Modeling Retinal Diseases Using Genetic Approaches in Mice

  • Akiko Maeda
  • Tadao Maeda
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1753)

Abstract

Genetic mouse models mimicking human diseases have been developed and utilized for retinal research in various topics, involving anatomy, physiology, biochemistry, and pathology. The main reasons why mouse models are important for retinal research include that rodents share a key retinal homology with humans and that genetic manipulation is relatively easily applicable for mice. Here, we describe genetic mouse models, which are categorized with functions in the retina and relationship with human diseases.

Key words

Mouse Visual cycle Phototransduction Retina Photoreceptor Retinal pigment epithelium 

References

  1. 1.
    Kiser PD, Palczewski K (2016) Retinoids and retinal diseases. Annu Rev Vis Sci 2:197–234.  https://doi.org/10.1146/annurev-vision-111815-114407 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Maeda A, Palczewski K (2013) Retinal degeneration in animal models with a defective visual cycle. Drug Discov Today Dis Models 10(4):e163–e172.  https://doi.org/10.1016/j.ddmod.2014.01.001 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Maeda A, Maeda T, Imanishi Y, Sun W, Jastrzebska B, Hatala DA, Winkens HJ, Hofmann KP, Janssen JJ, Baehr W, Driessen CA, Palczewski K (2006) Retinol dehydrogenase (RDH12) protects photoreceptors from light-induced degeneration in mice. J Biol Chem 281(49):37697–37704.  https://doi.org/10.1074/jbc.M608375200 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Hessel S, Eichinger A, Isken A, Amengual J, Hunzelmann S, Hoeller U, Elste V, Hunziker W, Goralczyk R, Oberhauser V, von Lintig J, Wyss A (2007) CMO1 deficiency abolishes vitamin a production from beta-carotene and alters lipid metabolism in mice. J Biol Chem 282(46):33553–33561.  https://doi.org/10.1074/jbc.M706763200 CrossRefPubMedGoogle Scholar
  5. 5.
    Amengual J, Gouranton E, van Helden YG, Hessel S, Ribot J, Kramer E, Kiec-Wilk B, Razny U, Lietz G, Wyss A, Dembinska-Kiec A, Palou A, Keijer J, Landrier JF, Bonet ML, von Lintig J (2011) Beta-carotene reduces body adiposity of mice via BCMO1. PLoS One 6(6):e20644.  https://doi.org/10.1371/journal.pone.0020644 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Amengual J, Lobo GP, Golczak M, Li HN, Klimova T, Hoppel CL, Wyss A, Palczewski K, von Lintig J (2011) A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J 25(3):948–959.  https://doi.org/10.1096/fj.10-173906 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Quadro L, Blaner WS, Salchow DJ, Vogel S, Piantedosi R, Gouras P, Freeman S, Cosma MP, Colantuoni V, Gottesman ME (1999) Impaired retinal function and vitamin a availability in mice lacking retinol-binding protein. EMBO J 18(17):4633–4644.  https://doi.org/10.1093/emboj/18.17.4633 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Seeliger MW, Biesalski HK, Wissinger B, Gollnick H, Gielen S, Frank J, Beck S, Zrenner E (1999) Phenotype in retinol deficiency due to a hereditary defect in retinol binding protein synthesis. Invest Ophthalmol Vis Sci 40(1):3–11PubMedGoogle Scholar
  9. 9.
    Cukras C, Gaasterland T, Lee P, Gudiseva HV, Chavali VR, Pullakhandam R, Maranhao B, Edsall L, Soares S, Reddy GB, Sieving PA, Ayyagari R (2012) Exome analysis identified a novel mutation in the RBP4 gene in a consanguineous pedigree with retinal dystrophy and developmental abnormalities. PLoS One 7(11):e50205.  https://doi.org/10.1371/journal.pone.0050205 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Kelly M, von Lintig J (2015) STRA6: role in cellular retinol uptake and efflux. Hepatobiliary Surg Nutr 4(4):229–242.  https://doi.org/10.3978/j.issn.2304-3881.2015.01.12 PubMedPubMedCentralGoogle Scholar
  11. 11.
