Unconventional myosins and the genetics of hearing loss

American Journal of Medical Genetics - Seminars in Medical Genetics

Volumn 89, Issue 3, 1999, Pages 147-157

  Friedman, Thomas B ^a   Sellers, James R ^b   Avraham, Karen B ^b  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b NONE

Author keywords

Deafness; Hearing loss; Myosin VI; Myosin VIIA; Myosin XV; Unconventional myosin

Indexed keywords

CYTOSKELETON PROTEIN; MYOSIN;

AUDITORY SYSTEM; CHROMOSOME 17P; CHROMOSOME 6Q; CONGENITAL DEAFNESS; ENDOCYTOSIS; GENE MUTATION; HAIR CELL; HEARING LOSS; INNER EAR; PRIORITY JOURNAL; REVIEW; STEREOCILIUM; USHER SYNDROME;

ANIMALS; DEAFNESS; HUMANS; MICE; MUTATION; MYOSINS;

EID: 0033600948     PISSN: 01487299     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-8628(19990924)89:3<147::AID-AJMG5>3.0.CO;2-6     Document Type: Review

References (80)

1. Adato A, Weil D, Kalinski H, Pel-Or Y, Ayadi H, Petit C, Korostishevsky M, Bonné-Tamir B. 1997. Mutation profile of all 49 exons of the human myosin VIIA gene, and haplotype analysis, in Usher 1B families from diverse origins. Am J Hum Genet 61: 813-821.
2. 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.
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 the structural integrity of inner ear hair cells. Nature Genet 11:369-375.
4. Baker JP, Titus MA, 1997. A family of unconventional myosins from the nematode Cacnorhabditis elegans. J Mol Biol 272:523-535.
5. Baker JP, Titus MA. 1998. Myosins: matching functions with motors. Curr Opin Cell Biol 10:80-86.
6. Bedell MA, Jenkins NA, Copeland NG. 1996. Good genes in bad neighborhoods. Nature Genet 12:229-232.
7. Boughman JA, Vernon M, Shaver KA. 1983. Usher syndrome: definition and estimate of prevalence from two high-risk populations. J Chron Dis 36:595-603.
8. Buss F, Kendrick-Jones J, Lionne C, Knight AE, Cote GP, Luzio JP. 1998. The localization of myosin VI at the Golgi complex and leading edge of fibroblasts and its phosphorylation and recruitment into membrane ruffles of A431 cells after growth factor stimulation. J Cell Biol 143:1535-1545.
9. Chaib H, Kaplan J, Gerber S, Vincent C, Ayadi H, Slim R, Munnich A, Weissenbach J, Petit C. 1997. A newly identified locus for Usher syndrome type I, USH1E, maps to chromosome 21q21. Hum Mol Genet 6: 27-31.
10. Chaussepied P. Morales MF. 1988. Modifying preselected sites on proteins: the stretch of residues 633-642 of the myosin heavy chain in part of the actin-binding site. Proc Natl Acad Sci USA 85:7471-7475.
11. Chishti AH, Kim Ac, Marfatia SM, Lutchman M, Hanspal M, Jindal H, Liu SC, Low PS, Rouleau GA, Mohandas N, Chasis JA, Conboy JG, Gascard P, Takakuwa Y, Huang SC, Benz EJ Jr., Bretscher A, Fehon RG, Gusella JF, Ramesh V, Solomon F, Marchesi VT, Tsukita S, Hoover KB. 1998. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci 23:281-282.
12. Cope MJT, Whisstock J, Rayment I, Kendrick-Jones J. 1996. Conservation within the myosin motor domain: implications for structure and function. Structure 4:969-987.
13. Cuevas JM, Espinós C, Millán JM, Sánchez F, Trujillo MJ, Garcia-Sandoval B, Ayuso C, Nájera C, Beneyto M. 1998. Detection of a novel Cys628STOP mutation of the myosin VIIA gene in Usher syndrome type Ib. Mol Cell Probes 12:417-420.
14. Deol MS, Green MS. 1966. Snell's waltzer, a new mutation affecting behaviour and the inner ear of the mouse. Genet Res 8:339-345.
15. DiLeone RJ, Russell LB, Kingsley DM. 1998. An extensive 3′ regulatory region controls expression of Bmp5 in specific anatomical structures of the mouse embryo. Genetics 148:401-408.
16. Dominguez R, Freyzon Y, Trybus KM, Cohen C. 1998. Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94:559-571.
