Mislocalized opsin and cAMP signaling: A mechanism for sprouting by rod cells in retinal degeneration

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 10, 2012, Pages 6355-6369

  Wang, Jianfeng ^a   Zhang, Nan ^a   Beuve, Annie ^a   Townes Anderson, Ellen ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE RECEPTOR; ADENYLATE CYCLASE; BETA IONONE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE RECEPTOR; G PROTEIN COUPLED RECEPTOR; OPSIN; SYNAPTOPHYSIN; BETA-IONONE; FORSKOLIN; NORISOPRENOID; SCOTOPSIN;

AGONIST; AMBYSTOMA; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITOMETRY; IMMUNOCYTOCHEMISTRY; NERVE CELL GROWTH; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIOIMMUNOASSAY; REGULATORY MECHANISM; RETINA DEGENERATION; RETINA ROD; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; METABOLISM; NEURITE; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PSEUDOPODIUM;

ADENYLATE CYCLASE; AMBYSTOMA; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FORSKOLIN; HUMANS; NEURITES; NORISOPRENOIDS; PHOSPHORYLATION; PSEUDOPODIA; RECEPTORS, DOPAMINE; RECEPTORS, PURINERGIC P1; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS; ROD OPSINS; SIGNAL TRANSDUCTION;

EID: 84871682541     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-10180     Document Type: Article

References (91)

1. Kerschensteiner M, Bareyre FM, Buddeberg BS, et al. Remodeling of axonal connections contributes to recovery in an animal model of multiple sclerosis. J Exp Med. 2004;200: 1027-1038.
2. Masliah E, Hansen L, Mallory M, Albright T, Terry RD. Abnormal brain spectrin immunoreactivity in sprouting neurons in Alzheimer disease. Neurosci Lett. 1991;129:1-5.
3. Geddes JW, Anderson KJ, Cotman CW. Senile plaques as aberrant sprout-stimulating structures. Exp Neurol. 1986;94: 767-776.
4. Dahl D, Perides G, Bignami A. Axonal regeneration in old multiple sclerosis plaques: immunohistochemical study with monoclonal antibodies to phosphorylated and non-phosphorylated neurofilament proteins. Acta Neuropathol. 1989;79: 154-159.
5. Li ZY, Kljavin IJ, Milam AH. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci. 1995;15:5429-5438.
6. John SK, Smith JE, Aguirre GD, Milam AH. Loss of cone molecular markers in rhodopsin-mutant human retinas with retinitis pigmentosa. Mol Vis. 2000;6:204-215.
7. Fariss RN, Li ZY, Milam AH. Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. Am J Ophthalmol. 2000;129:215-223.
8. Gupta N, Brown KE, Milam AH. Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and agerelated macular degeneration. Exp Eye Res. 2003;76:463-471.
9. Xiao M, Sastry SM, Li ZY, et al. Effects of retinal laser photocoagulation on photoreceptor basic fibroblast growth factor and survival. Invest Ophthalmol Vis Sci. 1998;39:618-630.
10. Lewis GP, Charteris DG, Sethi CS, Leitner WP, Linberg KA, Fisher SK. The ability of rapid retinal reattachment to stop or reverse the cellular and molecular events initiated by detachment. Invest Ophthalmol Vis Sci. 2002;43:2412-2420.
11. Sethi CS, Lewis GP, Fisher SK, et al. Glial remodeling and neural plasticity in human retinal detachment with proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci. 2005;46: 329-342.
12. Fei Y. Cone neurite sprouting: an early onset abnormality of the cone photoreceptors in the retinal degeneration mouse. Mol Vis. 2002;8:306-314.
13. Tam BM, Xie G, Oprian DD, Moritz OL. Mislocalized rhodopsin does not require activation to cause retinal degeneration and neurite outgrowth in Xenopus laevis. J Neurosci. 2006;26: 203-209.
