Skip to main content

Preclinical Models of Retinitis Pigmentosa

  • Protocol
  • First Online:
Retinitis Pigmentosa

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2560))

  • 1157 Accesses

Abstract

Retinitis pigmentosa (RP) is the name for a group of phenotypically-related heritable retinal degenerative disorders. Many genes have been implicated as causing variants of RP, and while the clinical phenotypes are remarkably similar, they may differ in age of onset, progression, and severity. Common inheritance patterns for specific genes connected with the development of the disorder include autosomal dominant, autosomal recessive, and X-linked. Modeling the disease in animals and other preclinical systems offers a cost-conscious, ethical, and time-efficient method for studying the disease subtypes. The history of RP models is briefly examined, and both naturally occurring and transgenic preclinical models of RP in many different organisms are discussed. Syndromic forms of RP and models thereof are reviewed as well.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368:1795–1809

    Article  CAS  Google Scholar 

  2. Zhang Q (2016) Retinitis pigmentosa: progress and perspective. Asia Pac J Ophthalmol (Phila) 5:265–271

    Article  CAS  Google Scholar 

  3. Usher syndrome. https://ghr.nlm.nih.gov/condition/usher-syndrome

  4. Bardet-Biedl syndrome. https://ghr.nlm.nih.gov/condition/bardet-biedl-syndrome

  5. Petrs-Silva H, Linden R (2013) Advances in gene therapy technologies to treat retinitis pigmentosa. Clin Ophthalmol 8:127–136

    Article  Google Scholar 

  6. Berger W, Kloeckener-Gruissem B, Neidhardt J (2010) The molecular basis of human retinal and vitreoretinal diseases. Prog Retin Eye Res 29:335–375

    Article  CAS  Google Scholar 

  7. Fletcher EL, Jobling AI, Vessey KA et al (2011) Animal models of retinal disease. In: Progress in molecular biology and translational science. Elsevier, pp 211–286

    Google Scholar 

  8. Hafezi F, Grimm C, Simmen BC et al (2000) Molecular ophthalmology: an update on animal models for retinal degenerations and dystrophies. Br J Ophthalmol 84:922–927

    Article  CAS  Google Scholar 

  9. Artero Castro A, Lukovic D, Jendelova P et al (2018) Concise review: human induced pluripotent stem cell models of retinitis pigmentosa. Stem Cells 36:474–481

    Article  Google Scholar 

  10. Keeler CE (1924) The inheritance of a retinal abnormality in white mice. Proc Natl Acad Sci 10:329–333

    Article  CAS  Google Scholar 

  11. Baehr W, Frederick JM (2009) Naturally occurring animal models with outer retina phenotypes. Vis Res 49:2636–2652

    Article  Google Scholar 

  12. Bhattacharya SS, Wright AF, Clayton JF et al (1984) Close genetic linkage between X-linked retinitis pigmentosa and a restriction fragment length polymorphism identified by recombinant DNA probe L1.28. Nature 309:253

    Article  CAS  Google Scholar 

  13. Farrar GJ, McWilliam P, Sharp EM et al (1989) Autosomal dominant retinitis pigmentosa: exclusion of a gene from extensive regions of chromosomes 6, 13, 20, and 21. Genomics 5:612–618

    Article  CAS  Google Scholar 

  14. Dryja TP, McGee TL, Reichel E et al (1990) A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343:364–366

    Article  CAS  Google Scholar 

  15. RetNet: Summaries. https://sph.uth.edu/retnet/sum-dis.htm

  16. Wagner TE, Hoppe PC, Jollick JD et al (1981) Microinjection of a rabbit beta-globin gene into zygotes and its subsequent expression in adult mice and their offspring. PNAS 78:6376–6380

    Article  CAS  Google Scholar 

  17. Flannery JG (1999) Transgenic animal models for the study of inherited retinal dystrophies. ILAR J 40:51–58

    Article  Google Scholar 

  18. Zack DJ, Bennett J, Wang Y et al (1991) Unusual topography of bovine rhodopsin promoter-lacZ fusion gene expression in transgenic mouse retinas. Neuron 6:187–199

    Article  CAS  Google Scholar 

  19. Lem J, Applebury ML, Falk JD et al (1991) Tissue-specific and developmental regulation of rod opsin chimeric genes in transgenic mice. Neuron 6:201–210

    Article  CAS  Google Scholar 

  20. Naash MI, Hollyfield JG, Ubaidi MR et al (1993) Simulation of human autosomal dominant retinitis pigmentosa in transgenic mice expressing a mutated murine opsin gene. PNAS 90:5499–5503

    Article  CAS  Google Scholar 

  21. Chader GJ (2002) Animal models in research on retinal degenerations: past progress and future hope. Vis Res 42:393–399

    Article  Google Scholar 

  22. Daiger SP, Bowne SJ, Sullivan LS (2015) Genes and mutations causing autosomal dominant retinitis pigmentosa. Cold Spring Harb Perspect Med 5:a017129

    Article  Google Scholar 

  23. Saliba RS, Munro PMG, Luthert PJ et al (2002) The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation. J Cell Sci 115:2907–2918

    Article  CAS  Google Scholar 

  24. Rossmiller B, Mao H, Lewin AS (2012) Gene therapy in animal models of autosomal dominant retinitis pigmentosa. Mol Vis 18:2479–2496

    CAS  Google Scholar 

  25. Kijas JW, Cideciyan AV, Aleman TS et al (2002) Naturally occurring rhodopsin mutation in the dog causes retinal dysfunction and degeneration mimicking human dominant retinitis pigmentosa. PNAS 99:6328–6333

    Article  CAS  Google Scholar 

  26. Barnett KC, Curtis R (1985) Autosomal dominant progressive retinal atrophy in Abyssinian cats. J Hered 76:168–170

    Article  CAS  Google Scholar 

  27. Chong NHV, Alexander RA, Barnett KC et al (1999) An immunohistochemical study of an autosomal dominant feline rod/cone dysplasia (Rdy Cats). Exp Eye Res 68:51–57

