Rd9 is a naturally occurring mouse model of a common form of retinitis pigmentosa caused by mutations in RPGR-ORF15

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Thompson, Debra A ^a   Khan, Naheed W ^a   Othman, Mohammad I ^a   Chang, Bo ^b   Jia, Lin ^a   Grahek, Garrett ^a   Wu, Zhijian ^c   Hiriyanna, Suja ^c   Nellissery, Jacob ^c   Li, Tiansen ^c   Khanna, Hemant ^d   Colosi, Peter ^c   Swaroop, Anand ^c   Heckenlively, John R ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b JACKSON LABORATORY   (United States)

^c NATIONAL EYE INSTITUTE   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; OPSIN; RETINITIS PIGMENTOSA GTPASE REGULATOR; RHODOPSIN; TRANSDUCIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; EYE PROTEIN; RPGR PROTEIN, MOUSE;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; CONTROLLED STUDY; ELECTRORETINOGRAM; FEMALE; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC ANALYSIS; MALE; MOUSE; NONHUMAN; OPEN READING FRAME; OUTER NUCLEAR LAYER THICKNESS; PIGMENT LOSS; PROTEIN EXPRESSION; RETINA CONE; RETINA DEGENERATION; RETINA DISEASE; RETINA ROD OUTER SEGMENT; RETINITIS PIGMENTOSA; RPGR GENE; STOP CODON; VISUAL SYSTEM PARAMETERS; X CHROMOSOME LINKED DISORDER; X LINKED RETINITIS PIGMENTOSA; 129 MOUSE; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; DISEASE MODEL; ELECTRORETINOGRAPHY; EXON; GENETICS; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; PATHOPHYSIOLOGY; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

ANIMALIA; MUS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; EXONS; EYE PROTEINS; FEMALE; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; MUTATION; RETINA; RETINAL DEGENERATION; RETINITIS PIGMENTOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODOPSIN; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84860487206     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035865     Document Type: Article

References (61)