14. Chong NH, Alexander RA, Barnett KC, Bird AC, Luthert PJ. An immunohistochemical study of an autosomal dominant feline rod/cone dysplasia (Rdy cats). Exp Eye Res. 1999;68:51-57.
15. Li ZY, Wong F, Chang JH, et al. Rhodopsin transgenic pigs as a model for human retinitis pigmentosa. Invest Ophthalmol Vis Sci. 1998;39:808-819.
16. Zhang N, Beuve A, Townes-Anderson E. The nitric oxide-cGMP signaling pathway differentially regulates presynaptic structural plasticity in cone and rod cells. J Neurosci. 2005;25: 2761-2770.
17. Hannila SS, Filbin MT. The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol. 2008;209:321-332.
18. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science. 2001;294: 1030-1038.
19. Alfinito PD, Townes-Anderson E. Activation of mislocalized opsin kills rod cells: a novel mechanism for rod cell death in retinal disease. Proc Natl Acad Sci U S A. 2002;99:5655-5660.
20. MacLeish PR, Townes-Anderson E. Growth and synapse formation among major classes of adult salamander retinal neurons in vitro. Neuron. 1988;1:751-760.
21. Fontainhas AM, Townes-Anderson E. RhoA and its role in synaptic structural plasticity of isolated salamander photoreceptors. Invest Ophthalmol Vis Sci. 2008;49:4177-4187.
22. Zhang N, Townes-Anderson E. Regulation of structural plasticity by different channel types in rod and cone photoreceptors. J Neurosci. 2002;22:7065-7079.
23. Nir I, Papermaster DS. Immunocytochemical localization of opsin in degenerating photoreceptors of RCS rats and rd and rds mice. Prog Clin Biol Res. 1989;314:251-264.
24. Roof DJ, 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.
25. Mandell JW, MacLeish PR, Townes-Anderson E. Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro. J Neurosci. 1993;13:3533-3548.
26. Rothermel JD, Parker Botelho LH. A mechanistic and kinetic analysis of the interactions of the diastereoisomers of adenosine 3', 5'-(cyclic)phosphorothioate with purified cyclic AMP-dependent protein kinase. Biochem J. 1988;251:757-762.
27. Dostmann WR, Taylor SS, Genieser HG, Jastorff B, Doskeland SO, Ogreid D. Probing the cyclic nucleotide binding sites of cAMP-dependent protein kinases I and II with analogs of adenosine 3', 5'-cyclic phosphorothioates. J Biol Chem. 1990; 265:10484-10491.
28. Taylor SS, Kim C, Vigil D, et al. Dynamics of signaling by PKA. Biochim Biophys Acta. 2005;1754:25-37.
29. Hanoune J, Defer N. Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol. 2001;41:145-174.
30. Xia Z, Choi EJ, Wang F, Blazynski C, Storm DR. Type I calmodulin-sensitive adenylyl cyclase is neural specific. J Neurochem. 1993;60:305-311.
31. Jackson CR, Chaurasia SS, Zhou H, Haque R, Storm DR, Iuvone PM. Essential roles of dopamine D4 receptors and the type 1 adenylyl cyclase in photic control of cyclic AMP in photoreceptor cells. J Neurochem. 2009;109:148-157.
32. Lippe C, Ardizzone C. Actions of vasopressin and isoprenaline on the ionic transport across the isolated frog skin in the presence and the absence of adenyl cyclase inhibitors MDL12330A and SQ22536. Comp Biochem Physiol C. 1991; 99:209-211.
33. Kvanta A, Seregard S, Sejersen S, Kull B, Fredholm BB. Localization of adenosine receptor messenger RNAs in the rat eye. Exp Eye Res. 1997;65:595-602.
34. Rey HL, Burnside B. Adenosine stimulates cone photoreceptor myoid elongation via an adenosine A2-like receptor. J Neurochem. 1999;72:2345-2355.
35. Alfinito PD, Alli R, Townes-Anderson E. Adenosine A(2a) receptor-mediated inhibition of rod opsin mRNA expression in tiger salamander. J Neurochem. 2002;83:665-672.