    Article  CAS  Google Scholar 

  28. Narfström K, Holland Deckman K, Menotti-Raymond M (2011) The domestic cat as a large animal model for characterization of disease and therapeutic intervention in hereditary retinal blindness. J Ophthalmol 2011:906943

    Google Scholar 

  29. Hennig AK, Peng G-H, Chen S (2008) Regulation of photoreceptor gene expression by Crx-associated transcription factor network. Brain Res 1192:114–133

    Article  CAS  Google Scholar 

  30. van Nie R, Iványi D, Démant P (1978) A new H-2-linked mutation, rds, causing retinal degeneration in the mouse. Tissue Antigens 12:106–108

    Article  Google Scholar 

  31. Travis GH, Brennan MB, Danielson PE et al (1989) Identification of a photoreceptor-specific mRNA encoded by the gene responsible for retinal degeneration slow (rds). Nature 338:70–73

    Article  CAS  Google Scholar 

  32. Sanyal S, Jansen HG (1981) Absence of receptor outer segments in the retina of rds mutant mice. Neurosci Lett 21:23–26

    Article  CAS  Google Scholar 

  33. Roderick TH, Chang B, Hawes NL et al (1997) A new dominant retinal degeneration (Rd4) associated with a chromosomal inversion in the mouse. Genomics 42:393–396

    Article  CAS  Google Scholar 

  34. Kitamura E, Danciger M, Yamashita C et al (2006) Disruption of the gene encoding the β1-subunit of transducin in the Rd4/+ mouse. Invest Ophthalmol Vis Sci 47:1293–1301

    Article  Google Scholar 

  35. Kedzierski W, Lloyd M, Birch DG et al (1997) Generation and analysis of transgenic mice expressing P216L-substituted rds/peripherin in rod photoreceptors. Invest Ophthalmol Vis Sci 38:498–509

    CAS  Google Scholar 

  36. Stricker HM, Ding X-Q, Quiambao A et al (2005) The Cys214-->Ser mutation in peripherin/rds causes a loss-of-function phenotype in transgenic mice. Biochem J 388:605–613

    Article  CAS  Google Scholar 

  37. Olsson JE, Gordon JW, Pawlyk BS et al (1992) Transgenic mice with a rhodopsin mutation (Pro23His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron 9:815–830

    Article  CAS  Google Scholar 

  38. Liu X, Wu T-H, Stowe S et al (1997) Defective phototransductive disk membrane morphogenesis in transgenic mice expressing opsin with a mutated N-terminal domain. J Cell Sci 110:2589–2597

    Article  CAS  Google Scholar 

  39. Machida S, Kondo M, Jamison JA et al (2000) P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci 41:3200–3209

    CAS  Google Scholar 

  40. Acosta ML, Shin Y-S, Ready S et al (2010) Retinal metabolic state of the proline-23-histidine rat model of retinitis pigmentosa. Am J Physiol Cell Physiol 298:C764–C774

    Article  CAS  Google Scholar 

  41. Sung CH, Makino C, Baylor D et al (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 14:5818–5833

    Article  CAS  Google Scholar 

  42. Li T, Snyder WK, Olsson JE et al (1996) Transgenic mice carrying the dominant rhodopsin mutation P347S: evidence for defective vectorial transport of rhodopsin to the outer segments. Proc Natl Acad Sci U S A 93:14176–14181

    Article  CAS  Google Scholar 

  43. Liu C, Li Y, Peng M et al (1999) Activation of caspase-3 in the retina of transgenic rats with the rhodopsin mutation s334ter during photoreceptor degeneration. J Neurosci 19:4778–4785

    Article  CAS  Google Scholar 

  44. Gryczan CW, Kuszak JR, Novak L et al (1995) A transgenic mouse model for autosomal dominant retinitis pigmentosa caused by a three base pair deletion in codon 255/256 of the opsin gene. Invest Ophthalmol Vis Sci 36:S423

    Google Scholar 

  45. Penn JS, Li S, Naash MI (2000) Ambient hypoxia reverses retinal vascular attenuation in a transgenic mouse model of autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci 41:4007–4013

    CAS  Google Scholar 

  46. Chen J, Shi G, Concepcion FA et al (2006) Stable rhodopsin/arrestin complex leads to retinal degeneration in a transgenic mouse model of autosomal dominant retinitis pigmentosa. J Neurosci 26:11929–11937

    Article  CAS  Google Scholar 

  47. Sancho-Pelluz J, Tosi J, Hsu C-W et al (2012) Mice with a D190N mutation in the gene encoding rhodopsin: a model for human autosomal-dominant retinitis pigmentosa. Mol Med 18:549–555

    Article  CAS  Google Scholar 

  48. Weber BHF, Lin B, White K et al (2002) A mouse model for Sorsby fundus dystrophy. Invest Ophthalmol Vis Sci 43:2732–2740

    Google Scholar 

  49. Jones SE, Jomary C, Neal MJ (1994) Expression of TIMP3 mRNA is elevated in retinas affected by simplex retinitis pigmentosa. FEBS Lett 352:171–174

    Article  CAS  Google Scholar 

  50. Sorsby A, Mason MEJ, Gardener N (1949) A fundus dystrophy with unusual features (late onset and dominant inheritance of a central retinal lesion showing oedema, haemorrhage and exudates developing into generalised choroidal atrophy with massive pigment proliferation). Br J Ophthalmol 33:67–97

    Article  CAS  Google Scholar 

  51. Marmorstein AD, Marmorstein LY (2007) The challenge of modeling macular degeneration in mice. Trends Genet 23:225–231

    Article  CAS  Google Scholar 

  52. Leco KJ, Waterhouse P, Sanchez OH et al (2001) Spontaneous air space enlargement in the lungs of mice lacking tissue inhibitor of metalloproteinases-3 (TIMP-3). J Clin Invest 108:817–829

    Article  CAS  Google Scholar 

  53. Nakao T, Tsujikawa M, Notomi S et al (2012) The role of mislocalized phototransduction in photoreceptor cell death of retinitis pigmentosa. PLoS One 7:e32472