1. Daiger SP, Bowne SJ, Sullivan LS, (2007) Perspective on genes and mutations causing retinitis pigmentosa. Arch Ophthalmol 125: 151-158.
2. Fishman GA, Farber MD, Derlacki DJ, (1988) X-linked retinitis pigmentosa: Profile of clinical findings. Arch Ophthalmol 106: 369-375.
3. Breuer DK, Yashar BM, Filippova E, Hiriyanna S, Lyons RH, et al. (2002) A comprehensive mutation analysis of RP2 and RPGR in a North American cohort of families with X-linked retinitis pigmentosa. Am J Hum Genet 70: 1545-1554.
4. Shu X, Blac GC, Rice JM, Hart-Holden N, Jones A, et al. (2007) RPGR mutation analysis and disease: an update. Hum Mutat 28: 322-328.
5. Vervoort R, Lennon A, Bird AC, Tulloch B, Axton R, et al. (2000) Mutational hot spot within a new RPGR exon in X-linked retinitis pigmentosa. Nat Genet 25: 462-466.
6. Andreasson S, Ponjavic V, Abrahamson M, Ehinger B, Wu W, et al. (1997) Phenotypes in three Swedish families with X-linked retinitis pigmentosa caused by different mutations in the RPGR gene. Am J Ophthalmol 124: 95-102.
7. Jacobson SG, Buraczynska M, Milam AH, Chen C, Jarvalainen M, et al. (1997) Disease expression in X-linked retinitis pigmentosa caused by a putative null mutation in the RPGR gene. Invest Ophthalmol Vis Sci 38: 1983-1997.
8. Lorenz B, Andrassi M, Kretschmann U, (2003) Phenotype in two families with RP3 associated with RPGR mutations. Ophthalmic Genet 24: 89-101.
9. Fishman GA, Grover S, Jacobson SG, Alexander KR, Derlacki DJ, et al. (1998) X-linked retinitis pigmentosa in two families with a missense mutation in the RPGR gene and putative change of glycine to valine at codon 60. Ophthalmology 105: 2286-2296.
10. Weleber RG, Butler NS, Murphey WH, Sheffield VC, Stone EM, (1997) X-linked retinitis pigmentosa associated with a 2-base pair insertion in codon 99 of the RP3 gene RPGR. Arch Ophthalmol 115: 1429-1435.
11. Ayyagari R, Demirci FY, Liu J, Bingham EL, Stringham H, et al. (2002) X-linked recessive atrophic macular degeneration from RPGR mutation. Genomics 80: 166-171.
12. Demirci FY, Rigatti BW, Wen G, Radak AL, Mah TS, et al. (2002) X-linked cone-rod dystrophy (locus COD1): identification of mutations in RPGR exon ORF15. Am J Hum Genet 70: 1049-1053.
13. Iannaccone A, Wang X, Jablonski MM, Kuo SF, Baldi A, et al. (2004) Increasing evidence for syndromic phenotypes associated with RPGR mutations. Am J Ophthalmol 137:785-786; author reply 786.
14. Yan D, Swain PK, Breuer D, Tucker RM, Wu W, et al. (1998) Biochemical characterization and subcellular localization of the mouse retinitis pigmentosa GTPase regulator (mRpgr). J Biol Chem 273: 19656-19663.
15. Shu X, Fry AM, Tulloch B, Manson FD, Crabb JW, et al. (2005) RPGR ORF15 isoform co-localizes with RPGRIP1 at centrioles and basal bodies and interacts with nucleophosmin. Hum Mol Genet 14: 1183-1197.
16. Hong DH, Pawlyk B, Sokolov M, Strissel KJ, Yang J, et al. (2003) RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Invest Ophthalmol Vis Sci 44: 2413-2421.
17. Khanna H, Hurd TW, Lillo C, Shu X, Parapuram SK, 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.
18. Hong DH, Yue G, Adamian M, Li T, (2001) Retinitis pigmentosa GTPase regulator (RPGRr)-interacting protein is stably associated with the photoreceptor ciliary axoneme and anchors RPGR to the connecting cilium. J Biol Chem 276: 12091-12099.
19. Boylan JP, Wright AF, (2000) Identification of a novel protein interacting with RPGR. Hum Mol Genet 9: 2085-2093.
20. Otto EA, Loeys B, Khanna H, Hellemans J, Sudbrak R, et al. (2005) Nephrocystin-5 a ciliary IQ domain protein is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat Genet 37: 282-288.
21. Chang B, Khanna H, Hawes N, Jimeno D, He S, 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.
22. Khanna H, Davis EE, Murga-Zamalloa CA, Estrada-Cuzcano A, Lopez I, et al. (2009) A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies. Nat Genet 41: 739-745.
23. Murga-Zamalloa CA, Atkins SJ, Peranen J, Swaroop A, Khanna H, (2010) Interaction of retinitis pigmentosa GTPase regulator (RPGR) with RAB8A GTPase: implications for cilia dysfunction and photoreceptor degeneration. Hum Mol Genet 19: 3591-3598.
24. Ghosh AK, Murga-Zamalloa CA, Chan L, Hitchcock PF, Swaroop A, et al. (2010) Human retinopathy-associated ciliary protein retinitis pigmentosa GTPase regulator mediates cilia-dependent vertebrate development. Hum Mol Genet 19: 90-98.
25. Shu X, Zeng Z, Gautier P, Lennon A, Gakovic M, 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.
26. Hong DH, Pawlyk BS, Shang J, Sandberg MA, Berson EL, et al. (2000) A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc Natl Acad Sci U S A 97: 3649-3654.
27. Brunner S, Skosyrski S, Kirschner-Schwabe R, Knobeloch KP, Neidhardt J, et al. (2010) Cone versus rod disease in a mutant Rpgr mouse caused by different genetic backgrounds. Invest Ophthalmol Vis Sci 51: 1106-1115.
28. Zhang Q, Acland GM, Wu WX, Johnson JL, Pearce-Kelling S, et al. (2002) Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration. Hum Mol Genet 11: 993-1003.
29. Beltran WA, Cideciyan AV, Lewin AS, Iwabe S, Khanna H, et al. (2012) Gene therapy rescues photoreceptor blindness in dogs and paves the way for treating human X-linked retinitis pigmentosa. Proc Natl Acad Sci U S A 109: 2132-2137.
30. Chang B, Hawes NL, Hurd RE, Davisson MT, Nusinowitz S, et al. (2002) Retinal degeneration mutants in the mouse. Vision Res 42 517-525.
31. Maeda A, Maeda T, Imanishi Y, Kuksa V, Alekseev A, et al. (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J Biol Chem 280 18822-18832.
