Estrogen protects the inner retina from apoptosis and ischemia-induced loss of Vesl-1L/Homer 1c immunoreactive synaptic connections

Investigative Ophthalmology and Visual Science

Volumn 44, Issue 7, 2003, Pages 3155-3162

  Kaja, Simon ^a,c   Yang, Shao Hua ^a   Wei, Jiao ^a   Fujitani, Kazuko ^b   Liu, Ran ^a   Brun Zinkernagel, Anne Marie ^a   Simpkins, James W ^a   Inokuchi, Kaoru ^b   Koulen, Peter ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; METABOTROPIC RECEPTOR; PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; MICROSCOPY; NERVE CELL; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA ISCHEMIA; SYNAPSE;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CARRIER PROTEINS; ESTROGENS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IN SITU NICK-END LABELING; ISCHEMIA; MICROSCOPY, IMMUNOELECTRON; NEURONS; NEUROPEPTIDES; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RETINAL DISEASES; RETINAL GANGLION CELLS; RETINAL VESSELS; SYNAPSES;

EID: 0037562460     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.02-1204     Document Type: Article

References (67)

1. Kawasaki A, Han MH, Wei JY, Hirata K, Otori Y, Barnstable CJ. Protective effect of arachidonic acid on glutamate neurotoxicity in rat retinal ganglion cells. Invest Ophthalmol Vis Sci. 2002;43:1835-1842.
2. Shen W, Slaughter MM. A nonexcitatory paradigm of glutamate toxicity. J Neurophysiol. 2002;87:1629-1634.
3. Sucher NJ, Lipton SA, Dreyer EB. Molecular basis of glutamate toxicity in retinal ganglion cells. Vision Res. 1997;37:3483-3493.
4. Harris A, Chung HS, Ciulla TA, Kagemann L. Progress in measurement of ocular blood flow and relevance to our understanding of glaucoma and age-related macular degeneration. Prog Retinal Eye Res. 1999;18:669-87.
5. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes: early onset and effect of insulin. J Clin Invest. 1998;102:783-791.
6. Hammes HP, Federoff HJ, Brownlee M. Nerve growth factor prevents both neuroretinal programmed cell death and capillary pathology in experimental diabetes. Mol Med. 1995;1:527-534.
7. Penman AD, Serjeant GR. Recent advances in the treatment of proliferative sickle cell retinopathy. Curr Opin Ophthalmol. 1992;3:379-388.
8. Munaut C, Lambert V, Noel A, et al. Presence of oestrogen receptor type beta in human retina. Br J Ophthalmol. 2001;85:877-882.
9. Wickham LA, Gao J, Toda I, Rocha EM, Ono M, Sullivan DA. Identification of androgen, estrogen and progesterone receptor mRNAs in the eye. Acta Ophthalmol Scand. 2000;78:146-153.
10. Wickham LA, Rocha EM, Gao J, et al. Identification and hormonal control of sex steroid receptors in the eye. Adv Exp Med Biol. 1998;438:95-100.
11. Kobayashi K, Kobayashi H, Ueda M, Honda Y. Estrogen receptor expression in bovine and rat retinas. Invest Ophthalmol Vis Sci. 1998;39:2105-2110.
12. Ogueta SB, Schwartz SD, Yamashita CK, Farber DB. Estrogen receptor in the human eye: influence of gender and age on gene expression. Invest Ophthalmol Vis Sci. 1999;40:1906-1911.
13. Tadokoro S, Tachibana T, Imanaka T, Nishida W, Sobue K. Involvement of unique leucine-zipper motif of PSD-Zip45 (Homer 1c/vesl-1L) in group 1 metabotropic glutamate receptor clustering. Proc Natl Acad Sci USA. 1999;96):13801-13806.
14. Kammermeier PJ, Xiao B, Tu JC, Worley PF, Ikeda SR. Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. J Neurosci. 2000;20:7238-7245.
15. 2+ stores and ion channels in neurons. Trends Neurosci. 2000;23:80-88.
16. Ango F, Pin JP, Tu JC, et al. Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by homerl proteins and neuronal excitation. J Neurosci. 2000;20:8710-8716.
17. Tu JC, Xiao B, Naisbitt S, et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron. 1999;23:583-592.
18. Tu JC, Xiao B, Yuan JP, et al. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron. 1998;21:717-726.