    Article  CAS  Google Scholar 

  54. Link BA, Collery RF (2015) Zebrafish models of retinal disease. Annu Rev Vis Sci 1:125–153

    Article  Google Scholar 

  55. Hendrickson A, Hicks D (2002) Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina. Exp Eye Res 74:435–444

    Article  CAS  Google Scholar 

  56. Petters RM, Alexander CA, Wells KD et al (1997) Genetically engineered large animal model for studying cone photoreceptor survival and degeneration in retinitis pigmentosa. Nat Biotechnol 15:965–970

    Article  CAS  Google Scholar 

  57. Li ZY, Wong F, Chang JH et al (1998) Rhodopsin transgenic pigs as a model for human retinitis pigmentosa. Invest Ophthalmol Vis Sci 39:808–819

    CAS  Google Scholar 

  58. Ross JW, de Castro JPF, Zhao J et al (2012) Generation of an inbred miniature pig model of retinitis pigmentosa. Invest Ophthalmol Vis Sci 53:501–507

    Article  CAS  Google Scholar 

  59. Ferrari S, Di Iorio E, Barbaro V et al (2011) Retinitis pigmentosa: genes and disease mechanisms. Curr Genomics 12:238–249

    Article  CAS  Google Scholar 

  60. Burt DW, Bruley C, Dunn IC et al (1999) The dynamics of chromosome evolution in birds and mammals. Nature 402:411–413

    Article  CAS  Google Scholar 

  61. Ulshafer RJ, Allen CB (1985) Ultrastructural changes in the retinal pigment epithelium of congenitally blind chickens. Curr Eye Res 4:1009–1021

    Article  CAS  Google Scholar 

  62. Semple-Rowland SL, Lee NR, Hooser JPV et al (1998) A null mutation in the photoreceptor guanylate cyclase gene causes the retinal degeneration chicken phenotype. PNAS 95:1271–1276

    Article  CAS  Google Scholar 

  63. Ulshafer RJ, Allen C, Dawson WW et al (1984) Hereditary retinal degeneration in the Rhode Island Red chicken. I. Histology and ERG. Exp Eye Res 39:125–135

    Article  CAS  Google Scholar 

  64. Wiik AC, Ropstad EO, Ekesten B et al (2015) Progressive retinal atrophy in Shetland sheepdog is associated with a mutation in the CNGA1 gene. Anim Genet 46:515–521

    Article  CAS  Google Scholar 

  65. Winkler PA, Ekenstedt KJ, Occelli LM et al (2013) A large animal model for CNGB1 autosomal recessive retinitis pigmentosa. PLoS One 8:e72229

    Article  CAS  Google Scholar 

  66. Cooper AE, Ahonen S, Rowlan JS et al (2014) A novel form of progressive retinal atrophy in Swedish Vallhund dogs. PLoS One 9:e106610

    Article  Google Scholar 

  67. Everson R, Pettitt L, Forman OP et al (2017) An intronic LINE-1 insertion in MERTK is strongly associated with retinopathy in Swedish Vallhund dogs. PLoS One 12:e0183021

    Article  Google Scholar 

  68. Zangerl B, Goldstein O, Philp AR et al (2006) Identical mutation in a novel retinal gene causes progressive rod-cone degeneration in dogs and retinitis pigmentosa in humans. Genomics 88:551–563

    Article  CAS  Google Scholar 

  69. Kukekova AV, Goldstein O, Johnson JL et al (2009) Canine RD3 mutation establishes rod-cone dysplasia type 2 (rcd2) as ortholog of human and murine rd3. Mamm Genome 20:109–123

    Article  CAS  Google Scholar 

  70. Petersen–Jones SM, Entz DD, Sargan DR (1999) cGMP phosphodiesterase-α mutation causes progressive retinal atrophy in the Cardigan Welsh Corgi dog. Invest Ophthalmol Vis Sci 40:1637–1644

    Google Scholar 

  71. Dekomien G, Runte M, Gödde R et al (2000) Generalized progressive retinal atrophy of Sloughi dogs is due to an 8-bp insertion in exon 21 of the PDE6B gene. Cytogenet Cell Genet 90:261–267

    Article  CAS  Google Scholar 

  72. Goldstein O, Mezey JG, Schweitzer PA et al (2013) IQCB1 and PDE6B mutations cause similar early onset retinal degenerations in two closely related terrier dog breeds. Invest Ophthalmol Vis Sci 54:7005–7019

    Article  CAS  Google Scholar 

  73. Downs LM, Bell JS, Freeman J et al (2013) Late-onset progressive retinal atrophy in the Gordon and Irish Setter breeds is associated with a frameshift mutation in C2orf71. Anim Genet 44:169–177

    Article  CAS  Google Scholar 

  74. Tuntivanich N, Pittler SJ, Fischer AJ et al (2009) Characterization of a canine model of autosomal recessive retinitis pigmentosa due to a PDE6A mutation. Invest Ophthalmol Vis Sci 50:801–813

    Article  Google Scholar 

  75. Suber ML, Pittler SJ, Qin N et al (1993) Irish setter dogs affected with rod/cone dysplasia contain a nonsense mutation in the rod cGMP phosphodiesterase beta-subunit gene. PNAS 90:3968–3972

    Article  CAS  Google Scholar 

  76. Narfström K, Nilsson SE (1985) Hereditary retinal degeneration in the Abyssinian cat: correlation of ophthalmoscopic and electroretinographic findings. Doc Ophthalmol 60:183–187

    Article  Google Scholar 

  77. Jacobson SG, Kemp CM, Narfström K et al (1989) Rhodopsin levels and rod-mediated function in Abyssinian cats with hereditary retinal degeneration. Exp Eye Res 49:843–852

    Article  CAS  Google Scholar 

  78. Narfström K, Nilsson SE (1986) Progressive retinal atrophy in the Abyssinian cat. Electron microscopy. Invest Ophthalmol Vis Sci 27:1569–1576

    Google Scholar 

  79. Chang B, Khanna H, Hawes N et al (2006) In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 15:1847–1857

    Article  CAS  Google Scholar 

  80. Han J, Dinculescu A, Dai X et al (2013) Review: the history and role of naturally occurring mouse models with Pde6b mutations. Mol Vis 19:2579–2589