36. Iuvone PM, Valenciano AI, Alonso-Gomez AI. Adenosine: a circadian modulator of melatonin biosynthesis in Xenopus photoreceptor cells. Invest Ophthalmol Vis Sci. 2000;41: S112-S112.
37. Jarvis MF, Schulz R, Hutchison AJ, Do UH, Sills MA, Williams M. [3H]CGS 21680, a selective A2 adenosine receptor agonist directly labels A2 receptors in rat brain. J Pharmacol Exp Ther. 1989;251:888-893.
38. Cohen AI, Blazynski C. Dopamine and its agonists reduce a light-sensitive pool of cyclic AMP in mouse photoreceptors. Vis Neurosci. 1990;4:43-52.
39. Iuvone PM, Ivanova TN, Alonso-Gomez AL. Dopamine D4 receptors regulate intracellular calcium concentration in cultured chicken cone photoreceptor cells: relationship to dopamine receptor-mediated inhibition of cAMP formation. Brain Res. 2008;1207:111-119.
40. Patel S, Chapman KL, Marston D, Hutson PH, Ragan CI. Pharmacological and functional characterisation of dopamine D4 receptors in the rat retina. Neuropharmacology. 2003;44: 1038-1046.
41. Rosenberg D, Groussin L, Jullian E, Perlemoine K, Bertagna X, Bertherat J. Role of the PKA-regulated transcription factor CREB in development and tumorigenesis of endocrine tissues. Ann N Y Acad Sci. 2002;968:65-74.
42. Lewis GP, Erickson PA, Anderson DH, Fisher SK. Opsin distribution and protein incorporation in photoreceptors after experimental retinal detachment. Exp Eye Res. 1991;53:629-640.
43. Kefalov VJ, Carter Cornwall M, Crouch RK. Occupancy of the chromophore binding site of opsin activates visual transduction in rod photoreceptors. J Gen Physiol. 1999;113:491-503.
44. Sherry DM, Bui DD, Degrip WJ. Identification and distribution of photoreceptor subtypes in the neotenic tiger salamander retina. Vis Neurosci. 1998;15:1175-1187.
45. Jin J, Crouch RK, Corson DW, Katz BM, MacNichol EF, Cornwall MC. Noncovalent occupancy of the retinal-binding pocket of opsin diminishes bleaching adaptation of retinal cones. Neuron. 1993;11:513-522.
46. Spencer M, Detwiler PB, Bunt-Milam AH. Distribution of membrane proteins in mechanically dissociated retinal rods. Invest Ophthalmol Vis Sci. 1988;29:1012-1020.
47. Khodair MA, Zarbin MA, Townes-Anderson E. Cyclic AMP prevents retraction of axon terminals in photoreceptors prepared for transplantation: an in vitro study. Invest Ophthalmol Vis Sci. 2005;46:967-973.
48. Cornwall MC, Fain GL. Bleached pigment activates transduction in isolated rods of the salamander retina. J Physiol. 1994; 480(pt 2):261-279.
49. Han J, Han L, Tiwari P, Wen Z, Zheng JQ. Spatial targeting of type II protein kinase A to filopodia mediates the regulation of growth cone guidance by cAMP. J Cell Biol. 2007;176:101-111.
50. Josselyn SA, Nguyen PV. CREB, synapses and memory disorders: past progress and future challenges. Curr Drug Targets CNS Neurol Disord. 2005;4:481-497.
51. Townes-Anderson E. Intersegmental fusion in vertebrate rod photoreceptors: rod cell structure revisited. Invest Ophthalmol Vis Sci. 1995;36:1918-1933.
52. Beltran WA, Allore HG, Johnson E, et al. CREB1/ATF1 activation in photoreceptor degeneration and protection. Invest Ophthalmol Vis Sci. 2009;50:5355-5363.