    Saari JC, Nawrot M, Garwin GG, Kennedy MJ, Hurley JB, Ghyselinck NB, Chambon P (2002) Analysis of the visual cycle in cellular retinol-binding protein type I (CRBPI) knockout mice. Invest Ophthalmol Vis Sci 43(6):1730–1735PubMedGoogle Scholar
  12. 12.
    Imanishi Y, Batten ML, Piston DW, Baehr W, Palczewski K (2004) Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J Cell Biol 164(3):373–383.  https://doi.org/10.1083/jcb.200311079 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Thompson DA, Li Y, McHenry CL, Carlson TJ, Ding X, Sieving PA, Apfelstedt-Sylla E, Gal A (2001) Mutations in the gene encoding lecithin retinol acyltransferase are associated with early-onset severe retinal dystrophy. Nat Genet 28(2):123–124.  https://doi.org/10.1038/88828 CrossRefPubMedGoogle Scholar
  14. 14.
    Batten ML, Imanishi Y, Maeda T, DC T, Moise AR, Bronson D, Possin D, Van Gelder RN, Baehr W, Palczewski K (2004) Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem 279(11):10422–10432.  https://doi.org/10.1074/jbc.M312410200 CrossRefPubMedGoogle Scholar
  15. 15.
    Kiser PD, Zhang J, Badiee M, Li Q, Shi W, Sui X, Golczak M, Tochtrop GP, Palczewski K (2015) Catalytic mechanism of a retinoid isomerase essential for vertebrate vision. Nat Chem Biol 11(6):409–415.  https://doi.org/10.1038/nchembio.1799 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Redmond TM, Poliakov E, Yu S, Tsai JY, Lu Z, Gentleman S (2005) Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proc Natl Acad Sci U S A 102(38):13658–13663.  https://doi.org/10.1073/pnas.0504167102 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Moiseyev G, Takahashi Y, Chen Y, Gentleman S, Redmond TM, Crouch RK, Ma JX (2006) RPE65 is an iron(II)-dependent isomerohydrolase in the retinoid visual cycle. J Biol Chem 281(5):2835–2840.  https://doi.org/10.1074/jbc.M508903200 CrossRefPubMedGoogle Scholar
  18. 18.
    Marlhens F, Bareil C, Griffoin JM, Zrenner E, Amalric P, Eliaou C, Liu SY, Harris E, Redmond TM, Arnaud B, Claustres M, Hamel CP (1997) Mutations in RPE65 cause Leber’s congenital amaurosis. Nat Genet 17(2):139–141.  https://doi.org/10.1038/ng1097-139 CrossRefPubMedGoogle Scholar
  19. 19.
    Redmond TM, Yu S, Lee E, Bok D, Hamasaki D, Chen N, Goletz P, Ma JX, Crouch RK, Pfeifer K (1998) Rpe65 is necessary for production of 11-cis-vitamin a in the retinal visual cycle. Nat Genet 20(4):344–351.  https://doi.org/10.1038/3813 CrossRefPubMedGoogle Scholar
  20. 20.
    Samardzija M, von Lintig J, Tanimoto N, Oberhauser V, Thiersch M, Reme CE, Seeliger M, Grimm C, Wenzel A (2008) R91W mutation in Rpe65 leads to milder early-onset retinal dystrophy due to the generation of low levels of 11-cis-retinal. Hum Mol Genet 17(2):281–292.  https://doi.org/10.1093/hmg/ddm304 CrossRefPubMedGoogle Scholar
  21. 21.
    Yamamoto H, Simon A, Eriksson U, Harris E, Berson EL, Dryja TP (1999) Mutations in the gene encoding 11-cis retinol dehydrogenase cause delayed dark adaptation and fundus albipunctatus. Nat Genet 22(2):188–191.  https://doi.org/10.1038/9707 CrossRefPubMedGoogle Scholar
  22. 22.