    CAS  Google Scholar 

  81. Farber DB, Flannery JG, Bowes-Rickman C (1994) The rd mouse story: seventy years of research on an animal model of inherited retinal degeneration. Prog Retin Eye Res 13:31–64

    Article  CAS  Google Scholar 

  82. Acosta ML, Fletcher EL, Azizoglu S et al (2005) Early markers of retinal degeneration in rd/rd mice. Mol Vis 11:717–728

    CAS  Google Scholar 

  83. Blanks JC, Adinolfi AM, Lolley RN (1974) Photoreceptor degeneration and synaptogenesis in retinal-degenerative (rd) mice. J Comp Neurol 156:95–106

    Article  CAS  Google Scholar 

  84. Chang B, Hawes NL, Hurd RE et al (2002) Retinal degeneration mutants in the mouse. Vis Res 42:517–525

    Article  CAS  Google Scholar 

  85. Chang B, Hawes NL, Pardue MT et al (2007) Two mouse retinal degenerations caused by missense mutations in the beta-subunit of rod cGMP phosphodiesterase gene. Vis Res 47:624–633

    Article  CAS  Google Scholar 

  86. Chang B, Heckenlively JR, Hawes NL et al (1993) New mouse primary retinal degeneration (rd-3). Genomics 16:45–49

    Article  CAS  Google Scholar 

  87. Heckenlively JR, Chang B, Peng C et al (1993) Variable expressivity of rd-3 retinal degeneration dependent on background strain. In: Hollyfield JG, Anderson RE, LaVail MM (eds) Retinal degeneration: clinical and laboratory applications. Springer US, Boston, pp 273–280

    Chapter  Google Scholar 

  88. Friedman JS, Chang B, Kannabiran C et al (2006) Premature truncation of a novel protein, RD3, exhibiting subnuclear localization is associated with retinal degeneration. Am J Hum Genet 79:1059–1070

    Article  CAS  Google Scholar 

  89. Kameya S, Hawes NL, Chang B et al (2002) Mfrp, a gene encoding a frizzled related protein, is mutated in the mouse retinal degeneration 6. Hum Mol Genet 11:1879–1886

    Article  CAS  Google Scholar 

  90. den Hollander AI, ten Brink JB, de Kok YJ et al (1999) Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet 23:217–221

    Article  Google Scholar 

  91. Mehalow AK, Kameya S, Smith RS et al (2003) CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet 12:2179–2189

    Article  CAS  Google Scholar 

  92. Pang J-J, Chang B, Hawes NL et al (2005) Retinal degeneration 12 (rd12): a new, spontaneously arising mouse model for human Leber congenital amaurosis (LCA). Mol Vis 11:152–162

    CAS  Google Scholar 

  93. D’Cruz PM, Yasumura D, Weir J et al (2000) Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 9:645–651

    Article  Google Scholar 

  94. Dowling JE, Sidman RL (1962) Inherited retinal dystrophy in the rat. J Cell Biol 14:73–109

    Article  CAS  Google Scholar 

  95. Duncan JL, LaVail MM, Yasumura D et al (2003) An RCS-like retinal dystrophy phenotype in mer knockout mice. Invest Ophthalmol Vis Sci 44:826–838

    Article  Google Scholar 

  96. Mullen RJ, Eicher EM, Sidman RL (1976) Purkinje cell degeneration, a new neurological mutation in the mouse. PNAS 73:208–212

    Article  CAS  Google Scholar 

  97. Fernandez-Gonzalez A, La Spada AR, Treadaway J et al (2002) Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295:1904–1906

    Article  CAS  Google Scholar 

  98. Redmond TM, Yu S, Lee E et al (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat Genet 20:344–351

    Article  CAS  Google Scholar 

  99. Van Hooser JP, Aleman TS, He YG et al (2000) Rapid restoration of visual pigment and function with oral retinoid in a mouse model of childhood blindness. Proc Natl Acad Sci U S A 97:8623–8628

    Article  Google Scholar 

  100. Lai C-M, Yu MJ, Brankov M et al (2004) Recombinant adeno-associated virus type 2-mediated gene delivery into the Rpe65−/− knockout mouse eye results in limited rescue. Genet Vaccines Ther 2:3

    Article  Google Scholar 

  101. Rohrer B, Lohr HR, Humphries P et al (2005) Cone opsin mislocalization in Rpe65−/− mice: a defect that can be corrected by 11-cis retinal. Invest Ophthalmol Vis Sci 46:3876–3882

    Article  Google Scholar 

  102. Znoiko SL, Rohrer B, Lu K et al (2005) Downregulation of cone-specific gene expression and degeneration of cone photoreceptors in the Rpe65−/− mouse at early ages. Invest Ophthalmol Vis Sci 46:1473–1479

    Article  Google Scholar 

  103. Wang H, den Hollander AI, Moayedi Y et al (2009) Mutations in SPATA7 cause Leber congenital amaurosis and juvenile retinitis pigmentosa. Am J Hum Genet 84:380–387

    Article  CAS  Google Scholar 

  104. Eblimit A, Nguyen T-MT, Chen Y et al (2015) Spata7 is a retinal ciliopathy gene critical for correct RPGRIP1 localization and protein trafficking in the retina. Hum Mol Genet 24:1584–1601

    Article  CAS  Google Scholar 

  105. Petersen-Jones SM, Occelli LM, Winkler PA et al (2018) Patients and animal models of CNGβ1-deficient retinitis pigmentosa support gene augmentation approach. J Clin Invest 128:190–206

    Article  Google Scholar 

  106. Hüttl S, Michalakis S, Seeliger M et al (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J Neurosci 25:130–138

    Article  Google Scholar 

  107. Zacchigna S, Oh H, Wilsch-Bräuninger M et al (2009) Loss of the cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration. J Neurosci 29:2297–2308

    Article  CAS  Google Scholar 

  108. Sharif AS, Yu D, Loertscher S et al (2018) C8ORF37 is required for photoreceptor outer segment disc morphogenesis by maintaining outer segment membrane protein homeostasis. J Neurosci 38:3160–3176

    Article  CAS  Google Scholar 

  109. Liou GI, Fei Y, Peachey NS et al (1998) Early onset photoreceptor abnormalities induced by targeted disruption of the interphotoreceptor retinoid-binding protein gene. J Neurosci 18:4511–4520

