Deletion of myosin VI causes slow retinal optic neuropathy and age-related macular degeneration (AMD)-relevant retinal phenotype

Cellular and Molecular Life Sciences

Volumn 72, Issue 20, 2015, Pages 3953-3969

  Schubert, Timm ^a   Gleiser, Corinna ^a   Heiduschka, Peter ^b,c   Franz, Christoph ^b   Nagel Wolfrum, Kerstin ^d   Sahaboglu, Ayse ^b   Weisschuh, Nicole ^b   Eske, Gordon ^a   Rohbock, Karin ^b   Rieger, Norman ^b   Paquet Durand, François ^b   Wissinger, Bernd ^b   Wolfrum, Uwe ^d   Hirt, Bernhard ^a   Singer, Wibke ^b   Rüttiger, Lukas ^b   Zimmermann, Ulrike ^b   Knipper, Marlies ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Bipolar cell; Choriocapillaris; Inner retina; Mouse model; Outer retina; Stereocilia; Synapse; Translocator protein TSPO

Indexed keywords

MYOSIN VI; MYOSIN HEAVY CHAIN;

AGE; AGE RELATED MACULAR DEGENERATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL INFILTRATION; CONTROLLED STUDY; ELECTRORETINOGRAM; FEMALE; GENE DELETION; GENOTYPE; HISTOPATHOLOGY; IMMUNOREACTIVITY; MACULAR DEGENERATION; MALE; MICROGLIA; MOUSE; MYOSIN VI GENE; NONHUMAN; OPTIC NERVE DISEASE; PHENOTYPE; PHOTORECEPTOR CELL; PIGMENT EPITHELIUM; RETINAL OPTIC NEUROPATHY; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; RETINA;

ANIMALS; GENE DELETION; GENOTYPE; MACULAR DEGENERATION; MICE; MICE, INBRED C57BL; MICROGLIA; MYOSIN HEAVY CHAINS; OPTIC NERVE DISEASES; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA;

EID: 84942372083     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1913-3     Document Type: Article

References (73)