    Nakamura M, Hotta Y, Tanikawa A, Terasaki H, Miyake Y (2000) A high association with cone dystrophy in fundus albipunctatus caused by mutations of the RDH5 gene. Invest Ophthalmol Vis Sci 41(12):3925–3932PubMedGoogle Scholar
  23. 23.
    Kim TS, Maeda A, Maeda T, Heinlein C, Kedishvili N, Palczewski K, Nelson PS (2005) Delayed dark adaptation in 11-cis-retinol dehydrogenase-deficient mice: a role of RDH11 in visual processes in vivo. J Biol Chem 280(10):8694–8704.  https://doi.org/10.1074/jbc.M413172200 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Sahu B, Sun W, Perusek L, Parmar V, Le YZ, Griswold MD, Palczewski K, Maeda A (2015) Conditional ablation of retinol dehydrogenase 10 in the retinal pigmented epithelium causes delayed dark adaption in mice. J Biol Chem 290(45):27239–27247.  https://doi.org/10.1074/jbc.M115.682096 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Golczak M, Kiser PD, Lodowski DT, Maeda A, Palczewski K (2010) Importance of membrane structural integrity for RPE65 retinoid isomerization activity. J Biol Chem 285(13):9667–9682.  https://doi.org/10.1074/jbc.M109.063941 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Maw MA, Kennedy B, Knight A, Bridges R, Roth KE, Mani EJ, Mukkadan JK, Nancarrow D, Crabb JW, Denton MJ (1997) Mutation of the gene encoding cellular retinaldehyde-binding protein in autosomal recessive retinitis pigmentosa. Nat Genet 17(2):198–200.  https://doi.org/10.1038/ng1097-198 CrossRefPubMedGoogle Scholar
  27. 27.
    Burstedt MS, Sandgren O, Holmgren G, Forsman-Semb K (1999) Bothnia dystrophy caused by mutations in the cellular retinaldehyde-binding protein gene (RLBP1) on chromosome 15q26. Invest Ophthalmol Vis Sci 40(5):995–1000PubMedGoogle Scholar
  28. 28.
    Morimura H, Berson EL, Dryja TP (1999) Recessive mutations in the RLBP1 gene encoding cellular retinaldehyde-binding protein in a form of retinitis punctata albescens. Invest Ophthalmol Vis Sci 40(5):1000–1004PubMedGoogle Scholar
  29. 29.
    Saari JC, Nawrot M, Kennedy BN, Garwin GG, Hurley JB, Huang J, Possin DE, Crabb JW (2001) Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron 29(3):739–748CrossRefPubMedGoogle Scholar
  30. 30.
    Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A, Chidambaram A, Gerrard B, Baird L, Stauffer D, Peiffer A, Rattner A, Smallwood P, Li Y, Anderson KL, Lewis RA, Nathans J, Leppert M, Dean M, Lupski JR (1997) A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet 15(3):236–246.  https://doi.org/10.1038/ng0397-236 CrossRefPubMedGoogle Scholar
  31. 31.
    Allikmets R, Shroyer NF, Singh N, Seddon JM, Lewis RA, Bernstein PS, Peiffer A, Zabriskie NA, Li Y, Hutchinson A, Dean M, Lupski JR, Leppert M (1997) Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science 277(5333):1805–1807CrossRefPubMedGoogle Scholar
  32. 32.
    Fritsche LG, Fleckenstein M, Fiebig BS, Schmitz-Valckenberg S, Bindewald-Wittich A, Keilhauer CN, Renner AB, Mackensen F, Mossner A, Pauleikhoff D, Adrion C, Mansmann U, Scholl HP, Holz FG, Weber BH (2012) A subgroup of age-related macular degeneration is associated with mono-allelic sequence variants in the ABCA4 gene. Invest Ophthalmol Vis Sci 53(4):2112–2118.  https://doi.org/10.1167/iovs.11-8785 CrossRefPubMedGoogle Scholar
  33. 33.