    Article  CAS  Google Scholar 

  110. Moshiri A, Humpal D, Leonard BC et al (2017) Arap1 deficiency causes photoreceptor degeneration in mice. Invest Ophthalmol Vis Sci 58:1709–1718

    Article  CAS  Google Scholar 

  111. Davis RJ, Tosi J, Janisch KM et al (2008) Functional rescue of degenerating photoreceptors in mice homozygous for a hypomorphic cGMP phosphodiesterase 6 b allele (Pde6b H620Q). Invest Ophthalmol Vis Sci 49:5067–5076

    Article  Google Scholar 

  112. Koch SF, Duong JK, Hsu C-W et al (2017) Genetic rescue models refute nonautonomous rod cell death in retinitis pigmentosa. PNAS 114:5259–5264

    Article  CAS  Google Scholar 

  113. Tsang SH, Gouras P, Yamashita CK et al (1996) Retinal degeneration in mice lacking the γ subunit of the rod cGMP phosphodiesterase. Science 272:1026–1029

    Article  CAS  Google Scholar 

  114. Sakamoto K, McCluskey M, Wensel TG et al (2009) New mouse models for recessive retinitis pigmentosa caused by mutations in the Pde6a gene. Hum Mol Genet 18:178–192

    Article  CAS  Google Scholar 

  115. Nishimura DY, Baye LM, Perveen R et al (2010) Discovery and functional analysis of a retinitis pigmentosa gene, C2ORF71. Am J Hum Genet 86:686–695

    Article  CAS  Google Scholar 

  116. Li C, Wang L, Zhang J et al (2014) CERKL interacts with mitochondrial TRX2 and protects retinal cells from oxidative stress-induced apoptosis. Biochim Biophys Acta 1842:1121–1129

    Article  CAS  Google Scholar 

  117. Lehmann M, Knust E, Hebbar S (2019) Drosophila melanogaster: a valuable genetic model organism to elucidate the biology of retinitis pigmentosa. In: Weber BHF, Langmann T (eds) Retinal degeneration: methods and protocols. Springer New York, New York, pp 221–249

    Chapter  Google Scholar 

  118. Pelletier V, Jambou M, Delphin N et al (2007) Comprehensive survey of mutations in RP2 and RPGR in patients affected with distinct retinal dystrophies: genotype-phenotype correlations and impact on genetic counseling. Hum Mutat 28:81–91

    Article  CAS  Google Scholar 

  119. Vervoort R, Lennon A, Bird AC et al (2000) Mutational hot spot within a new RPGR exon in X-linked retinitis pigmentosa. Nat Genet 25:462–466

    Article  CAS  Google Scholar 

  120. Tee JJL, Smith AJ, Hardcastle AJ et al (2016) RPGR-associated retinopathy: clinical features, molecular genetics, animal models and therapeutic options. Br J Ophthalmol 100:1022–1027

    Article  Google Scholar 

  121. Khanna H, Hurd TW, Lillo C et al (2005) RPGR-ORF15, which is mutated in retinitis pigmentosa, associates with SMC1, SMC3, and microtubule transport proteins. J Biol Chem 280:33580–33587

    Article  CAS  Google Scholar 

  122. Khanna H, Davis EE, Murga-Zamalloa CA et al (2009) A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies. Nat Genet 41:739–745

    Article  CAS  Google Scholar 

  123. Randall CJ, McLachlan I (1979) Retinopathy in commercial layers. Vet Rec 105:41–42

    Article  CAS  Google Scholar 

  124. Randall CJ, Wilson MA, Pollock BJ et al (1983) Partial retinal dysplasia and subsequent degeneration in a mutant strain of domestic fowl (rdd). Exp Eye Res 37:337–347

    Article  CAS  Google Scholar 

  125. Burt DW, Morrice DR, Lester DH et al (2003) Analysis of the rdd locus in chicken: a model for human retinitis pigmentosa. Mol Vis 9:164–170

    CAS  Google Scholar 

  126. Ali M, Hocking PM, McKibbin M et al (2011) Mpdz null allele in an avian model of retinal degeneration and mutations in human Leber congenital amaurosis and retinitis pigmentosa. Invest Ophthalmol Vis Sci 52:7432–7440

    Article  CAS  Google Scholar 

  127. van de Pavert SA, Kantardzhieva A, Malysheva A et al (2004) Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci 117:4169–4177

    Article  Google Scholar 

  128. West EL, Pearson RA, Tschernutter M et al (2008) Pharmacological disruption of the outer limiting membrane leads to increased retinal integration of transplanted photoreceptor precursors. Exp Eye Res 86:601–611

    Article  CAS  Google Scholar 

  129. Pearson RA, Barber AC, West EL et al (2010) Targeted disruption of outer limiting membrane junctional proteins (Crb1 and ZO-1) increases integration of transplanted photoreceptor precursors into the adult wild-type and degenerating retina. Cell Transplant 19:487–503

    Article  CAS  Google Scholar 

  130. Zeiss CJ, Acland GM, Aguirre GD (1999) Retinal pathology of canine X-linked progressive retinal atrophy, the locus homologue of RP3. Invest Ophthalmol Vis Sci 40:3292–3304

    CAS  Google Scholar 

  131. Zhang Q, Acland GM, Wu WX et al (2002) Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration. Hum Mol Genet 11:993–1003

    Article  CAS  Google Scholar 

  132. Beltran WA, Hammond P, Acland GM et al (2006) A frameshift mutation in RPGR exon ORF15 causes photoreceptor degeneration and inner retina remodeling in a model of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci 47:1669–1681

    Article  Google Scholar 

  133. Thompson DA, Khan NW, Othman MI et al (2012) Rd9 is a naturally occurring mouse model of a common form of retinitis pigmentosa caused by mutations in RPGR-ORF15. PLoS One 7:e35865

    Article  CAS  Google Scholar 

  134. Hong D-H, Pawlyk BS, Shang J et al (2000) A retinitis pigmentosa GTPase regulator (RPGR)- deficient mouse model for X-linked retinitis pigmentosa (RP3). PNAS 97:3649–3654