53. Geller SF, Lewis GP, Fisher SK. FGFR1, signaling, and AP-1 expression after retinal detachment: reactive Muller and RPE cells. Invest Ophthalmol Vis Sci. 2001;42:1363-1369.
54. Lolley RN, Schmidt SY, Farber DB. Alterations in cyclic AMP metabolism associated with photoreceptor cell degeneration in the C3H mouse. J Neurochem. 1974;22:701-707.
55. Weiss ER, Hao Y, Dickerson CD, et al. Altered cAMP levels in retinas from transgenic mice expressing a rhodopsin mutant. Biochem Biophys Res Commun. 1995;216:755-761.
56. Nir I, Haque R, Iuvone PM. Regulation of cAMP by light and dopamine receptors is dysfunctional in photoreceptors of dystrophic retinal degeneration slow(rds) mice. Exp Eye Res. 2001;73:265-272.
57. Traverso V, Bush RA, Sieving PA, Deretic D. Retinal cAMP levels during the progression of retinal degeneration in rhodopsin P23H and S334ter transgenic rats. Invest Ophthalmol Vis Sci. 2002;43:1655-1661.
58. Harada T, Imaki J, Hagiwara M, et al. Phosphorylation of CREB in rat retinal cells after focal retinal injury. Exp Eye Res. 1995; 61:769-772.
59. Paquet-Durand F, Azadi S, Hauck SM, Ueffing M, van Veen T, Ekstrom P. Calpain is activated in degenerating photoreceptors in the rd1 mouse. J Neurochem. 2006;96:802-814.
60. Deretic D. A role for rhodopsin in a signal transduction cascade that regulates membrane trafficking and photoreceptor polarity. Vision Res. 2006;46:4427-4433.
61. Nachury MV, Seeley ES, Jin H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol. 2010;26:59-87.
62. Sung CH, 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.
63. Ishiguro S, Fukuda K, Kanno C, Mizuno K. Accumulation of immunoreactive opsin on plasma membranes in degenerating rod cells of rd/rd mutant mice. Cell Struct Funct. 1987;12: 141-155.
64. Nir I, Sagie G, Papermaster DS. Opsin accumulation in photoreceptor inner segment plasma membranes of dystrophic RCS rats. Invest Ophthalmol Vis Sci. 1987;28:62-69.
65. Nir I, Agarwal N, Sagie G, Papermaster DS. Opsin distribution and synthesis in degenerating photoreceptors of rd mutant mice. Exp Eye Res. 1989;49:403-421.
66. Agarwal N, Nir I, Papermaster DS. Opsin synthesis and mRNA levels in dystrophic retinas devoid of outer segments in retinal degeneration slow (rds) mice. J Neurosci. 1990;10:3275-3285.
67. Schalken JJ, Janssen JJ, Sanyal S, Hawkins RK, de Grip WJ. Development and degeneration of retina in rds mutant mice: immunoassay of the rod visual pigment rhodopsin. Biochim Biophys Acta. 1990;1033:103-109.
68. Marc RE, Murry RF, Fisher SK, Linberg KA, Lewis GP. Amino acid signatures in the detached cat retina. Invest Ophthalmol Vis Sci. 1998;39:1694-1702.
69. Lewis GP, Sethi CS, Linberg KA, Charteris DG, Fisher SK. Experimental retinal reattachment: a new perspective. Mol Neurobiol. 2003;28:159-175.
70. Mervin K, Valter K, Maslim J, Lewis G, Fisher S, Stone J. Limiting photoreceptor death and deconstruction during experimental retinal detachment: the value of oxygen supplementation. Am J Ophthalmol. 1999;128:155-164.
71. Rattner A, Toulabi L, Williams J, Yu H, Nathans J. The genomic response of the retinal pigment epithelium to light damage and retinal detachment. J Neurosci. 2008;28:9880-9889.
72. Sunahara RK, Beuve A, Tesmer JJ, Sprang SR, Garbers DL, Gilman AG. Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J Biol Chem. 1998; 273:16332-16338.