    Quazi F, Lenevich S, Molday RS (2012) ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer. Nat Commun 3:925.  https://doi.org/10.1038/ncomms1927 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Weng J, Mata NL, Azarian SM, Tzekov RT, Birch DG, Travis GH (1999) Insights into the function of rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell 98(1):13–23.  https://doi.org/10.1016/S0092-8674(00)80602-9 CrossRefPubMedGoogle Scholar
  35. 35.
    Mata NL, Weng J, Travis GH (2000) Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration. Proc Natl Acad Sci U S A 97(13):7154–7159.  https://doi.org/10.1073/pnas.130110497 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Maeda A, Maeda T, Imanishi Y, Kuksa V, Alekseev A, Bronson JD, Zhang H, Zhu L, Sun W, Saperstein DA, Rieke F, Baehr W, Palczewski K (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J Biol Chem 280(19):18822–18832.  https://doi.org/10.1074/jbc.M501757200 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Maeda A, Maeda T, Sun W, Zhang H, Baehr W, Palczewski K (2007) Redundant and unique roles of retinol dehydrogenases in the mouse retina. Proc Natl Acad Sci U S A 104(49):19565–19570.  https://doi.org/10.1073/pnas.0707477104 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Janecke AR, Thompson DA, Utermann G, Becker C, Hubner CA, Schmid E, McHenry CL, Nair AR, Ruschendorf F, Heckenlively J, Wissinger B, Nurnberg P, Gal A (2004) Mutations in RDH12 encoding a photoreceptor cell retinol dehydrogenase cause childhood-onset severe retinal dystrophy. Nat Genet 36(8):850–854.  https://doi.org/10.1038/ng1394 CrossRefPubMedGoogle Scholar
  39. 39.
    Maeda A, Maeda T, Golczak M, Palczewski K (2008) Retinopathy in mice induced by disrupted all-trans-retinal clearance. J Biol Chem 283(39):26684–26693.  https://doi.org/10.1074/jbc.M804505200 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Maeda T, Maeda A, Matosky M, Okano K, Roos S, Tang J, Palczewski K (2009) Evaluation of potential therapies for a mouse model of human age-related macular degeneration caused by delayed all-trans-retinal clearance. Invest Ophthalmol Vis Sci 50(10):4917–4925.  https://doi.org/10.1167/iovs.09-3581 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Chen Y, Okano K, Maeda T, Chauhan V, Golczak M, Maeda A, Palczewski K (2012) Mechanism of all-trans-retinal toxicity with implications for stargardt disease and age-related macular degeneration. J Biol Chem 287(7):5059–5069.  https://doi.org/10.1074/jbc.M111.315432 CrossRefPubMedGoogle Scholar
  42. 42.
    Chen Y, Palczewska G, Mustafi D, Golczak M, Dong Z, Sawada O, Maeda T, Maeda A, Palczewski K (2013) Systems pharmacology identifies drug targets for Stargardt disease-associated retinal degeneration. J Clin Invest 123(12):5119–5134.  https://doi.org/10.1172/JCI69076 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Maeda A, Golczak M, Chen Y, Okano K, Kohno H, Shiose S, Ishikawa K, Harte W, Palczewska G, Maeda T, Palczewski K (2011) Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat Chem Biol 8(2):170–178.  https://doi.org/10.1038/nchembio.759 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Liou GI, Fei Y, Peachey NS, Matragoon S, Wei S, Blaner WS, Wang Y, Liu C, Gottesman ME, Ripps H (1998) Early onset photoreceptor abnormalities induced by targeted disruption of the interphotoreceptor retinoid-binding protein gene. J Neurosci 18(12):4511–4520PubMedGoogle Scholar
  45. 45.