    Article  CAS  Google Scholar 

  135. Guo H, Li J, Gao F et al (2015) Whole-exome sequencing reveals a novel CHM gene mutation in a family with choroideremia initially diagnosed as retinitis pigmentosa. BMC Ophthalmol 15:1–7

    Article  Google Scholar 

  136. Tolmachova T, Anders R, Abrink M et al (2006) Independent degeneration of photoreceptors and retinal pigment epithelium in conditional knockout mouse models of choroideremia. J Clin Invest 116:386–394

    Article  CAS  Google Scholar 

  137. Simunovic MP, Jolly JK, Xue K et al (2016) The spectrum of CHM gene mutations in choroideremia and their relationship to clinical phenotype. Invest Ophthalmol Vis Sci 57:6033–6039

    Article  CAS  Google Scholar 

  138. Shu X, Zeng Z, Gautier P et al (2010) Zebrafish Rpgr is required for normal retinal development and plays a role in dynein-based retrograde transport processes. Hum Mol Genet 19:657–670

    Article  CAS  Google Scholar 

  139. Raghupathy RK, McCulloch DL, Akhtar S et al (2014) Pathogenesis of X-linked RP3: insights from animal models. Adv Exp Med Biol 801:477–485

    Article  Google Scholar 

  140. Shu X, Zeng Z, Gautier P et al (2011) Knockdown of the zebrafish ortholog of the retinitis pigmentosa 2 (RP2) gene results in retinal degeneration. Invest Ophthalmol Vis Sci 52:2960–2966

    Article  CAS  Google Scholar 

  141. Evans RJ, Schwarz N, Nagel-Wolfrum K et al (2010) The retinitis pigmentosa protein RP2 links pericentriolar vesicle transport between the Golgi and the primary cilium. Hum Mol Genet 19:1358–1367

    Article  CAS  Google Scholar 

  142. Hurd T, Zhou W, Jenkins P et al (2010) The retinitis pigmentosa protein RP2 interacts with polycystin 2 and regulates cilia-mediated vertebrate development. Hum Mol Genet 19:4330–4344

    Article  CAS  Google Scholar 

  143. Boughman JA, Vernon M, Shaver KA (1983) Usher syndrome: definition and estimate of prevalence from two high-risk populations. J Chronic Dis 36:595–603

    Article  CAS  Google Scholar 

  144. Norris DP, Grimes DT (2012) Mouse models of ciliopathies: the state of the art. Dis Model Mech 5:299–312

    Article  CAS  Google Scholar 

  145. Li G, Vega R, Nelms K et al (2007) A role for Alström syndrome protein, Alms1, in kidney ciliogenesis and cellular quiescence. PLoS Genet 3:e8

    Article  Google Scholar 

  146. Collin GB, Cyr E, Bronson R et al (2005) Alms1-disrupted mice recapitulate human Alström syndrome. Hum Mol Genet 14:2323–2333

    Article  CAS  Google Scholar 

  147. Mykytyn K, Mullins RF, Andrews M et al (2004) Bardet–Biedl syndrome type 4 (BBS4)-null mice implicate Bbs4 in flagella formation but not global cilia assembly. PNAS 101:8664–8669

    Article  CAS  Google Scholar 

  148. Stubdal H, Lynch CA, Moriarty A et al (2000) Targeted deletion of the tub mouse obesity gene reveals that tubby is a loss-of-function mutation. Mol Cell Biol 20:878–882

    Article  CAS  Google Scholar 

  149. Forsythe E, Beales PL (2013) Bardet–Biedl syndrome. Eur J Hum Genet 21:8–13

    Article  CAS  Google Scholar 

  150. Hamel CP (2007) Cone rod dystrophies. Orphanet J Rare Dis 2:7

    Article  Google Scholar 

  151. Nishimura DY, Fath M, Mullins RF et al (2004) Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin. PNAS 101:16588–16593

    Article  CAS  Google Scholar 

  152. Zhang Q, Nishimura D, Seo S et al (2011) Bardet-Biedl syndrome 3 (Bbs3) knockout mouse model reveals common BBS-associated phenotypes and Bbs3 unique phenotypes. PNAS 108:20678–20683

    Article  CAS  Google Scholar 

  153. Abd-El-Barr MM, Sykoudis K, Andrabi S et al (2007) Impaired photoreceptor protein transport and synaptic transmission in a mouse model of Bardet–Biedl syndrome. Vis Res 47:3394–3407

    Article  CAS  Google Scholar 

  154. Ross AJ, May-Simera H, Eichers ER et al (2005) Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat Genet 37:1135–1140

    Article  CAS  Google Scholar 

  155. Davis RE, Swiderski RE, Rahmouni K et al (2007) A knockin mouse model of the Bardet–Biedl syndrome 1 M390R mutation has cilia defects, ventriculomegaly, retinopathy, and obesity. PNAS 104:19422–19427

    Article  CAS  Google Scholar 

  156. Lockhart CM, Nakano M, Rettie AE et al (2014) Generation and characterization of a murine model of Bietti crystalline dystrophy. Invest Ophthalmol Vis Sci 55:5572–5581

    Article  CAS  Google Scholar 

  157. Lai TYY, Chu K-O, Chan K-P et al (2010) Alterations in serum fatty acid concentrations and desaturase activities in Bietti crystalline dystrophy unaffected by CYP4V2 genotypes. Invest Ophthalmol Vis Sci 51:1092–1097

    Article  Google Scholar 

  158. Audo I, Vanakker OM, Smith A et al (2007) Pseudoxanthoma elasticum with generalized retinal dysfunction, a common finding? Invest Ophthalmol Vis Sci 48:4250–4256

    Article  Google Scholar 

  159. Roth BM, Yuan A, Ehlers JP (2012) Retinal and choroidal findings in oxalate retinopathy using EDI-OCT. Ophthalmic Surg Lasers Imaging 43:S142–S144

    Article  Google Scholar 

  160. Choi RY, Chortkoff SC, Gorusupudi A et al (2016) Crystalline maculopathy associated with high-dose lutein supplementation. JAMA Ophthalmol 134:1445–1448