17. el-Amraoui A, Sahly I, Picaud S, Sahel J, Abitbol M, Petit G. 1996. Human Usher 1B/mouse shaker-1: the retinal phenotype discrepancy explained by the presence/absence of myosin VIIA in the photoreceptor cells. Hum Mol Genet 5:1171-1178.
18. Espinós C, Millán JM, Sánchez F, Beneyton M, Nájera C. 1998. Ala397Asp mutation of myosin VIIA gene segregating in a Spanish family with type Ib Usher Syndrome. Hum Genet 102:691-694.
19. Evans KL, Fantes J, Simpson C, Arveiler B, Muir W, Fletcher J, van Heyningen V, Steel KP, Brown KA, Brown SDM, St. Clair D, Porteous DJ. 1993. Human olfactory marker protein maps close to tyrosinase and is a candidate gene for Usher syndrome type I. Hum Mol Genet 2:115-118.
20. Fisher AJ, Smith CA, Thoden JB, Smith R, Sutoh K, Holden HM, Rayment I. 1995. X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.A1F4. Biochemistry 34:8960-8972.
21. Friedman TB, Liang Y, Weber JL, Hinnant JT, Barber TD, Winata S, Arhya IN, Asher JH, Jr. 1995. A gene for congenital, recessive deafness DFNB3 maps to the pericentromeric region of chromosome 17. Nature Genet 9:86-91.
22. Gabriel HD, Jung D, Butzler G, Temme A, Traub O, Winterhager E, Willecke K. 1998. Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J Cell Biol 140:1453-1461.
23. Gibson F, Walsh J, Mburu P, Varela A, Brown KA, Antonio M, Beisel KW, Steel KP, Brown SD. 1995. A type VII myosin encoded by the mouse deafness gene shaker-1. Nature 374:62-64.
24. Gillespie PG, Wagner MC, Hudspeth AJ. 1993. Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron 11:581-594.
25. Griffith AJ, Friedman TB. 1999. Making sense out of sound. Nature Genet 21:347-349.
26. Guilford P, Ben Arab S, Blanchard S, Levilliers J, Weissenbach J, Belkahia A, Petit C. 1994. A non-syndrome form of neurosensory, recessive deafness maps to the pericentromeric region of chromosome 13q. Nature Genet 6:24-28.
27. Hasson T, Gillespie PG, Garcia JA, MacDonald RB, Zhao Y, Yee AG, Mooseker MS, Corey DP. 1997. Unconventional myosins in inner-ear sensory epithelia. J Cell Biol 137:1287-1307.
28. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. 1995. Expression in cochlea and retina of myosin-VIIa, the gene defective in Usher syndrome type 1B. Proc Natl Acad Sci USA 92:9815-9819.
29. Hasson T, Mooseker MS. 1994. Porcine myosin-VI: characterization of a new mammalian unconventional myosin. J Cell Biol 127: 425-440.
30. Hasson T, Walsh J, Cable J, Mooseker MS, Brown SD, Steel KP. 1997. Effects of shaker-1 mutations on myosin-VIIa protein and mRNA expression. Cell Motil Cytoskeleton 37:127-138.
31. Holmes KC. 1997. The swinging lever-arm hypothesis of muscle contraction. Curr Biol 7:R112-118.
32. Houdusse A, Kalaboris VN, Himmel D, Szent-Györgyi AG, Cohen C. 1999. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: A novel conformation of the myosin head. Cell 97:459-470.
33. Huang JD, Brady ST, Richards BW, Stenolen D, Resau JH, Copeland NG, Jenkins NA. 1999. Direct interaction of microtubule- and actin-based transport motors. Nature 397:267-270.
34. Hudspeth AJ, Gillespie PG. 1994. Pulling springs to tune transduction: adaptation by hair cells. Neuron 12:1-9.
35. Janecke AR, Meins M, Sadeghi M, Grundmann K, Apfelstedt-Sylla E, Zrenner E, Rosenberg T, Gal A. 1999. Twelve novel myosin VIIA mutations in 34 patients with Usher syndrome type I: confirmation of genetic heterogeneity. Hum Mutat 13:133-140.
36. Kaplan J, Gerber S, Bonneau D, Rozer JM, Delrieu O, Briard ML, Dollfus H, Ghazi I, Dufier IL, Frezal J. 1992. A gene for Usher syndrome type 1 (USH1A) maps to chromosome 14q. Genomics 14:979-987.
37. Keats BJ, Nouri N, Pelias MZ, Deininger PL, Litt M. 1994. Tightly linked flanking microsatellite markers for the Usher syndrome type 1 locus on the short arm of chromosome 11. Am J Hum Genet 54:681-686.
38. Kellerman KA, Miller KG. 1992. An unconventional myosin hevy chain gene from Drosophila melanogaster. J Cell Biol 119:823-834.
