Early Alteration of Retinal Neurons in Aipl1 -/- Animals

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 5, 2014, Pages 3081-3092

  Singh, Ratnesh Kumar ^a   Kolandaivelu, Saravanan ^a   Ramamurthy, Visvanathan ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Childhood blindness; LCA; Photoreceptor degeneration; Remodeling; Retina

Indexed keywords

CALBINDIN; GLIAL FIBRILLARY ACIDIC PROTEIN; METABOTROPIC RECEPTOR 6; SECRETAGOGIN; SYNAPTOPHYSIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M1; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL TISSUE; ARTICLE; ARYL HYDROCARBON RECEPTOR INTERACTING PROTEIN LIKE 1 GENE; CELL LOSS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; GENE; GLIOSIS; HISTOLOGY; IMMUNOCYTOCHEMISTRY; MOUSE; MUELLER CELL; NERVE CELL DEGENERATION; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA HORIZONTAL NERVE CELL; RETINA INNER PLEXIFORM LAYER; RETINA NERVE CELL; RETINA ROD;

CHILDHOOD BLINDNESS; LCA; PHOTORECEPTOR DEGENERATION; REMODELING; RETINA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PHOSPHOPROTEINS; RETINAL DISEASES; RETINAL NEURONS; SYNAPTIC MEMBRANES;

EID: 84900794469     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13728     Document Type: Article

References (51)