    Article  Google Scholar 

  161. Karikkineth AC, Scheibye-Knudsen M, Fivenson E et al (2017) Cockayne syndrome: clinical features, model systems and pathways. Ageing Res Rev 33:3–17

    Article  CAS  Google Scholar 

  162. van der Horst GTJ, van Steeg H, Berg RJW et al (1997) Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 89:425–435

    Article  Google Scholar 

  163. Gorgels TGMF, van der Pluijm I, Brandt RMC et al (2007) Retinal degeneration and ionizing radiation hypersensitivity in a mouse model for Cockayne syndrome. Mol Cell Biol 27:1433–1441

    Article  CAS  Google Scholar 

  164. Jacobsohn E (1888) Ein Fall von Retinitis pigmentosa atypica. Klin Monatsbl Augenheilkd 26:202–206

    Google Scholar 

  165. Wang T, Milam AH, Steel G et al (1996) A mouse model of gyrate atrophy of the choroid and retina. Early retinal pigment epithelium damage and progressive retinal degeneration. J Clin Invest 97:2753–2762

    Article  CAS  Google Scholar 

  166. Sergouniotis PI, Davidson AE, Lenassi E et al (2012) Retinal structure, function, and molecular pathologic features in gyrate atrophy. Ophthalmology 119:596–605

    Article  Google Scholar 

  167. Bisaillon JJ, Radden LA, Szabo ET et al (2014) The retarded hair growth (rhg) mutation in mice is an allele of ornithine aminotransferase (Oat). Mol Genet Metab Rep 1:378–390

    Article  CAS  Google Scholar 

  168. Wang T, Lawler AM, Steel G et al (1995) Mice lacking ornithine–δ–amino–transferase have paradoxical neonatal hypoornithinaemia and retinal degeneration. Nat Genet 11:185–190

    Article  Google Scholar 

  169. Curtain M, Donahue LR, Ward-Bailey PF (2009) Cataracts and retarded hair growth in rhg. MGI Direct Data Submission:7

    Google Scholar 

  170. Kaiser-Kupfer MI, Ludwig IH, de Monasterio FM et al (1985) Gyrate atrophy of the choroid and retina: early findings. Ophthalmology 92:394–401

    Article  CAS  Google Scholar 

  171. Louie CM, Caridi G, Lopes VS et al (2010) AHI1 is required for photoreceptor outer segment development and is a modifier for retinal degeneration in nephronophthisis. Nat Genet 42:175–180

    Article  CAS  Google Scholar 

  172. Joubert syndrome. https://ghr.nlm.nih.gov/condition/joubert-syndrome

  173. Rachel RA, Yamamoto EA, Dewanjee MK et al (2015) CEP290 alleles in mice disrupt tissue-specific cilia biogenesis and recapitulate features of syndromic ciliopathies. Hum Mol Genet 24:3775–3791

    Article  CAS  Google Scholar 

  174. Bongorno J, Guy J, Lewin AS (2004) 437. Developing a mouse model of the mitochondrial NARP syndrome using AAV-ribozymes for ATP6. Mol Ther 9:S167

    Article  Google Scholar 

  175. NARP. https://ghr.nlm.nih.gov/condition/neuropathy-ataxia-and-retinitis-pigmentosa

  176. Refsum disease. https://ghr.nlm.nih.gov/condition/refsum-disease

  177. Wierzbicki AS, Lloyd MD, Schofield CJ et al (2002) Refsum’s disease: a peroxisomal disorder affecting phytanic acid α-oxidation. J Neurochem 80:727–735

    Article  CAS  Google Scholar 

  178. Ronquillo CC, Bernstein PS, Baehr W (2012) Senior–Løken syndrome: a syndromic form of retinal dystrophy associated with nephronophthisis. Vis Res 75:88–97

    Article  CAS  Google Scholar 

  179. Jiang S-T, Chiou Y-Y, Wang E et al (2009) Essential role of nephrocystin in photoreceptor intraflagellar transport in mouse. Hum Mol Genet 18:1566–1577

    Article  CAS  Google Scholar 

  180. Won J, de Evsikova CM, Smith RS et al (2011) NPHP4 is necessary for normal photoreceptor ribbon synapse maintenance and outer segment formation, and for sperm development. Hum Mol Genet 20:482–496

    Article  CAS  Google Scholar 

  181. Collin GB, Won J, Hicks WL et al (2012) Meckelin is necessary for photoreceptor intraciliary transport and outer segment morphogenesis. Invest Ophthalmol Vis Sci 53:967–974

    Article  CAS  Google Scholar 

  182. Tammachote R, Hommerding CJ, Sinders RM et al (2009) Ciliary and centrosomal defects associated with mutation and depletion of the Meckel syndrome genes MKS1 and MKS3. Hum Mol Genet 18:3311–3323

    Article  CAS  Google Scholar 

  183. Williams DS (2008) Usher syndrome: animal models, retinal function of Usher proteins, and prospects for gene therapy. Vis Res 48:433–441

    Article  CAS  Google Scholar 

  184. Johnson KR, Gagnon LH, Webb LS et al (2003) Mouse models of USH1C and DFNB18: phenotypic and molecular analyses of two new spontaneous mutations of the Ush1c gene. Hum Mol Genet 12:3075–3086

    Article  CAS  Google Scholar 

  185. Lentz JJ, Gordon WC, Farris HE et al (2010) Deafness and retinal degeneration in a novel USH1C knock-in mouse model. Dev Neurobiol 70:253–267

    Article  CAS  Google Scholar 

  186. Liu X, Bulgakov OV, Darrow KN et al (2007) Usherin is required for maintenance of retinal photoreceptors and normal development of cochlear hair cells. PNAS 104:4413–4418

    Article  CAS  Google Scholar 

  187. Noben-Trauth K, Naggert JK, North MA et al (1996) A candidate gene for the mouse mutation tubby. Nature 380:534–538

    Article  CAS  Google Scholar 

  188. Menotti-Raymond M, Deckman KH, David V et al (2010) Mutation discovered in a feline model of human congenital retinal blinding disease. Invest Ophthalmol Vis Sci 51:2852–2859