1. Hasson T, Mooseker MS (1996) Vertebrate unconventional myosins. J Biol Chem 271:16431-16434
2. Buss F, Kendrick-Jones J (2008) How are the cellular functions of myosin VI regulated within the cell? Biochem Biophys Res Commun 369:165-175
3. Avraham KB, Hasson T, Steel KP, Kingsley DM, Russell LB, Mooseker MS, Copeland NG, Jenkins NA (1995) The mouse Snell's Waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat Genet 11:369-375
4. Breckler J, Au K, Cheng J, Hasson T, Burnside B (2000) Novel myosin VI isoform is abundantly expressed in retina. Exp Eye Res 70:121-134
5. Kitamoto J, Libby RT, Gibbs D, Steel KP, Williams DS (2005) Myosin VI is required for normal retinal function. Exp Eye Res 81:116-120
6. Hertzano R, Shalit E, Rzadzinska AK, Dror AA, Song L, Ron U, Tan JT, Shitrit AS, Fuchs H, Hasson T et al (2008) A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells. PLoS Genet 4:e1000207
7. Heidrych P, Zimmermann U, Kuhn S, Franz C, Engel J, Duncker SV, Hirt B, Pusch CM, Ruth P, Pfister M et al (2009) Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum Mol Genet 18:2779-2790
8. Duncker SV, Franz C, Kuhn S, Schulte U, Campanelli D, Brandt N, Hirt B, Fakler B, Blin N, Ruth P et al (2013) Otoferlin couples to clathrin-mediated endocytosis in mature cochlear inner hair cells. J Neurosci 33:9508-9519
9. Tumbarello DA, Kendrick-Jones J, Buss F (2013) Myosin VI and its cargo adaptors - linking endocytosis and autophagy. J Cell Sci 126:2561-2570
10. Samuels IS, Bell BA, Sturgill-Short G, Ebke LA, Rayborn M, Shi L, Nishina PM, Peachey NS (2013) Myosin 6 is required for iris development and normal function of the outer retina. Invest Ophthalmol Vis Sci 54:7223-7233
11. Saksens NT, Fleckenstein M, Schmitz-Valckenberg S, Holz FG, den Hollander AI, Keunen JE, Boon CJ, Hoyng CB (2014) Macular dystrophies mimicking age-related macular degeneration. Prog Retin Eye Res 39:23-57
12. Mirza M, Volz C, Karlstetter M, Langiu M, Somogyi A, Ruonala MO, Tamm ER, Jagle H, Langmann T (2013) Progressive retinal degeneration and glial activation in the CLN6 (nclf) mouse model of neuronal ceroid lipofuscinosis: a beneficial effect of DHA and curcumin supplementation. PLoS One 8:e75963
13. Langmann T (2007) Microglia activation in retinal degeneration. J Leukoc Biol 81:1345-1351
14. Karlstetter M, Nothdurfter C, Aslanidis A, Moeller K, Horn F, Scholz R, Neumann H, Weber BH, Rupprecht R, Langmann T (2014) Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J Neuroinflammation 11:3. doi: 10.1186/1742-2094-1111-1183
15. Wierzbowska J, Figurska M, Stankiewicz A, Sierdzinski J (2008) Risk factors in age-related macular degeneration and glaucoma - own observations. Klin Oczna 110:370-374
16. Self T, Sobe T, Copeland NG, Jenkins NA, Avraham KB, Steel KP (1999) Role of myosin VI in the differentiation of cochlear hair cells. Dev Biol 214:331-341
17. Sahaboglu A, Tanimoto N, Bolz S, Garrido MG, Ueffing M, Seeliger MW, Löwenheim H, Ekstrom P, Paquet-Durand F (2014) Knockout of PARG110 confers resistance to cGMP-induced toxicity in mammalian photoreceptors. Cell Death Dis 5:e1234
18. Karlstetter M, Langmann T (2014) Microglia in the aging retina. Adv Exp Med Biol 801:207-212
19. Weleber RG (1998) The dystrophic retina in multisystem disorders: the electroretinogram in neuronal ceroid lipofuscinoses. Eye (Lond) 12(Pt 3b):580-590
20. Mattapallil MJ, Wawrousek EF, Chan CC, Zhao H, Roychoudhury J, Ferguson TA, Caspi RR (2012) The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest Ophthalmol Vis Sci 53:2921-2927
21. Luhmann UF, Lange CA, Robbie S, Munro PM, Cowing JA, Armer HE, Luong V, Carvalho LS, MacLaren RE, Fitzke FW et al (2012) Differential modulation of retinal degeneration by Ccl2 and Cx3cr1 chemokine signalling. PLoS One 7:e35551
22. Marmorstein AD, Finnemann SC, Bonilha VL, Rodriguez-Boulan E (1998) Morphogenesis of the retinal pigment epithelium: toward understanding retinal degenerative diseases. Ann N Y Acad Sci 857:1-12
23. Haverkamp S, Wässle H (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23
24. Sherry DM, Wang MM, Bates J, Frishman LJ (2003) Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465:480-498