32. He S, Parapuram SK, Hurd TW, Behnam B, Margolis B, et al. (2008) Retinitis Pigmentosa GTPase Regulator (RPGR) protein isoforms in mammalian retina: insights into X-linked Retinitis Pigmentosa and associated ciliopathies. Vision Res 48: 366-376.
33. Khorana HG, Knox BE, Nasi E, Swanson R, Thompson DA, (1988) Expression of a bovine rhodopsin gene in Xenopus oocytes: demonstration of light-dependent ionic currents. Proc Natl Acad Sci U S A 85: 7917-7921.
34. Hemati N, Feathers KL, Chrispell JD, Reed DM, Carlson TJ, et al. (2005) RPE65 surface epitopes protein interactions and expression in rod- and cone-dominant species. Mol Vis 11: 1151-1165.
35. LaVail MM, Matthes MT, Yasumura D, Faktorovich EG, Steinberg RH, (1997) Histological method to assess photoreceptor light damage and protection by survival factors. Plenum Press New York.
36. Nusinowitz S, Ridder WH III, Heckenlively JR, (2002) Electrophysiologic testing of the mouse visual system In: Systematic evaluation of the mouse eye. John SWM Nishina PM Sundberg JP eds 320-332.
37. Chavali VR, Khan NW, Cukras CA, Bartsch DU, Jablonski MM, et al. (2011) A CTRP5 gene S163R mutation knock-in mouse model for late-onset retinal degeneration. Hum Mol Genet 20: 2000-2014.
38. Machida S, Raz-Prag D, Fariss RN, Sieving PA, Bush RA, (2008) Photopic ERG negative response from amacrine cell signaling in RCS rat retinal degeneration. Invest Ophthalmol Vis Sci 49: 442-452.
39. Viswanathan S, Frishman LJ, Robson JG, Walters JW, (2001) The photopic negative response of the flash electroretinogram in primary open angle glaucoma. Invest Ophthalmol Vis Sci 42: 514-522.
40. Wali N, Leguire LE, (1991) Dark-adapted luminance-response functions with skin and corneal electrodes. Doc Ophthalmol 76 367-375.
41. Gresh J, Goletz PW, Crouch RK, Rohrer B, (2003) Structure-function analysis of rods and cones in juvenile adult and aged C57bl/6 and Balb/c mice. Vis Neurosci 20: 211-220.
42. Breton ME, Schueller AW, Lamb TD, Pugh EN Jr, (1994) Analysis of ERG a-wave amplification and kinetics in terms of the G-protein cascade of phototransduction. Invest Ophthalmol Vis Sci 35: 295-309.
43. Penn RD, Hagins WA, (1969) Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223: 201-204.
44. Hood DC, Birch DG, (1992) A computational model of the amplitude and implicit time of the b-wave of the human ERG. Vis Neurosci 8: 107-126.
45. Robson JG, Frishman LJ, (1995) Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12: 837-850.
46. Stockton RA, Slaughter MM, (1989) B-wave of the electroretinogram A reflection of ON bipolar cell activity. J Gen Physiol 93: 101-122.
47. Aleman TS, LaVail MM, Montemayor R, Ying G, Maguire MM, et al. (2001) Augmented rod bipolar cell function in partial receptor loss: an ERG study in P23H rhodopsin transgenic and aging normal rats. Vision Res 41: 2779-2797.
48. Wachtmeister L, (1998) Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res 17: 485-521.
49. Machida S, Kondo M, Jamison JA, Khan NW, Kononen LT, et al. (2000) P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci 41: 3200-3209.
50. Beltran WA, Hammond P, Acland GM, Aguirre GD, (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.
51. Aleman TS, Cideciyan AV, Sumaroka A, Schwartz SB, Roman AJ, et al. (2007) Inner retinal abnormalities in X-linked retinitis pigmentosa with RPGR mutations. Invest Ophthalmol Vis Sci 48: 4759-4765.
52. Adamian M, Pawlyk BS, Hong DH, Berson EL, (2006) Rod and cone opsin mislocalization in an autopsy eye from a carrier of X-linked retinitis pigmentosa with a Gly436Asp mutation in the RPGR gene. Am J Ophthalmol 142: 515-518.
53. Aguirre GD, Yashar BM, John SK, Smith JE, Breuer DK, et al. (2002) Retinal histopathology of an XLRP carrier with a mutation in the RPGR exon ORF15. Exp Eye Res 75: 431-443.
54. Rohrer B, Lohr HR, Humphries P, Redmond TM, Seeliger M, 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.
55. Beltran WA, Acland GM, Aguirre GD, (2009) Age-dependent disease expression determines remodeling of the retinal mosaic in carriers of RPGR exon ORF15 mutations. Invest Ophthalmol Vis Sci 50: 3985-3995.
56. Ben-Arie-Weintrob Y, Berson EL, Dryja TP, (2005) Histopathologic-genotypic correlations in retinitis pigmentosa and allied diseases. Ophthalmic Genet 26: 91-100.
57. Neidhardt J, Glaus E, Lorenz B, Netzer C, Li Y, et al. (2008) Identification of novel mutations in X-linked retinitis pigmentosa families and implications for diagnostic testing. Mol Vis 14: 1081-1093.
58. Sandberg MA, Rosner B, Weigel-DiFranco C, Dryja TP, Berson EL, (2007) Disease course of patients with X-linked retinitis pigmentosa due to RPGR gene mutations. Invest Ophthalmol Vis Sci 48: 1298-1304.
59. Fahim AT, Bowne SJ, Sullivan LS, Webb KD, Williams JT, et al. (2011) Allelic heterogeneity and genetic modifier loci contribute to clinical variation in males with X-linked retinitis pigmentosa due to RPGR mutations. PLoS One 6 e2302.
60. Sharon D, Sandberg MA, Rabe VW, Stillberger M, Dryja TP, et al. (2003) RP2 and RPGR mutations and clinical correlations in patients with X-linked retinitis pigmentosa. Am J Hum Genet 73: 1131-1146.
61. Cideciyan AV, Aleman TS, Jacobson SG, Khanna H, Sumaroka A, et al. (2007) Centrosomal-ciliary gene CEP290/NPHP6 mutations result in blindness with unexpected sparing of photoreceptors and visual brain: implications for therapy of Leber congenital amaurosis. Hum Mutat 28: 1074-1083.