    Parker RO, Fan J, Nickerson JM, Liou GI, Crouch RK (2009) Normal cone function requires the interphotoreceptor retinoid binding protein. J Neurosci 29(14):4616–4621.  https://doi.org/10.1523/JNEUROSCI.0063-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Chen P, Hao W, Rife L, Wang XP, Shen D, Chen J, Ogden T, Van Boemel GB, Wu L, Yang M, Fong HK (2001) A photic visual cycle of rhodopsin regeneration is dependent on Rgr. Nat Genet 28(3):256–260.  https://doi.org/10.1038/90089 CrossRefPubMedGoogle Scholar
  47. 47.
    Morimura H, Saindelle-Ribeaudeau F, Berson EL, Dryja TP (1999) Mutations in RGR, encoding a light-sensitive opsin homologue, in patients with retinitis pigmentosa. Nat Genet 23(4):393–394.  https://doi.org/10.1038/70496 CrossRefPubMedGoogle Scholar
  48. 48.
    Tanimoto N, Sothilingam V, Seeliger MW (2013) Functional phenotyping of mouse models with ERG. Methods Mol Biol 935:69–78.  https://doi.org/10.1007/978-1-62703-080-9_4 CrossRefPubMedGoogle Scholar
  49. 49.
    Kolesnikov AV, Kefalov VJ (2012) Transretinal ERG recordings from mouse retina: rod and cone photoresponses. J Vis Exp (61).  https://doi.org/10.3791/3424
  50. 50.
    Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicolo M, Kosaras B, Wong G, Gannon KS, Margolskee RF, Sidman RL, Pugh EN Jr, Makino CL, Lem J (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc Natl Acad Sci U S A 97(25):13913–13918.  https://doi.org/10.1073/pnas.250478897 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Chang B, Hurd R, Wang J, Nishina P (2013) Survey of common eye diseases in laboratory mouse strains. Invest Ophthalmol Vis Sci 54(7):4974–4981.  https://doi.org/10.1167/iovs.13-12289 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Naeem MA, Chavali VR, Ali S, Iqbal M, Riazuddin S, Khan SN, Husnain T, Sieving PA, Ayyagari R, Riazuddin S, Hejtmancik JF, Riazuddin SA (2012) GNAT1 associated with autosomal recessive congenital stationary night blindness. Invest Ophthalmol Vis Sci 53(3):1353–1361.  https://doi.org/10.1167/iovs.11-8026 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kohl S, Baumann B, Rosenberg T, Kellner U, Lorenz B, Vadala M, Jacobson SG, Wissinger B (2002) Mutations in the cone photoreceptor G-protein alpha-subunit gene GNAT2 in patients with achromatopsia. Am J Hum Genet 71(2):422–425.  https://doi.org/10.1086/341835 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Baehr W, Karan S, Maeda T, Luo DG, Li S, Bronson JD, Watt CB, Yau KW, Frederick JM, Palczewski K (2007) The function of guanylate cyclase 1 and guanylate cyclase 2 in rod and cone photoreceptors. J Biol Chem 282(12):8837–8847.  https://doi.org/10.1074/jbc.M610369200 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Perrault I, Rozet JM, Calvas P, Gerber S, Camuzat A, Dollfus H, Chatelin S, Souied E, Ghazi I, Leowski C, Bonnemaison M, Le Paslier D, Frezal J, Dufier JL, Pittler S, Munnich A, Kaplan J (1996) Retinal-specific guanylate cyclase gene mutations in Leber’s congenital amaurosis. Nat Genet 14(4):461–464.  https://doi.org/10.1038/ng1296-461 CrossRefPubMedGoogle Scholar
  56. 56.
    Miki N, Baraban JM, Keirns JJ, Boyce JJ, Bitensky MW (1975) Purification and properties of the light-activated cyclic nucleotide phosphodiesterase of rod outer segments. J Biol Chem 250(16):6320–6327PubMedGoogle Scholar
  57. 57.