39. Kelley PM, Weston MD, Chen ZY, Orten DJ, Hasson T, Overbeck LD, Pinnt J, Talmadge Cr, Ing P, Mooseker MS, Corey D, Sumegi J, Kimberling WJ. 1997. The genomic structure of the gene defective in Usher syndrome type Ib (MYO7A). Genomics 40: 73-79.
40. Kimberling WJ, Moller C. 1995. Clinical and molecular genetics of Usher syndrome. J Am Acad Audiol 6:63-72.
41. Kimberling WJ, Moller CG, Davenport S, Priluck IA, Beighton PH, Greenberg J, Reardon W. Weston MD, Kenyon JB, Grunkemeyer JA. 1992. Linkage of Usher syndrome type I gene (USH1B) to the long arm of chromosome 11. Genoimcs 14:988-994.
42. Kingsley DM, Bland AE, Grubber JM, Marker PC, Russell LB, Copeland NG, Jenkins NA. 1992. The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGFβ superfamily. Cell 71:399-410.
43. Kolega J. 1998. Cytoplasmic dynamics of myosin IIA and IIB: spatial "sorting" of isofonns in locomoting cells. J Cell Sci 111:2085-2095.
44. Lantz VA, Miller KG. 1998. A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J Cell Biol 140:897-910.
45. Lévy G, Levi-Acobas F, Blanchard S, Gerber S, Larget-Piet D, Chenal V, Liu XZ, Newton V, Steel KP, Brown SD, Munnich A, Kaplan J, Petit C, Weil D. 1997. Myosin VIIA gene: heterogeneity of the mutations responsible for Usher syndrome type 1B. Hum Mol Genet 6:111-116.
46. Liang Y, Wang A, Probst FJ, Arhya IN, Barber TD, Chen KS, Deshmukh D, Dolan DF, Hinnant JT, Carter LF, Jain PK, Lalwani AK, Li XC, Lupski JR, Moeljopawiro S, Morell R, Negrini C, Wilcox ER, Winata S, Camper SA, Friedman TB. 1998. Genetic mapping refines DFNB3 to 17p11.2, suggests multiple alleles of DFNB3, and supports homology to the mouse model shaker-2. Am J Hum Genet 62:9114-915.
47. Liang Y, Wang A, Belyamseva IA, Anderson DW, Probst FJ, Barber TD, Miller W, Touchman J, Jin L, Sullivan SL, Sellers JR, Camper SA, Lloyd RV, Kachar B, Friedman TB, Fridell RA. 1999. Characterization of the human and mouse unconventional myosin XV genes responsible for hereditary deafness and Shaker 2. Genomics 61:243-258.
48. Liu XZ, Hope C, Walsh J, Newton V, Ke XM, Liang CY, Xu LR, Zhou JM, Trump D, Steel KP, Bundey S, Brown SD. 1998a. Mutations in the myosin VIIA gene cause a wide phenotypic spectrum, including atypical Usher syndrome. Am J Hum Genet 63: 909-912.
49. Lui X, Ondek B, Williams DS. 1998b. Mutant myosin VIIa causes defective melanosome distribution in the RPE of shaker-1 mice. Nature Genet 19:117-118.
50. Liu XZ, Newton VE, Steel KP, Brown SD. 1997a. Identification of a new mutation of the myosin VII head region in Usher syndrome type I. Hum Mutat 10:168-170.
51. Lui XZ, Walsh J, Mburu P, Kendrick-Jones J, Cope MJ, Steel KP, Brown SD. 1997b. Mutations in the mosin VIIA gene cause non-syndromic recessive deafness. Nature Genet 16:188-190.
52. 2+-ATPase activity ot Acanthamvoeba myosin I. J Biol Chem 252:8329-8332.
53. Mburu P, Liu XZ, Walsh J, Saw D Jr., Cope MJ, Gibson F, Kendrick-Jones J, Steel KP, Brown SD. 1997. Mutation analysis of the mouse myosin VIIA deafness gene. Genes Funct 1:191-203.
54. Mermall V, McNally JG, Miller KG. 1994. Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embriyos. Nature 369:560-562
55. Mermall V, Miller KG. 1995. The 95F unconventional myosin is required for proper organization of the Drosophila syncytial blastoderm. J Cell Biol 129:1575-1588.
56. Mermall V, Post PL, Mooseker MS. 1998. Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279:527-533.
57. Patterson B, Spudich JA. 1996. Cold-sensitive mutations of Dictyostelium myosin heavy chain highlight functional domains of the myosin motor. Genetics 143:801-810.
58. Probst FJ, Fridell RA, Raphael Y, Saunders TL, Wang A, Liang Y, Morell RJ, Touchman JW, Lyons RH, Noben-Trauth K, Friedman TB, Camper SA. 1998. Correction of deafness in shaker-2 mice by an unconventional myosin in a BAC transgene. Science 280:1444-1447.