1. Masland RH. The fundamental plan of the retina. NatNeurosci. 2001;4:877-886.
2. Masland RH. Neuronal diversity in the retina. Curr OpinNeurobiol. 2001;11:431-436.
3. Masland RH. The neuronal organization of the retina. Neuron.2012;76:266-280.
4. Jones BW, Kondo M, Terasaki H, Lin Y, McCall M, Marc RE. Retinal remodeling. Jpn J Ophthalmol. 2012;56:289-306.
5. Jones BW, Watt CB, Frederick JM, et al. Retinal remodelingtriggered by photoreceptor degenerations. J Comp Neurol.2003;464:1-16.
6. Marc RE, Jones BW, Anderson JR, et al. Neural reprogrammingin retinal degeneration. Invest Ophthalmol Vis Sci. 2007;48:3364-3371.
7. Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling inretinal degeneration. Prog Retin Eye Res. 2003;22:607-655.
8. Terzibasi E, Calamusa M, Novelli E, Domenici L, Strettoi E, Cellerino A. Age-dependent remodelling of retinal circuitry. Neurobiol Aging. 2009;30:819-828.
9. Fariss RN, Li ZY, Milam AH. Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas withretinitis pigmentosa. Am J Ophthalmol. 2000;129:215-223.
10. Jacobson SG, Cideciyan AV, Aleman TS, et al. Human retinaldisease from AIPL1 gene mutations: foveal cone loss withminimal macular photoreceptors and rod function remaining. Invest Ophthalmol Vis Sci. 2011;52:70-79.
11. Jacobson SG, Sumaroka A, Aleman TS, Cideciyan AV, DancigerM, Farber DB. Evidence for retinal remodelling in retinitispigmentosa caused by PDE6B mutation. Br J Ophthalmol.2007;91:699-701.
12. Strettoi E, Pignatelli V, Rossi C, Porciatti V, Falsini B. Remodeling of second-order neurons in the retina of rd/rdmutant mice. Vision Res. 2003;43:867-877.
13. Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. Morphological and functional abnormalities in the inner retinaof the rd/rd mouse. J Neurosci. 2002;22:5492-5504.
14. Carter-Dawson LD, LaVail MM, Sidman RL. Differential effect ofthe rd mutation on rods and cones in the mouse retina. InvestOphthalmol Vis Sci. 1978;17:489-498.
15. LaVail MM, Matthes MT, Yasumura D, Steinberg RH. Variabilityin rate of cone degeneration in the retinal degeneration (rd/rd)mouse. Exp Eye Res. 1997;65:45-50.
16. Lin B, Masland RH, Strettoi E. Remodeling of cone photoreceptorcells after rod degeneration in rd mice. Exp Eye Res.2009;88:589-599.
17. Chua J, Fletcher EL, Kalloniatis M. Functional remodeling ofglutamate receptors by inner retinal neurons occurs from anearly stage of retinal degeneration. J Comp Neurol. 2009;514:473-491.
18. Gargini C, Terzibasi E, Mazzoni F, Strettoi E. Retinal organizationin the retinal degeneration 10 (rd10) mutant mouse: amorphological and ERG study. J Comp Neurol. 2007;500:222-238.
19. Kuny S, Gaillard F, Mema SC, et al. Inner retina remodeling in amouse model of stargardt-like macular dystrophy (STGD3). Invest Ophthalmol Vis Sci. 2010;51:2248-2262.
20. Pignatelli V, Cepko CL, Strettoi E. Inner retinal abnormalities ina mouse model of Leber's congenital amaurosis. J CompNeurol. 2004;469:351-359.
21. Pennesi ME, Stover NB, Stone EM, Chiang PW, Weleber RG. Residual electroretinograms in young Leber congenital amaurosispatients with mutations of AIPL1. Invest Ophthalmol VisSci. 2011;52:8166-8173.
22. Ramamurthy V, Niemi GA, Reh TA, Hurley JB. Leber congenitalamaurosis linked to AIPL1: a mouse model reveals destabilizationof cGMP phosphodiesterase. Proc Natl Acad Sci U S A.2004;101:13897-13902.
23. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and diseasemechanisms. Prog Retin Eye Res. 2008;27:391-419.
24. Dharmaraj S, Leroy BP, Sohocki MM, et al. The phenotype ofLeber congenital amaurosis in patients with AIPL1 mutations. Arch Ophthalmol. 2004;122:1029-1037.
25. Sohocki MM, Perrault I, Leroy BP, et al. Prevalence of AIPL1mutations in inherited retinal degenerative disease. Mol GenetMetab. 2000;70:142-150.
26. Testa F, Surace EM, Rossi S, et al. Evaluation of Italian patientswith leber congenital amaurosis due to AIPL1 mutationshighlights the potential applicability of gene therapy. InvestOphthalmol Vis Sci. 2011;52:5618-5624.
27. van der Spuy J, Munro PM, Luthert PJ, et al. Predominant rodphotoreceptor degeneration in Leber congenital amaurosis. Mol Vis. 2005;11:542-553.
28. Kolandaivelu S, Huang J, Hurley JB, Ramamurthy V. AIPL1, aprotein associated with childhood blindness, interacts withalpha-subunit of rod phosphodiesterase (PDE6) and isessential for its proper assembly. J Biol Chem. 2009;284:30853-30861.