    Brown BM, Ramirez T, Rife L, Craft CM (2010) Visual Arrestin 1 contributes to cone photoreceptor survival and light adaptation. Invest Ophthalmol Vis Sci 51(5):2372–2380.  https://doi.org/10.1167/iovs.09-4895 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Lyubarsky AL, Chen C, Simon MI, Pugh EN Jr (2000) Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses. J Neurosci 20(6):2209–2217PubMedGoogle Scholar
  59. 59.
    Nikonov SS, Daniele LL, Zhu X, Craft CM, Swaroop A, Pugh EN Jr (2005) Photoreceptors of Nrl −/− mice coexpress functional S- and M-cone opsins having distinct inactivation mechanisms. J Gen Physiol 125(3):287–304.  https://doi.org/10.1085/jgp.200409208 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Pak JS, Lee EJ, Craft CM (2015) The retinal phenotype of Grk1−/− is compromised by a Crb1 rd8 mutation. Mol Vis 21:1281–1294PubMedPubMedCentralGoogle Scholar
  61. 61.
    Dizhoor AM, Ray S, Kumar S, Niemi G, Spencer M, Brolley D, Walsh KA, Philipov PP, Hurley JB, Stryer L (1991) Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science 251(4996):915–918CrossRefPubMedGoogle Scholar
  62. 62.
    Kawamura S, Hisatomi O, Kayada S, Tokunaga F, Kuo CH (1993) Recoverin has S-modulin activity in frog rods. J Biol Chem 268(20):14579–14582PubMedGoogle Scholar
  63. 63.
    Chen CK, Inglese J, Lefkowitz RJ, Hurley JB (1995) Ca(2+)-dependent interaction of recoverin with rhodopsin kinase. J Biol Chem 270(30):18060–18066CrossRefPubMedGoogle Scholar
  64. 64.
    Makino CL, Dodd RL, Chen J, Burns ME, Roca A, Simon MI, Baylor DA (2004) Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J Gen Physiol 123(6):729–741.  https://doi.org/10.1085/jgp.200308994 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Nemet I, Ropelewski P, Imanishi Y (2015) Rhodopsin trafficking and mistrafficking: signals, molecular components, and mechanisms. Prog Mol Biol Transl Sci 132:39–71.  https://doi.org/10.1016/bs.pmbts.2015.02.007 CrossRefPubMedGoogle Scholar
  66. 66.
    Sung CH, Makino C, Baylor D, Nathans J (1994) 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 14(10):5818–5833PubMedGoogle Scholar
  67. 67.
    Jiang L, Tam BM, Ying G, Wu S, Hauswirth WW, Frederick JM, Moritz OL, Baehr W (2015) Kinesin family 17 (osmotic avoidance abnormal-3) is dispensable for photoreceptor morphology and function. FASEB J 29(12):4866–4880.  https://doi.org/10.1096/fj.15-275677 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Liu X, Udovichenko IP, Brown SD, Steel KP, Williams DS (1999) Myosin VIIa participates in opsin transport through the photoreceptor cilium. J Neurosci 19(15):6267–6274PubMedGoogle Scholar
  69. 69.
    Chiang WC, Kroeger H, Sakami S, Messah C, Yasumura D, Matthes MT, Coppinger JA, Palczewski K, LaVail MM, Lin JH (2015) Robust endoplasmic reticulum-associated degradation of rhodopsin precedes retinal degeneration. Mol Neurobiol 52(1):679–695.  https://doi.org/10.1007/s12035-014-8881-8 CrossRefPubMedGoogle Scholar
  70. 70.
    Sakami S, Kolesnikov AV, Kefalov VJ, Palczewski K (2014) P23H opsin knock-in mice reveal a novel step in retinal rod disc morphogenesis. Hum Mol Genet 23(7):1723–1741.  https://doi.org/10.1093/hmg/ddt561 CrossRefPubMedGoogle Scholar
  71. 71.
