Late-onset inner retinal dysfunction in mice lacking sigma receptor 1 (σR1)

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 10, 2011, Pages 7749-7760

  Ha, Yonju ^a   Saul, Alan ^a   Tawfik, Amany ^a   Williams, Cory ^a   Bollinger, Kathryn ^a   Smith, Robert ^a   Tachikawa, Masanori ^b   Zorrilla, Eric ^c   Ganapathy, Vadivel ^a   Smith, Sylvia B ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF TOYAMA   (Japan)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; SIGMA 1 OPIATE RECEPTOR; CASP3 PROTEIN, MOUSE; MESSENGER RNA; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B WAVE; BLOOD VESSEL PERMEABILITY; CELL LOSS; CONTROLLED STUDY; DNA FRAGMENTATION; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; MICROSCOPY; MOUSE; NICK END LABELING; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RETINA DISEASE; RETINA FOVEA; RETINA NEOVASCULARIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DISEASE MODEL; ELECTRORETINOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE; GENOTYPE; METABOLISM; MOUSE MUTANT; NERVE FIBER; OPTIC DISK; OPTIC NERVE DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA; RETINA GANGLION CELL; ULTRASTRUCTURE;

ANIMALS; AXONS; BLOTTING, WESTERN; CASPASE 3; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION; GENOTYPE; IN SITU NICK-END LABELING; INTRAOCULAR PRESSURE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OPTIC DISK; OPTIC NERVE DISEASES; RECEPTORS, SIGMA; RETINA; RETINAL DISEASES; RETINAL GANGLION CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84862833548     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8169     Document Type: Article

References (43)

1. Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell. 2007;131:596-610.
2. Ola MS, Moore PM, El-Sherbeny A, et al. Expression pattern of sigma receptor 1 mRNA and protein in mammalian retina. Mol Brain Res. 2001;95:86-95.
3. Schoenwald RD, Barfknecht CF, Xia E, Newton RE. The presence of sigma-receptors in the lacrimal gland. J Ocul Pharmacol. 1993;9:125-139.
4. Bucolo C, Campana G, Di Toro R, Cacciaguerra S, Spampinato S. Sigma 1 recognition sites in rabbit iris-ciliary body: topical sigma 1-site agonists lower intraocular pressure. J Pharmacol Exp Ther. 1999;289:1362-1369.
5. Campana G, Bucolo C, Murari G, Spampinato S. Ocular hypotensive action of topical flunarizine in the rabbit: role of sigma 1 recognition sites. J Pharmacol Exp Ther. 2002;303:1086-1094.
6. Wang L, Duncan G. Silencing of sigma-1 receptor induces cell death in human lens cells. Exp Cell Res. 2006;312:1439-1446.
7. Wang L, Prescott AR, Spruce BA, Sanderson J, Duncan G. Sigma receptor antagonists inhibit human lens cell growth and induce pigmentation. Invest Ophthalmol Vis Sci. 2005;46:1403-1408.
8. Senda T, Matsuno K, Mita S. The presence of sigma receptor subtypes in bovine retinal membranes. Exp Eye Res. 1997;64:857-860.
9. Ola MS, Moore P, Maddox D, et al. Analysis of sigma receptor (σR1) expression in retinal ganglion cells cultured under hyperglycemic conditions and in diabetic mice. Mol Brain Res. 2002;107:97-107.
10. Liu LL, Wang L, Zhong YM, Yang XL. Expression of sigma receptor 1 mRNA and protein in rat retina. Neuroscience. 2010;167:1151-1159.
11. Mavlyutov TA, Nickells RW, Guo LW. Accelerated retinal ganglion cell death in mice deficient in the sigma-1 receptor. Mol Vis. 2011;17:1034-1043.
12. Jiang G, Mysona B, Dun Y, et al. Expression, subcellular localization and regulation of sigma receptor in retinal Müller cells. Invest Ophthalmol Vis Sci. 2006;47:5576-5582.
13. Ha Y, Dun Y, Thangaraju M, Ganapathy V, Smith SB. Sigma receptor 1 modulates ER stress in retinal neurons. Invest Ophthalmol Vis Sci. 2011;52:527-540.
14. Martin PM, Ola MS, Agarwal N, Ganapathy V, Smith SB. The sigma receptor ligand (+)-pentazocine prevents apoptotic retinal ganglion cell death induced in vitro by homocysteine and glutamate. Mol Brain Res. 2004;123:66-75.
15. Dun Y, Thangaraju M, Prasad P, Ganapathy V, Smith SB. Prevention of excitotoxicity in primary retinal ganglion cells by (+)-pentazocine, a sigma receptor-1 specific ligand. Invest Ophthalmol Vis Sci. 2007;48:4785-4794.
16. Smith SB, Duplantier JN, Dun Y, et al. In vivo protection against retinal neurodegeneration by the sigma receptor 1 ligand (+)-pentazocine. Invest Ophthalmol Vis Sci. 2008;49:4154-4161.
17. Tchedre KT, Huang RQ, Dibas A, et al. Sigma-1 receptor regulation of voltage-gated calcium channels involves a direct interaction. Invest Ophthalmol Vis Sci. 2008;49:4993-5002.
18. Zhang XJ, Liu LL, Jiang SX, Zhong YM, Yang XL. Activation of the sigma receptor 1 suppresses NMDA responses in rat retinal ganglion cells. Neuroscience. 2011;177:12-22.
19. Sabino V, Cottone P, Parylak SL, Steardo L, Zorrilla EP. Sigma-1 receptor knockout mice display a depressive-like phenotype. Behav Brain Res. 2009;198:472-476.
20. Moore P, El-Sherbeny A, Roon P, et al. Apoptotic retinal ganglion cell death is induced in vivo by the excitatory amino acid homocysteine. Exp Eye Res. 2001;73:45-47.
21. Bucolo C, Drago F, Lin LR, Reddy VN. Sigma receptor ligands protect human retinal cells against oxidative stress. Neuroreport. 2006;17:287-291.
22. Sieving PA, Frishman LJ, Steinberg RH. Scotopic threshold response of proximal retina in cat. J Neurophysiol. 1986;56:1049-1061.
23. Saszik SM, Robson JG, Frishman LJ. The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J Physiol. 2002;543:899-916.
24. Seiji M, Iwashita S. On the site of melanin formation in melanocytes. J Biochem Tokyo. 1963;54:465-467.
25. May CA, Lütjen-Drecoll E. Morphology of the murine optic nerve. Invest Ophthalmol Vis Sci. 2002;43:2206-2212.
26. Howell GR, Libby RT, Jakobs TC, et al. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J Cell Biol. 2007;179:1523-1537.
27. Ruiz-Ederra J, Garcia M, Hicks D, Vecino E. Comparative study of the three neurofilament subunits within pig and human retinal ganglion cells, Mol Vis. 2004;10:83-92.
28. Maurice T, Su TP. The pharmacology of sigma-1 receptors. Pharmacol Ther. 2009;124:195-206.
29. Langa F, Codony X, Tovar V, et al. Generation and phenotypic analysis of sigma receptor type I (sigma 1) knockout mice. Eur J Neurosci. 2003;18:2188-2196.
30. Cendán CM, Pujalte JM, Portillo-Salido E, Montoliu L, Baeyens JM. Formalin-induced pain is reduced in sigma(1) receptor knockout mice. Eur J Pharmacol. 2005;511:73-74.
31. Entrena JM, Cobos EJ, Nieto FR, et al. Sigma-1 receptors are essential for capsaicin-induced mechanical hypersensitivity: studies with selective sigma-1 ligands and sigma-1 knockout mice. Pain. 2009;143:252-261.
32. de la Puente B, Nadal X, Portillo-Salido E, et al. Sigma-1 receptors regulate activity-induced spinal sensitization and neuropathic pain after peripheral nerve injury. Pain. 2009;145:294-303.
33. Fontanilla D, Johannessen M, Hajipour AR, et al. The hallucinogen N, N-dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator. Science. 2009;323:934-937.
34. Mavlyutov TA, Epstein ML, Andersen KA, Ziskind-Conhaim L, Ruoho AE. The sigma-1 receptor is enriched in postsynaptic sites of C-terminals in mouse motoneurons: an anatomical and behavioral study. Neuroscience. 2010;167:247-255.
35. Johannessen M, Ramachandran S, Riemer L, et al. Voltage-gated sodium channel modulation by sigma-receptors in cardiac myocytes and heterologous systems. Am J Physiol Cell Physiol. 2009;296:C1049-1057.
36. Frishman LJ, Wang MH. Electroretinogram of human, monkey and mouse. In: Levin LA, Nilsson SFE, Ver Hoeve J, Wu S, Kaufman PL, Alm A. Adler's Physiology of the Eye. 11th ed. New York: Saunders Elsevier; 2011:480-501.
37. Crish SD, Calkins DJ. Neurodegeneration in glaucoma: progression and calcium-dependent intracellular mechanisms. Neuroscience. 2011;176:1-11.
38. Clapham DE. Calcium signaling. Cell. 1995;80:259-268.
39. 2+stores: activation and function. Trends Neurosci. 1995;18:299-306.
40. Berridge MJ, Bootman MD, Lipp P. Calcium: a life and death signal. Nature. 1998;395:645-648.
41. Wu Z, Bowen WD. Role of sigma-1 receptor C-terminal segment in inositol 1,4,5-trisphosphate receptor activation: constitutive enhancement of calcium signaling in MCF-7 tumor cells. J Biol Chem. 2008;283:28198-28215.
42. Tchedre KT, Yorio T. Sigma-1 receptors protect RGC-5 cells from apoptosis by regulating intracellular calcium, Bax levels, and caspase-3 activation. Invest Ophthalmol Vis Sci. 2008;49:2577-2588.
43. Kim I, Xu W, Reed JC. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov. 2008;7:1013-1030.