109:1499-1504.
4. Carelli V., Ross-Cisneros F.N., Sadun A.A. Mitochondrial dysfunction as a cause of optic neuropathies. Prog. Retin. Eye Res. 2004, 1:53-89.
5. Chang H.H., Lin D.P., Chen Y.S., Liu H.J., Lin W., Tsao Z.J., Teng M.C., Chen B.Y. Intravitreal homocysteine-thiolactone injection leads to the degeneration of multiple retinal cells, including photoreceptors. Mol. Vis. 2011, 17:1946-1956.
6. Clement C.I., Goldberg I., Healey P.R., Graham S.L. Plasma homocysteine, MTHFR gene mutation, and open-angle glaucoma. J. Glaucoma 2009, 1:73-78.
7. Dun Y., Thangaraju M., Prasad P., Ganapathy V., Smith S.B. Prevention of excitotoxicity in primary retinal ganglion cells by (+)-Pentazocine, a sigma receptor-1-specific ligand. Invest. Ophthalmol. Vis. Sci. 2007, 48:4785-4794.
8. Edwards M.M., Marín deEvsikova C., Collin G.B., Gifford E., Wu J., Hicks W.L., Whiting C., Varvel N.H., Maphis N., Lamb B.T., Naggert J.K., Nishina P.M., Peachey N.S. Photoreceptor degeneration, azoospermia, leukoencephalopathy and abnormal retinal pigment epithelial cell function in mice expressing an early stop mutation in CLCN2. Invest. Ophthalmol. Vis. Sci. 2010, 51:3264-3272.
9. Felekis T., Katsanos K.H., Zois C.D., Vartholomatos G., Kolaitis N., Asproudis I., Tsianos E.V. Anterior ischemic optic neuropathy in a patient with Crohn's disease and aberrant MTHFR and GPIIIa gene variants. J. Crohns Colitis 2010, 4:471-474.
10. Frishman L.J., Wang M.H. Electroretinogram of human, monkey and mouse. Adler's Physiology of the Eye 2011, 480-501. Saunders Elsevier, New York, NY. eleventh ed. L.A. Levin, S.F.E. Nilsson, J. Ver Hoeve, S.M. Wu, P.L. Kaufman, A. Alm (Eds.).
11. Ganapathy P.S., Moister B., Roon P., Mysona B.A., Duplantier J., Dun Y., Moister T.K., Farley M.J., Prasad P.D., Liu K., Smith S.B. Endogenous elevation of homocysteine induces retinal neuron death in the cystathionine-beta-synthase mutant mouse. Invest. Ophthalmol. Vis. Sci. 2009, 50:4460-4470.
12. Ganapathy P.S., Dun Y., Ha Y., Duplantier J., Allen J.B., Farooq A., Bozard B.R., Smith S.B. Sensitivity of staurosporine-induced differentiated RGC-5 cells to homocysteine. Curr. Eye Res. 2010, 35:80-90.
13. Ganapathy P.S., Perry R.L., Tawfik A., Smith R.M., Perry E., Roon P., Bozard B.R., Ha Y., Smith S.B. Homocysteine-mediated modulation of mitochondrial dynamics in retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 2011, 52:5551-5558.
14. Gerding H. Ocular complications and a new surgical approach to lens dislocation in homocystinuria due to cystathionine-beta-synthetase deficiency. Eur. J. Pediatr. 1998, 157:S94-S101.
15. Ha Y., Saul A., Tawfik A., Williams C., Bollinger K., Smith R., Tachikawa M., Zorrilla E., Ganapathy V., Smith S.B. Late-onset inner retinal dysfunction in mice lacking sigma receptor 1 (σR1). Invest. Ophthalmol. Vis. Sci. 2011, 52:7749-7760.
16. Jaksic V., Markovic V., Milenkovic S., Stefanovic I., Jakovic N., Knezevic M. MTHFR C677T homozygous mutation in a patient with pigmentary glaucoma and central retinal vein occlusion. Ophthalmic Res. 2010, 43:193-196.
17. Lahey J.M., Kearney J.J., Tunc M. Hypercoagulable states and central retinal vein occlusion. Curr. Opin. Pulm. Med. 2003, 9:385-392.
18. Lawrance A.K., Racine J., Deng L., Wang X., Lachapelle P., Rozen R. Complete deficiency of methylenetetrahydrofolate reductase in mice is associated with impaired retinal function and variable mortality, hematological profiles, and reproductive outcomes. J. Inherit. Metab. Dis. 2011, 34:147-157.