    Jiang H, Xiong S, Xia X (2014) Retinitis pigmentosaassociated rhodopsin mutant T17M induces endoplasmic reticulum (ER) stress and sensitizes cells to ER stress-induced cell death. Mol Med Rep 9(5):1737–1742.  https://doi.org/10.3892/mmr.2014.1987 CrossRefPubMedGoogle Scholar
  72. 72.
    Gibbs D, Kitamoto J, Williams DS (2003) Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the usher syndrome 1B protein. Proc Natl Acad Sci U S A 100(11):6481–6486.  https://doi.org/10.1073/pnas.1130432100 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Liu X, Ondek B, Williams DS (1998) Mutant myosin VIIa causes defective melanosome distribution in the RPE of shaker-1 mice. Nat Genet 19(2):117–118.  https://doi.org/10.1038/470 CrossRefPubMedGoogle Scholar
  74. 74.
    Rachel RA, Yamamoto EA, Dewanjee MK, May-Simera HL, Sergeev YV, Hackett AN, Pohida K, Munasinghe J, Gotoh N, Wickstead B, Fariss RN, Dong L, Li T, Swaroop A (2015) CEP290 alleles in mice disrupt tissue-specific cilia biogenesis and recapitulate features of syndromic ciliopathies. Hum Mol Genet 24(13):3775–3791.  https://doi.org/10.1093/hmg/ddv123 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Drivas TG, Holzbaur EL, Bennett J (2013) Disruption of CEP290 microtubule/membrane-binding domains causes retinal degeneration. J Clin Invest 123(10):4525–4539.  https://doi.org/10.1172/JCI69448 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Chen Y, Sawada O, Kohno H, Le YZ, Subauste C, Maeda T, Maeda A (2013) Autophagy protects the retina from light-induced degeneration. J Biol Chem 288(11):7506–7518.  https://doi.org/10.1074/jbc.M112.439935 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Kim JY, Zhao H, Martinez J, Doggett TA, Kolesnikov AV, Tang PH, Ablonczy Z, Chan CC, Zhou Z, Green DR, Ferguson TA (2013) Noncanonical autophagy promotes the visual cycle. Cell 154(2):365–376.  https://doi.org/10.1016/j.cell.2013.06.012 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Zhou Z, Doggett TA, Sene A, Apte RS, Ferguson TA (2015) Autophagy supports survival and phototransduction protein levels in rod photoreceptors. Cell Death Differ 22(3):488–498.  https://doi.org/10.1038/cdd.2014.229 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Rohrer B, Lohr HR, Humphries P, Redmond TM, Seeliger MW, Crouch RK (2005) Cone opsin mislocalization in Rpe65−/− mice: a defect that can be corrected by 11-cis retinal. Invest Ophthalmol Vis Sci 46(10):3876–3882.  https://doi.org/10.1167/iovs.05-0533 CrossRefPubMedGoogle Scholar
  80. 80.
    Batten ML, Imanishi Y, DC T, Doan T, Zhu L, Pang J, Glushakova L, Moise AR, Baehr W, Van Gelder RN, Hauswirth WW, Rieke F, Palczewski K (2005) Pharmacological and rAAV gene therapy rescue of visual functions in a blind mouse model of Leber congenital amaurosis. PLoS Med 2(11):e333.  https://doi.org/10.1371/journal.pmed.0020333 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Sakamoto K, McCluskey M, Wensel TG, Naggert JK, Nishina PM (2009) New mouse models for recessive retinitis pigmentosa caused by mutations in the Pde6a gene. Hum Mol Genet 18(1):178–192.  https://doi.org/10.1093/hmg/ddn327 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Akiko Maeda
    • 1
  • Tadao Maeda
    • 2
  1. 1.Department of Ophthalmology and Visual SciencesCase Western Reserve UniversityClevelandUSA
  2. 2.Research Division, Kobe Research InstituteHEALIOS K.K.KobeJapan

Personalised recommendations