25. Collaco A, Jakab R, Hegan P, Mooseker M, Ameen N (2010) α-AP-2 directs myosin VI-dependent endocytosis of cystic fibrosis transmembrane conductance regulator chloride channels in the intestine. J Biol Chem 285:17177-17187
26. Arango-Gonzalez B, Trifunovic D, Sahaboglu A, Kranz K, Michalakis S, Farinelli P, Koch S, Koch F, Cottet S, Janssen-Bienhold U et al (2014) Identification of a common non-apoptotic cell death mechanism in hereditary retinal degeneration. PLoS One 9:e112142
27. Ach T, Huisingh C, McGwin G Jr, Messinger JD, Zhang T, Bentley MJ, Gutierrez DB, Ablonczy Z, Smith RT, Sloan KR et al (2014) Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium. Invest Ophthalmol Vis Sci 55:4832-4841
28. Boretsky A, Khan F, Burnett G, Hammer DX, Ferguson RD, van Kuijk F, Motamedi M (2012) In vivo imaging of photoreceptor disruption associated with age-related macular degeneration: a pilot study. Lasers Surg Med 44:603-610
29. Curcio CA, Millican CL, Allen KA, Kalina RE (1993) Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci 34:3278-3296
30. McLeod DS, Grebe R, Bhutto I, Merges C, Baba T, Lutty GA (2009) Relationship between RPE and choriocapillaris in age-related macular degeneration. Invest Ophthalmol Vis Sci 50:4982-4991
31. Curcio CA, Johnson M (2012) Structure, function and pathology of Bruch's membrane. In: Hilton D (ed) Retina, 5th edn. Elsevier, London
32. Breton ME, Schueller AW, Montzka DP (1991) Electroretinogram b-wave implicit time and b/a wave ratio as a function of intensity in central retinal vein occlusion. Ophthalmology 98:1845-1853
33. Perlman I (1983) Relationship between the amplitudes of the b wave and the a wave as a useful index for evaluating the electroretinogram. Br J Ophthalmol 67:443-448
34. Fortune B, Bearse MA Jr, Cioffi GA, Johnson CA (2002) Selective loss of an oscillatory component from temporal retinal multifocal ERG responses in glaucoma. Invest Ophthalmol Vis Sci 43:2638-2647
35. Gupta N, Brown KE, Milam AH (2003) Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res 76:463-471
36. Wang M, Wang X, Zhao L, Ma W, Rodriguez IR, Fariss RN, Wong WT (2014) Macroglia-microglia interactions via TSPO signaling regulates microglial activation in the mouse retina. J Neurosci 34:3793-3806
37. Marmorstein AD, Marmorstein LY (2007) The challenge of modeling macular degeneration in mice. Trends Genet 23:225-231
38. Elizabeth Rakoczy P, Yu MJ, Nusinowitz S, Chang B, Heckenlively JR (2006) Mouse models of age-related macular degeneration. Exp Eye Res 82:741-752
39. Congdon N, O'Colmain B, Klaver CC, Klein R, Munoz B, Friedman DS, Kempen J, Taylor HR, Mitchell P (2004) Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol 122:477-485
40. Fine SL, Berger JW, Maguire MG, Ho AC (2000) Age-related macular degeneration. N Engl J Med 342:483-492
41. Sarks S, Cherepanoff S, Killingsworth M, Sarks J (2007) Relationship of Basal laminar deposit and membranous debris to the clinical presentation of early age-related macular degeneration. Invest Ophthalmol Vis Sci 48:968-977
42. Marmorstein LY, McLaughlin PJ, Peachey NS, Sasaki T, Marmorstein AD (2007) Formation and progression of sub-retinal pigment epithelium deposits in Efemp1 mutation knock-in mice: a model for the early pathogenic course of macular degeneration. Hum Mol Genet 16:2423-2432
43. Rusten TE, Stenmark H (2009) How do ESCRT proteins control autophagy? J Cell Sci 122:2179-2183
44. Buschini E, Piras A, Nuzzi R, Vercelli A (2011) Age related macular degeneration and drusen: neuroinflammation in the retina. Prog Neurobiol 95:14-25
45. Schuetz E, Thanos S (2004) Microglia-targeted pharmacotherapy in retinal neurodegenerative diseases. Curr Drug Targets 5:619-627
46. Ma W, Zhao L, Wong WT (2012) Microglia in the outer retina and their relevance to pathogenesis of age-related macular degeneration. Adv Exp Med Biol 723:37-42
47. Ma W, Zhao L, Fontainhas AM, Fariss RN, Wong WT (2009) Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD. PLoS One 4:e7945
48. Berson EL, Gouras P, Hoff M (1969) Temporal aspects of the electroretinogram. Arch Ophthalmol 81:207-214
49. Fuerst DJ, Tessler HH, Fishman GA, Yokoyama MM, Wyhinny GJ, Vygantas CM (1984) Birdshot retinochoroidopathy. Arch Ophthalmol 102:214-219