19. Xiao B, Tu JC, Petralia RS, et al. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron. 1998;21:707-716.
20. Kato A, Ozawa F, Saitoh Y, Fukazawa Y, Sugiyama H, Inokuchi, K. Novel members of the Vesl/Homer family of PDZ-proteins that bind metabotropic glutamate receptors. J Biol Chem. 1998;273:23969-23975.
21. Shiraishi Y, Mizutani A, Bito H, et al. Cupidin, an isoform of Homer/Vesl, interacts with the actin cytoskeleton and activated rho family small GTPases and is expressed in developing mouse cerebellar granule cells. J Neurosci. 1999;19:8389-8400.
22. Kato A, Fukuda T, Fukazawa Y, et al. Phorbol esters promote postsynaptic accumulation of Vesl-1S/Homer-1a protein. Eur J Neurosci. 2001;13:1292-1302.
23. Simpkins JW, Rajakumar G, Zhang YQ, et al. Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J Neurosurg. 1997;87:724-730.
24. Dubal DB, Zhu H, Yu J, et al. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci USA. 2001;98:1952-1957.
25. Yang SH, He Z, Wu SS, et al. 17-beta estradiol can reduce secondary ischemic damage and mortality of subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2001;21:174-181.
26. Yang SH, Perez E, Cutright J, et al. Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model. J Appl Physiol. 2002;92:202-210.
27. Shi J, Bui JD, Yang SH, et al. Estrogens decrease reperfusion-associated cortical ischemic damage: a MRI analysis in a transient focal ischemia model. Stroke. 2001;32:987-992.
28. Green PS, Yang SH, Nilsson KR, Kumar AS, Covey DF, Simpkins JW. The nonfeminizing enantiomer of 17beta-estradiol exerts protective effects in neuronal cultures and a rat model of cerebral ischemia. Endocrinology. 2001;142:400-406.
29. Zhang YQ, Shi J, Rajakumar G, Day AL, Simpkins JW. Effects of gender and estradiol treatment on focal brain ischemia. Brain Res. 1998;784:321-324.
30. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD. Gender-linked brain injury in experimental stroke. Stroke. 1998;29:159-165.
31. Rusa R, Alkayed NJ, Crain BJ, et al. 17beta-estradiol reduces stroke injury in estrogen-deficient female animals. Stroke. 1999;30:1665-1670.
32. Hurn PD, Macrae IM. Estrogen as a neuroprotectant in stroke. J Cereb Blood Flow Metab. 2000;20:631-652.
33. Sawada M, Alkayed NJ, Goto S, et al. Estrogen receptor antagonist ICI182, 780 exacerbates ischemic injury in female mouse. J Cereb Blood Flow Metab. 2000;20:112-118.
34. Sampei K, Goto S, Alkayed NJ, et al. Stroke in estrogen receptor-alpha-deficient mice. Stroke. 2000;31:738-743.
35. Dubal DB, Kashon ML, Pettigrew LC, et al. Estradiol protects against ischemic injury. J Cereb Blood Flow Metab. 1998;18:1253-1258.
36. Green PS, Gridley KE, Simpkins JW. Nuclear estrogen receptor-independent neuroprotection by estratrienes: a novel interaction with glutathione. Neuroscience. 1998;84:7-10.
37. Snow KK, Seddon JM. Age-related eye diseases: impact of hormone replacement therapy, and reproductive and other risk factors. Int J Fertil Womens Med. 2000;45:301-313.
38. Tang MX, Jacobs D, Stern Y, et al. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet. 1996;348:429-432.
39. The Eye Disease Case-Control Study Group. Risk factors for neovascular age-related macular degeneration. Arch Ophthalmol. 1992;110:1701-1708.
40. The Eye Disease Case-Control Study Group. Risk factors for idiopathic macular holes. Am J Ophthalmol. 1994;118:754-761.
41. Smith W, Mitchell P, Wang JJ. Gender, oestrogen, hormone replacement and age-related macular degeneration: results from the Blue Mountains Eye Study. Aust NZ J Ophthalmol. 1997;25(suppl 1):S13-S15.
42. Nonaka A, Kiryu J, Tsujikawa A, et al. Administration of 17β-stradiol attenuates retinal ischemia-reperfusion injury in rats. Invest Ophthalmol Vis Sci. 2000;41:2689-2696.
43. Chen Q, Moulder K, Tenkova T, Hardy K, Olney JW, Romano C. Excitotoxic cell death dependent on inhibitory receptor activation. Exp Neurol. 1999;160:215-225.