73. Burnside B, Basinger S. Retinomotor pigment migration in the teleost retinal pigment epithelium. II. Cyclic-3', 5'-adenosine monophosphate induction of dark-adaptive movement in vitro. Invest Ophthalmol Vis Sci. 1983;24:16-23.
74. Mattson MP, Taylor-Hunter A, Kater SB. Neurite outgrowth in individual neurons of a neuronal population is differentially regulated by calcium and cyclic AMP. J Neurosci. 1988;8: 1704-1711.
75. Benfey M, Bunger UR, Vidal-Sanz M, Bray GM, Aguayo AJ. Axonal regeneration from GABAergic neurons in the adult rat thalamus. J Neurocytol. 1985;14:279-296.
76. Lyon MJ, Stelzner DJ. Tests of the regenerative capacity of tectal efferent axons in the frog, Rana pipiens. J Comp Neurol. 1987;255:511-525.
77. Kater SB, Mills LR. Regulation of growth cone behavior by calcium. J Neurosci. 1991;11:891-899.
78. Lopes VS, Jimeno D, Khanobdee K, et al. Dysfunction of heterotrimeric kinesin-2 in rod photoreceptor cells and the role of opsin mislocalization in rapid cell death. Mol Biol Cell. 2010;21:4076-4088.
79. Bitensky MW, Wheeler MA, Rasenick MM, et al. Functional exchange of components between light-activated photoreceptor phosphodiesterase and hormone-activated adenylate cyclase systems. Proc Natl Acad Sci U S A. 1982;79:3408-3412.
80. Muschietti JP, Bianchini GM, Martinetto HE, et al. Reconstitution of a light-stimulated adenylate cyclase from retina and Neurospora crassa preparations: characterization of the heterologous systems using normal and degenerative retinas. Eur J Biochem. 1989;185:205-210.
81. Dickerson CD, Weiss ER. The coupling of pertussis toxinsensitive G proteins to phospholipase A2 and adenylyl cyclase in CHO cells expressing bovine rhodopsin. Exp Cell Res. 1995; 216:46-50.
82. Concepcion F, Mendez A, Chen J. The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vision Res. 2002;42:417-426.
83. Tan E, Wang Q, Quiambao AB, et al. The relationship between opsin overexpression and photoreceptor degeneration. Invest Ophthalmol Vis Sci. 2001;42:589-600.
84. Nakao T, Tsujikawa M, Notomi S, Ikeda Y, Nishida K. The role of mislocalized phototransduction in photoreceptor cell death of retinitis pigmentosa. PLoS One. 2012;7:e32472. Available at: http: //www.plosone.org/article/info%3Adoi%2F10. 1371%2Fjournal.pone.0032472. Accessed July 19, 2012.
85. Concepcion F, Chen J. Q344ter mutation causes mislocalization of rhodopsin molecules that are catalytically active: a mouse model of Q344ter-induced retinal degeneration. PLoS One. 2010;5:e10904. Available at: http://www.plosone.org/ article/info%3Adoi%2F10.1371%2Fjournal.pone.0010904. Accessed July 19, 2012.
86. Terakita A, Tsukamoto H, Koyanagi M, Sugahara M, Yamashita T, Shichida Y. Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. J Neurochem. 2008;105:883-890.
87. Yau KW, Hardie RC. Phototransduction motifs and variations. Cell. 2009;139:246-264.
88. Peng YW, Rhee SG, Yu WP, et al. Identification of components of a phosphoinositide signaling pathway in retinal rod outer segments. Proc Natl Acad Sci U S A. 1997;94:1995-2000.
89. Kurimoto T, Yin Y, Omura K, et al. Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J Neurosci. 2010; 30:15654-15663.
90. Kandel ER. The molecular biology of memory storage: a dialog between genes and synapses. Biosci Rep. 2001;21:565-611.
91. Nir I, Cohen D, Papermaster DS. Immunocytochemical localization of opsin in the cell membrane of developing rat retinal photoreceptors. J Cell Biol. 1984;98:1788-1795.