19. Maeda M., Fujio Y., Azuma J. MTHFR gene polymorphism and diabetic retinopathy. Curr. Diabetes Rev. 2006, 4:467-476.
20. Micheal S., Qamar R., Akhtar F., Khan M.I., Khan W.A., Ahmed A. MTHFR gene C677T and A1298C polymorphisms and homocysteine levels in primary open angle and primary closed angle glaucoma. Mol. Vis. 2009, 15:2268-2278.
21. Moore P., El-sherbeny A., Roon P., Schoenlein P.V., Ganapathy V., Smith S.B. Apoptotic cell death in the mouse retinal ganglion cell layer is induced in vivo by the excitatory amino acid homocysteine. Exp. Eye Res. 2001, 73:45-57.
22. Mudd S.H. Hypermethioninemias of genetic and non-genetic origin: a review. Am. J. Med. Genet. C., Semin. Med. Genet. 2011, 157:3-32.
23. Mulvihill A., Yap S., O'Keefe M., Howard P.M., Naughten E.R. Ocular findings among patients with late-diagnosed or poorly controlled homocystinuria compared with a screened, well-controlled population. J. Amer. Assoc. Ped. Ophthalmol. Strabismus 2001, 5:311-315.
24. Peachey N.S., Roveri L., Messing A., McCall M.A. Functional consequences of oncogene-induced horizontal cell degeneration in the retinas of transgenic mice. Vis. Neurosci. 1997, 14:627-632.
25. Poloschek C.M., Fowler B., Unsold R., Lorenz B. Disturbed visual system function in methionine synthase deficiency. Graefes Arch. Clin. Exp. Ophthalmol. 2005, 243:497-500.
26. Ridder W.H., Nusinowitz S. The visual evoked potential in the mouse-origins and response characteristics. Vis. Res. 2006, 46:902-913.
27. Roybal C.N., Yang S., Sun C.W., Hurtado D., Vander, Jagt D.L., Townes T.M., Abcouwer S.F. Homocysteine increases the expression of vascular endothelial growth factor by a mechanism involving endoplasmic reticulum stress and transcription factor ATF4. J. Biol. Chem. 2004, 279:14844-14852.
28. Seddon J.M., Gensler G., Klein M.L., Milton R.C. Evaluation of plasma homocysteine and risk of age-related macular degeneration. Am. J. Ophthalmol. 2006, 141:201-203.
29. Tranchina L., Centofanti M., Oddone F., Tanga L., Roberti G., Liberatoscioli L., Cortese C., Manni G. Levels of plasma homocysteine in pseudoexfoliation glaucoma. Graefes Arch. Clin. Exp. Ophthalmol. 2011, 3:443-448.
30. Tsina E.K., Marsden D.L., Hansen R.M., Fulton A.B. Maculopathy and retinal degeneration in cobalamin C methylmalonic aciduria and homocystinuria. Arch. Ophthalmol. 2005, 123:1143-1146.
31. Turgut B., Kaya M., Arslan S., Demir T., Güler M., Kaya M.K. Levels of circulating homocysteine, vitamin B6, vitamin B12, and folate in different types of open-angle glaucoma. Clin. Interv. Aging 2010, 5:133-139.
32. Vessani R.M., Ritch R., Liebmann J.M., Jofe M. Plasma homocysteine is elevated in patients with exfoliation syndrome. Am. J. Ophthalmol. 2003, 136:41-46.
33. Watanabe M., Osada J., Aratani Y., Kluckman K., Reddick R., Malinow M.R. Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocysteinemia. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:1585-1589.
34. Wu J., Peachey N.S., Marmorstein A. D. Light-evoked responses of the mouse retinal pigment epithelium. J. Neurophysiol. 2004, 91:1134-1142.
35. V1.3 subunits regulate the light peak of the electroretinogram. J. Neurophys. 2007, 97:3731-3735.
36. Yang G., Lu J., Pan C. The impact of plasma homocysteine level on development of retinopathy in type 2 diabetes mellitus. Zhonghua Nei Ke Za Zhi 2002, 41:34-38.
37. Yu M., Narayanan S.P., Wang F., Morse E., Macklin W.B., Peachey N.S. Visual abnormalities associated with enhanced optic nerve myelination. Brain Res. 2011, 1374:36-42.