50. Ponjavic V, Andreasson S, Ehinger B (1994) Full-field electroretinograms in patients with central areolar choroidal dystrophy. Acta Ophthalmol (Copenh) 72:537-544
51. Kofoed PK, Munch IC, Holfort SK, Sillesen H, Jensen LP, Iversen HK, Larsen M (2013) Cone pathway function in relation to asymmetric carotid artery stenosis: correlation to blood pressure. Acta Ophthalmol 91:728-732
52. Rizzo JF 3rd, Berson EL, Lessell S (1986) Retinal and neurologic findings in the Laurence-Moon-Bardet-Biedl phenotype. Ophthalmology 93:1452-1456
53. Bresnick GH, Palta M (1987) Temporal aspects of the electroretinogram in diabetic retinopathy. Arch Ophthalmol 105:660-664
54. Tremblay F, Laroche RG, De Becker I (1995) The electroretinographic diagnosis of the incomplete form of congenital stationary night blindness. Vision Res 35:2383-2393
55. Larsson J, Bauer B, Andréasson S (2000) The 30-Hz flicker cone ERG for monitoring the early course of central retinal vein occlusion. Acta Ophthalmol Scand 78:187-190
56. Nakayama M, Nakayama A, van Lessen M, Yamamoto H, Hoffmann S, Drexler HC, Itoh N, Hirose T, Breier G, Vestweber D et al (2013) Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat Cell Biol 15:249-260
57. Göbel K, Erb C (2014) Neurological disorders and glaucoma - an overview. Klin Monbl Augenheilkd 231:130-135
58. Scheetz TE, Fingert JH, Wang K, Kuehn MH, Knudtson KL, Alward WL, Boldt HC, Russell SR, Folk JC, Casavant TL et al (2013) A genome-wide association study for primary open angle glaucoma and macular degeneration reveals novel Loci. PLoS One 8:e58657
59. Wachtmeister L (1998) Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res 17:485-521
60. Smith BJ, Wang X, Chauhan BC, Cote PD, Tremblay F (2014) Contribution of retinal ganglion cells to the mouse electroretinogram. Doc Ophthalmol 128:155-168
61. + channels. J Physiol 590:2501-2517
62. Haq W, Arango-Gonzalez B, Zrenner E, Euler T, Schubert T (2014) Synaptic remodeling generates synchronous oscillations in the degenerated outer mouse retina. Front Neural Circuits. doi: 10.3389/fncir.2014.00108
63. Luu CD, Szental JA, Lee SY, Lavanya R, Wong TY (2010) Correlation between retinal oscillatory potentials and retinal vascular caliber in type 2 diabetes. Invest Ophthalmol Vis Sci 51:482-486
64. Kergoat H, Lovasik JV (1990) The effects of altered retinal vascular perfusion pressure on the white flash scotopic ERG and oscillatory potentials in man. Electroencephalogr Clin Neurophysiol 75:306-322
65. Ahmed F, Brown KM, Stephan DA, Morrison JC, Johnson EC, Tomarev SI (2004) Microarray analysis of changes in mRNA levels in the rat retina after experimental elevation of intraocular pressure. Invest Ophthalmol Vis Sci 45:1247-1258
66. Steele MR, Inman DM, Calkins DJ, Horner PJ, Vetter ML (2006) Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest Ophthalmol Vis Sci 47:977-985
67. Wang X, Tay SS, Ng YK (2000) An immunohistochemical study of neuronal and glial cell reactions in retinae of rats with experimental glaucoma. Exp Brain Res 132:476-484
68. Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F (2005) Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol 169:285-295
69. Weisschuh N, Neumann D, Wolf C, Wissinger B, Gramer E (2005) Prevalence of myocilin and optineurin sequence variants in German normal tension glaucoma patients. Mol Vis 11:284-287
70. Rezaie T, Sarfarazi M (2005) Molecular cloning, genomic structure, and protein characterization of mouse optineurin. Genomics 85:131-138
71. Ahmed ZM, Morell RJ, Riazuddin S, Gropman A, Shaukat S, Ahmad MM, Mohiddin SA, Fananapazir L, Caruso RC, Husnain T et al (2003) Mutations of MYO6 are associated with recessive deafness, DFNB37. Am J Hum Genet 72:1315-1322
72. Avraham KB, Hasson T, Sobe T, Balsara B, Testa JR, Skvorak AB, Morton CC, Copeland NG, Jenkins NA (1997) Characterization of unconventional MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice. Hum Mol Genet 6:1225-1231
73. Melchionda S, Ahituv N, Bisceglia L, Sobe T, Glaser F, Rabionet R, Arbones ML, Notarangelo A, Di Iorio E, Carella M et al (2001) MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice, is mutated in autosomal dominant nonsyndromic hearing loss. Am J Hum Genet 69:635-640