29. Ku CA, Chiodo VA, Boye SL, et al. Gene therapy using selfcomplementaryY733F capsid mutant AAV2/8 restores visionin a model of early onset Leber congenital amaurosis. HumMol Genet. 2011;20:4569-4581.
30. Sun X, Pawlyk B, Xu X, et al. Gene therapy with a promotertargeting both rods and cones rescues retinal degenerationcaused by AIPL1 mutations. Gene Ther. 2010;17:117-131.
31. Tan MH, Smith AJ, Pawlyk B, et al. Gene therapy for retinitispigmentosa and Leber congenital amaurosis caused by defectsin AIPL1: effective rescue of mouse models of partial andcomplete Aipl1 deficiency using AAV2/2 and AAV2/8 vectors. Hum Mol Genet. 2009;18:2099-2114.
32. Kirschman LT, Kolandaivelu S, Frederick JM, et al. The Lebercongenital amaurosis protein, AIPL1, is needed for the viabilityand functioning of cone photoreceptor cells. Hum Mol Genet.2010;19:1076-1087.
33. Dumitrescu ON, Pucci FG, Wong KY, Berson DM. Ectopicretinal ON bipolar cell synapses in the OFF inner plexiformlayer: contacts with dopaminergic amacrine cells and melanopsinganglion cells. J Comp Neurol. 2009;517:226-244.
34. Tom Dieck S, Altrock WD, Kessels MM, et al. Moleculardissection of the photoreceptor ribbon synapse: physicalinteraction of Bassoon and RIBEYE is essential for theassembly of the ribbon complex. J Cell Biol. 2005;168:825-836.
35. Koike C, Obara T, Uriu Y, et al. TRPM1 is a component of theretinal ON bipolar cell transduction channel in the mGluR6cascade. Proc Natl Acad Sci U S A. 2010;107:332-337.
36. Omori Y, Araki F, Chaya T, et al. Presynaptic dystroglycanpikachurincomplex regulates the proper synaptic connectionbetween retinal photoreceptor and bipolar cells. J Neurosci.2012;32:6126-6137.
37. Cordeiro S, Guseva D, Wulfsen I, Bauer CK. Expression patternof Kv11 (Ether a-go-go-related gene; erg) K{thorn} channels in themouse retina. PLoS ONE. 2011;6:e29490.
38. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR. Vesicular neurotransmitter transporter expressionin developing postnatal rodent retina: GABA andglycine precede glutamate. J Neurosci. 2003;23:518-529.
39. Melone M, Burette A, Weinberg RJ. Light microscopicidentification and immunocytochemical characterization ofglutamatergic synapses in brain sections. J Comp Neurol.2005;492:495-509.
40. Phillips MJ, Otteson DC, Sherry DM. Progression of neuronaland synaptic remodeling in the rd10 mouse model of retinitispigmentosa. J Comp Neurol. 2010;518:2071-2089.
41. Haverkamp S, Wassle H. Immunocytochemical analysis of themouse retina. J Comp Neurol. 2000;424:1-23.
42. Puthussery T, Gayet-Primo J, Taylor WR. Localization of thecalcium-binding protein secretagogin in cone bipolar cells ofthe mammalian retina. J Comp Neurol. 2010;518:513-525.
43. Chua J, Nivison-Smith L, Fletcher EL, Trenholm S, AwatramaniGB, Kalloniatis M. Early remodeling of Muller cells in the rd/rdmouse model of retinal dystrophy. J Comp Neurol. 2013;521:2439-2453.
44. Peichl L, Gonzalez-Soriano J. Morphological types of horizontalcell in rodent retinae: a comparison of rat, mouse, gerbil, andguinea pig. Vis Neurosci. 1994;11:501-517.
45. Caporale N, Kolstad KD, Lee T, et al. LiGluR restores visualresponses in rodent models of inherited blindness. Mol Ther.2011;19:1212-1219.
46. Jones BW, Marc RE. Retinal remodeling during retinaldegeneration. Exp Eye Res. 2005;81:123-137.
47. Hendrickson A, Bumsted-O'Brien K, Natoli R, Ramamurthy V, Possin D, Provis J. Rod photoreceptor differentiation in fetaland infant human retina. Exp Eye Res. 2008;87:415-426.
48. Kolandaivelu S, Singh RK, Ramamurthy V. AIPL1, a proteinlinked to blindness, is essential for the stability of enzymesmediating cGMP metabolism in cone photoreceptor cells. Hum Mol Genet. 2013;23:1002-1012.
49. Chen M, Wang K, Lin B. Development and degeneration ofcone bipolar cells are independent of cone photoreceptors ina mouse model of retinitis pigmentosa. PLoS ONE. 2012;7:e44036.
50. Cuenca N, Pinilla I, Sauve Y, Lund R. Early changes in synapticconnectivity following progressive photoreceptor degenerationin RCS rats. Eur J Neurosci. 2005;22:1057-1072.
51. Cuenca N, Pinilla I, Sauve Y, Lu B, Wang S, Lund RD. Regressiveand reactive changes in the connectivity patterns of rod andcone pathways of P23H transgenic rat retina. Neuroscience.2004;127:301-317.