59. Rayment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, Holmes KC, Milligan RA. 1993. Structure of the actin-myosin complex and its implications for muscle contraction. Science 261:58-65.
60. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM. 1993. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261:50-58.
61. Russell LB. 1971. Definition of functional units in a small chromosomal segment of the mouse and its use in interpreting the nature of radiation-induced mutations. Mutat Res 11:107-123.
62. Sankila EM, Pakarinen L, Kaariainen H, Aittomaki K, Karjalainen S, Sistonen P, de la Chapelle A. 1995. Assignment of an Usher syndrome type III (USH3) gene to chromosome 3q. Hum Mol Genet 4:93-98.
63. Self T, Mahony M, Fleming J, Walsh J, Brown SD, Steel KP. 1998, Shaker-1 mutations reveal roles for myosin VIIA in both development and function of cochlear hair cells. Development 125:557-566.
64. 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.
65. Sellers JR. 1999. Protein profiles: myosin. London: Oxford University Press.
66. Smith RJ, Berlin CI, Hejtmancik JF, Keats BJ, Kimberling WJ, Lewis RA, Moller CG, Pelias MZ, Tranebjaerg L. 1994. Clinical diagnosis of the Usher syndromes. Usher Syndrome Consortium. Am J Med Genet 50:32-38.
67. Sole CF, Durfler RH, Duyk GM, Corey DP. 1995. Molecular cloning of myosins from the bulltrog saccnlar macula: a candidate tor the hair tell adaptation motor. Auditory Neurosci 1:63-75.
68. Spudich JA. 1994 How molecular motors work. Nature 372:515-518.
69. Steel KP, Brown SDM. 1994. Genes and deafness. Trends Genet 10:428-435.
70. Tamagawa Y, Kitamura K, Ishida T, Ishikawa K, Tanaka H, Tsuji S, Nishizawa M. 1996. A gene for a dominant form of non-syndromic sensorineural deafness (DFNA11) maps within the region containing the DFNB2 recessive deafness gene. Hum Mol Genet 5:849-852.
71. Titus MA. 1998. Coming to grips with a multitude ot myosins. Trends Cell Biol 8:171-172.
72. Van Camp G, Smith RJH, 1999. http://dnalab-www.uia.ac.be/dnalab/hhh.
73. Vernon M 1969. Usher syndrome - deafness and progressive blindness. Clinical cases, prevention, theory and literature survey. J Chron Dis 22:133-151.
74. Wang A, Liang Y, Fridell RA, Probst FJ. Wilcox EK, Touchman JW, Morton CC, Morell RJ, Noben-Trauth K, Camper SA, Friedman TB. 1998. Association of unconventional myosin MYO15 mutations with human nonsyndromic deafness DFNB3, Science 280:1447-1451.
75. Wayne S, Der Kaloustian VM, Schloss M, Polomeno K, Scott DA, Hejtmancik JF. Sheffield VC, Smith RJ. 1996, Localization of the Usher syndrome type IB gene (Ush ID) to chromosome 10. Hum Mol Genet 5: 1689-1692.
76. Wayne S, Lowry RB, McLeod DR, Knaus R, Farr C, Smith RJH. 1997. Localization of the Usher syndrome type IF (Ush1F) to chromosome 10. Am J Hum Genet 61:A300.
77. Weil D, Blanchard S, Kaplan J, Guilford P. Gibson F, Walsh J, Mburu P, Varela A, Levilliers J, Westou MD. 1995. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374:60-61.
78. Weil D, Kussel P, Blanchard S, Levy C. LeviAcobas F, Drira M, Ayadi H, Petit C 1997. The autosomal recessive isolated deafness, DFNB2, and the Usher 1B syndrome are allelic defects of the myosin-VIIA gene. Nature Genet 16:191-193.
79. Wells AL, Lin AW, Chen L-Q, Safer D, Cain SM, Hasson T, Carragher BO. Milligan KA, Sweeney HL. 1999. Myosin VI is an actin-based motor that moves backwards. Nature 401:502-508.
80. Weston MD, Kelley PM, Overbeck LD, Wagenaar M, Orten DJ, Hasson T, Chen ZY, Corey D, Mooseker M. Sumegi J. Cremers C, Moller C, Jacobson SG, Gorin MB, Kimberling WJ, 1996. Myosin VIIA mutation screening in 1H9 Usher syndrome type 1 patients. Am J Hum Genet 59:1074-1083.