44. Macaione S, Ientile R, Lentini M, Di Giorgio RM. Effects of estrogens and progesterone on GABA system in ovariectomized rat retina. Ital J Biochem. 1981;30:279-289.
45. Harris-Yitzhak M, Harris A, Ben-Refael Z, Zarfati D, Garzozi HJ, Martin BJ. Estrogen-replacement therapy: effects on retrobulbar hemodynamics. Am J Ophthalmol. 2000;129:623-628.
46. Shi J, Simpkins JW. 17 beta-Estradiol modulation of glucose transporter 1 expression in blood-brain barrier. Am J Physiol. 1997;272:E1016-E1022.
47. Brandstätter JH, Koulen P, Kuhn R, van der Putten H, Wässle H. Compartmental localization of a metabotropic glutamate receptor (mGluR7): two different active sites at a retinal synapse. J Neurosci. 1996;16:4749-4756.
48. Koulen P, Kuhn R, Wässle H, Brandstätter JH. Group I metabotropic glutamate receptors mGluR1a and mGluR5a: localization in both synaptic layers of the rat retina. J Neurosci. 1997;17:2200-2211.
49. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wassle H. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci. 1998;18:10136-10149.
50. Koulen P. Localization of synapse-associated proteins during postnatal development of the rat retina. Eur J Neurosci. 1999;11:2007-2018.
51. Koulen P, Garner CC, Wassle H. Immunocytochemical localization of the synapse-associated protein SAP102 in the rat retina. J Comp Neurol. 1998;397:326-336.
52. Dowling JE, Boycott BB. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci. 1966;166:80-111.
53. Famiglietti EV, Kolb H. A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res. 1975;84:293-300.
54. Chun M-H, Han S-H, Chung J-W, Wässle H. Electron microscopic analysis of the rod pathway of the rat retina. J Comp Neurol. 1993;332:421-432.
55. Wiechmann AF, O'Steen WK. Melatonin increases photoreceptor susceptibility to light-induced damage. Invest Ophthalmol Vis Sci. 1992;33:1894-1902.
56. Nathan L, Chaudhuri G. Antioxidant and prooxidant actions of estrogens: potential physiological and clinical implications. Semin Reprod Endocrinol. 1998;16:309-314.
57. Schwenke DC. Aging, menopause, and free radicals. Semin Reprod Endocrinol. 1998;16:281-308.
58. Stefansson E, Wilson CA, Schoen T, Kuwabara T. Experimental ischemia induces cell mitosis in the adult rat retina. Invest Ophthalmol Vis Sci. 1988;29:1050-11055.
59. Tsujikawa A, Ogura Y, Hiroshiba N, Miyamoto K, Kiryu J, Honda Y. Tacrolimus (FK506) attenuates leukocyte accumulation after transient retinal ischemia. Stroke. 1998;29:1431-1438.
60. Hughes WF. Quantitation of ischemic damage in the rat retina. Exp Eye Res. 1991;53:573-582.
61. Hayashi A, Weinberger AW, Kim HC, de Juan E Jr. Genistein, a protein tyrosine kinase inhibitor ameliorates retinal degeneration after ischemia-reperfusion injury in rat. Invest Ophthalmol Vis Sci. 1997;38:1193-1202.
62. Weber M, Mohand-Said S, Hicks D, Dreyfus H, Sahel JA. Monosialoganglioside GM1 reduces ischemia-reperfusion-induced injury in the rat retina. Invest Ophthalmol Vis Sci. 1996;37:267-273.
63. Weishaupt JH, Bahr M. Degeneration of axotomized retinal ganglion cells as a model for neuronal apoptosis in the central nervous system - molecular death and survival pathways. Restor Neurol Neurosci. 2001;19:19-27.
64. Watanabe M, Sawai H, Fukuda Y. Survival of axotomized retinal ganglion cells in adult mammals. Clin Neurosci. 1997;4:233-239.
65. McKinnon SJ. Glaucoma, apoptosis, and neuroprotection. Curr Opin Ophthalmol. 1997;8:28-37.
66. Rabbani O, Panickar KS, Rajakumar G, et al. 17 beta-estradiol attenuates fimbrial lesion-induced decline of ChAT-immunoreactive neurons in the rat medial septum. Exp Neurol. 1997;146:179-186.
67. Tanzer L, Jones KJ. Gonadal steroid regulation of hamster facial nerve regeneration: effects of dihydrotestosterone and estradiol. Exp Neurol. 1997;146:258-264.