    Article  Google Scholar 

  189. Nour M, Fliesler SJ, Naash MI (2008) Genetic supplementation of RDS alleviates a loss-of-function phenotype in C214S model of retinitis pigmentosa. Adv Exp Med Biol 613:129–138

    Article  CAS  Google Scholar 

  190. Cai X, Conley SM, Naash MI (2010) Gene therapy in the retinal degeneration slow model of retinitis pigmentosa. In: Anderson RE, Hollyfield JG, LaVail MM (eds) Retinal degenerative diseases. Springer New York, New York, pp 611–619

    Chapter  Google Scholar 

  191. Li T, Franson WK, Gordon JW et al (1995) Constitutive activation of phototransduction by K296E opsin is not a cause of photoreceptor degeneration. PNAS 92:3551–3555

    Article  CAS  Google Scholar 

  192. Peachey NS, Wang M, Naash MI (1997) The Vpp Mouse. In: LaVail MM, Hollyfield JG, Anderson RE (eds) Degenerative retinal diseases. Springer US, Boston, pp 89–97

    Chapter  Google Scholar 

  193. Choi EH, Suh S, Sander CL et al (2018) Insights into the pathogenesis of dominant retinitis pigmentosa associated with a D477G mutation in RPE65. Hum Mol Genet 27:2225–2243

    Article  CAS  Google Scholar 

  194. Dekomien G, Vollrath C, Petrasch-Parwez E et al (2010) Progressive retinal atrophy in Schapendoes dogs: mutation of the newly identified CCDC66 gene. Neurogenetics 11:163–174

    Article  CAS  Google Scholar 

  195. Ahonen SJ, Arumilli M, Lohi H (2013) A CNGB1 frameshift mutation in Papillon and Phalène dogs with progressive retinal atrophy. PLoS One 8:e72122

    Article  CAS  Google Scholar 

  196. Downs LM, Mellersh CS (2014) An intronic SINE insertion in FAM161A that causes exon-skipping is associated with progressive retinal atrophy in Tibetan Spaniels and Tibetan Terriers. PLoS One 9:e93990

    Article  Google Scholar 

  197. Scott RS, McMahon EJ, Pop SM et al (2001) Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411:207

    Article  CAS  Google Scholar 

  198. McHenry CL, Liu Y, Feng W et al (2004) MERTK arginine-844-cysteine in a patient with severe rod-cone dystrophy: loss of mutant protein function in transfected cells. Invest Ophthalmol Vis Sci 45:1456–1463

    Article  Google Scholar 

  199. Gal A, Li Y, Thompson DA et al (2000) Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 26:270–271

    Article  CAS  Google Scholar 

  200. Smith SB (1992) C57BL/6J-vit/vit mouse model of retinal degeneration: light microscopic analysis and evaluation of rhodopsin levels. Exp Eye Res 55:903–910

    Article  CAS  Google Scholar 

  201. Tang M, Pawlyk BS, Kosaras B et al (1997) ERG abnormalities in relation to histopathologic findings in vitiligo mutant mice. Exp Eye Res 65:215–222

    Article  CAS  Google Scholar 

  202. Pittler SJ, Keeler CE, Sidman RL et al (1993) PCR analysis of DNA from 70-year-old sections of rodless retina demonstrates identity with the mouse rd defect. PNAS 90:9616–9619

    Article  CAS  Google Scholar 

  203. Farber DB (1995) From mice to men: the cyclic GMP phosphodiesterase gene in vision and disease. The Proctor lecture. Invest Ophthalmol Vis Sci 36:263–275

    CAS  Google Scholar 

  204. Wu W-H, Tsai Y-T, Justus S et al (2016) CRISPR repair reveals causative mutation in a preclinical model of retinitis pigmentosa. Mol Ther 24:1388–1394

    Article  CAS  Google Scholar 

  205. Bunel M, Chaudieu G, Hamel C et al (2019) Natural models for retinitis pigmentosa: progressive retinal atrophy in dog breeds. Hum Genet 138:441–453

    Article  CAS  Google Scholar 

  206. Cai X, Conley SM, Naash MI (2009) RPE65: role in the visual cycle, human retinal disease, and gene therapy. Ophthalmic Genet 30:57

    Article  CAS  Google Scholar 

  207. Goldstein O, Jordan JA, Aguirre GD et al (2013) A non-stop S-antigen gene mutation is associated with late onset hereditary retinal degeneration in dogs. Mol Vis 19:1871–1884

    CAS  Google Scholar 

  208. Downs LM, Wallin-Håkansson B, Boursnell M et al (2011) A frameshift mutation in golden retriever dogs with progressive retinal atrophy endorses SLC4A3 as a candidate gene for human retinal degenerations. PLoS One 6:e21452

    Article  CAS  Google Scholar 

  209. Goldstein O, Kukekova AV, Aguirre GD et al (2010) Exonic SINE insertion in STK38L causes canine early retinal degeneration (erd). Genomics 96:362–368

    Article  CAS  Google Scholar 

  210. Downs LM, Wallin-Håkansson B, Bergström T et al (2014) A novel mutation in TTC8 is associated with progressive retinal atrophy in the golden retriever. Canine Genet Epidemiol 1:4

    Article  Google Scholar 

  211. Fath MA, Mullins RF, Searby C et al (2005) Mkks-null mice have a phenotype resembling Bardet–Biedl syndrome. Hum Mol Genet 14:1109–1118

    Article  CAS  Google Scholar 

  212. Smith UM, Consugar M, Tee LJ et al (2006) The transmembrane protein Meckelin (MKS3) is mutated in Meckel-Gruber syndrome and the wpk rat. Nat Genet 38:191–196

    Article  CAS  Google Scholar 

  213. Ohlemiller KK, Hughes RM, Lett JM et al (1997) Progression of cochlear and retinal degeneration in the tubby (rd5) mouse. Audiol Neurootol 2:175–185

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Travor, M.D. (2023). Preclinical Models of Retinitis Pigmentosa. In: Tsang, S.H., Quinn, P.M. (eds) Retinitis Pigmentosa. Methods in Molecular Biology, vol 2560. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2651-1_19

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2651-1_19

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2650-4

  • Online ISBN: 978-1-0716-2651-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics