Myosin VI: Cellular functions and motor properties

Annual Review of Cell and Developmental Biology

Volumn 20, Issue , 2004, Pages 649-676

  Buss, Folma ^a   Spudich, Giulietta ^b   Kendrick Jones, John ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Actin; Cell motility; Endocytosis; Golgi; Motor protein

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; DIMER; MONOMER; MYOSIN; MYOSIN VI; PROTEIN D CLIP 190; PROTEIN DISABLED 2; PROTEIN GIPC; PROTEIN SAP97; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CELL ENERGY; CELL MIGRATION; CELL MOTION; CELL RESPIRATION; CELL VACUOLE; COMPLEX FORMATION; DIMERIZATION; DROSOPHILA; ENDOCYTOSIS; GOLGI COMPLEX; HEARING IMPAIRMENT; HUMAN; HYDROLYSIS; INTRACELLULAR TRANSPORT; MAMMAL CELL; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; DEAFNESS; DROSOPHILA; MAMMALS; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MYOSIN HEAVY CHAINS; PROTEIN STRUCTURE, TERTIARY;

MAMMALIA;

EID: 8444246367     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.20.012103.094243     Document Type: Review

References (125)

1. Ahmed ZM, Morell RJ, Riazuddin S, Gropman A, Shaukat S, et al. 2003. Mutations of MYO6 are associated with recessive deafness, DFNB37. Am. J. Hum. Genet. 72:1315-22
2. Aschenbrenner L, Lee T, Hasson T. 2003. Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol. Biol. Cell 14:2728-43
3. Avraham KB, Hasson T, Steel KP, Kingsley DM, Russell LB, et al. 1995. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat. Genet. 11:369-75
4. Baker JP, Titus MA. 1997. A family of unconventional myosins from the nematode Caenorhabditis elegans. J. Mol. Biol. 272:523-35
5. Bernent WM, Mooseker MS. 1995. TEDS rule: a molecular rationale for differential regulation of myosins by phosphorylation of the heavy chain head. Cell Motil. Cytoskelet. 31:87-92
6. Bennett EM, Chen CY, Engqvist-Goldstein AE, Drubin DG, Brodsky FM. 2001. Clathrin hub expression dissociates the actin-binding protein Hip1R from coated pits and disrupts their alignment with the actin cytoskeleton. Traffic 2:851-58
7. Berg JS, Powell BC, Cheney RE. 2001. A millennial myosin census. Mol. Biol. Cell 12:780-94
8. Biemesderfer D, Mentone SA, Mooseker M, Hasson T. 2002. Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules. Am. J. Physiol. Renal Physiol. 282:F785-94
9. Borisy GG, Svitkina TM. 2000. Actin machinery: pushing the envelope. Curr. Opin. Cell Biol. 12:104-12
10. Breckler J, Au K, Cheng J, Hasson T, Burnside B. 2000. Novel myosin VI isoform is abundantly expressed in retina. Exp. Eye Res. 70:121-34
11. Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE. 2001. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17:517-68
12. Brown SS. 1997. Myosins in yeast. Curr. Opin. Cell Biol. 9:44-48
13. Brown SS. 1999. Cooperation between microtubule- and actin-based motor proteins. Annu. Rev. Cell Dev. Biol. 15:63-80
14. Brzeska H, Knaus UG, Wang ZY, Bokoch GM, Korn ED. 1997. p21-activated kinase has substrate specificity similar to Acanthamoeba myosin I heavy chain kinase and activates Acanthamoeba myosin I. Proc. Natl. Acad. Sci. USA 94:1092-95
15. Bunn RC, Jensen MA, Reed BC. 1999. Protein interactions with the glucose transporter binding protein GLUT1CBP that provide a link between GLUT1 and the cytoskeleton. Mol. Biol. Cell 10:819-32
16. Buss F, Arden SD, Lindsay M, Luzio JP, Kendrick-Jones J. 2001a. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J. 20:3676-84
17. Buss F, Kendrick-Jones J, Lionne C, Knight AE, Cote GP, Paul Luzio J. 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. 143:1535-45
18. Buss F, Luzio JP, Kendrick-Jones J. 2001b. Myosin VI, a new force in clathrin mediated endocytosis. FEBS Lett. 508:295-99
19. Buss F, Luzio JP, Kendrick-Jones J. 2002. Myosin VI, an actin motor for membrane traffic and cell migration. Traffic 3:851-58
20. Christensen EI, Birn H, Verroust P, Moestrup SK. 1998. Membrane receptors for endocytosis in the renal proximal tubule. Int. Rev. Cytol. 180:237-84
21. Craig R, Smith R, Kendrick-Jones J. 1983. Light-chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules. Nature 302:436-39
22. Cramer LP. 1999. Organization and polarity of actin filament networks in cells: implications for the mechanism of myosin-based cell motility. Biochem. Soc. Symp. 65:173-205
23. De La Cruz EM, Ostap EM, Sweeney HL. 2001. Kinetic mechanism and regulation of myosin VI. J. Biol. Chem. 276:32373-81
24. De Vries L, Lou X, Zhao G, Zheng B, Farquhar MG. 1998. GIPC, a PDZ domain containing protein, interacts specifically with the C terminus of RGS-GAIP. Proc. Natl. Acad. Sci. USA 95:12340-45
25. Defacque H, Egeberg M, Habermann A, Diakonova M, Roy C, et al. 2000. Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO J. 19:199-212
26. DeMali KA, Barlow CA, Burridge K. 2002. Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol. 159:881-91
27. DeMali KA, Burridge K. 2003. Coupling membrane protrusion and cell adhesion. J. Cell Sci. 116:2389-97
28. Deng W, Leaper K, Bownes M. 1999. A targeted gene silencing technique shows that Drosophila myosin VI is required for egg chamber and imaginai disc morphogenesis. J. Cell Sci. 112:3677-90
29. Deol M, Green M. 1966. Snell's Waltzer, a new mutation affecting behaviour and the inner ear of the mouse. Genet. Res. 8:339-45
30. Engqvist-Goldstein AE, Drubin DG. 2003. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19:287-332
31. Fisher AJ, Smith CA, Thoden JB, Smith R, Sutoh K, et al. 1995. X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AlF4. Biochemistry 34:8960-72
32. Friedman TB, Sellers JR, Avraham KB. 1999. Unconventional myosins and the genetics of hearing loss. Am. J. Med. Genet. 89:147-57
33. Fujimoto LM, Roth R, Heuser JE, Schmid SL. 2000. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1:161-71
34. Fujita A, Kurachi Y. 2000. SAP family proteins. Biochem. Biophys. Res. Commun. 269:1-6
35. Fulop V, Colitti CV, Genest D, Berkowitz RS, Yiu GK, et al. 1998. DOC-2/hDab2, a candidate tumor suppressor gene involved in the development of gestational trophoblastic diseases. Oncogene 17:419-24
36. Gaidarov I, Santini F, Warren RA, Keen JH. 1999. Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1:1-7
37. Gao Y, Li M, Chen W, Simons M. 2000. Synectin, syndecan-4 cytoplasmic domain binding PDZ protein, inhibits cell migration. J. Cell Physiol. 184:373-79
38. Geeves MA, Holmes KC. 1999. Structural mechanism of muscle contraction. Annu. Rev. Biochem. 68:687-728
39. Geisbrecht ER, Montell DJ. 2002. Myosin VI is required for E-cadherin-mediated border cell migration. Nat. Cell Biol. 4:616-20
40. Geli MI, Riezman H. 1998. Endocytic internalization in yeast and animal cells: similar and different. J. Cell Sci. 111:1031-37
41. Gonczy P. 2002. Mechanisms of spindle positioning: focus on flies and worms. Trends Cell Biol. 12:332-39
42. Goodson HV, Skube SB, Stalder R, Valetti C, Kreis TE, et al. 2003. CLIP-170 interacts with dynactin complex and the APC-binding protein EB1 by different mechanisms. Cell Motil. Cytoskelet. 55:156-73
43. Gotthardt M, Trommsdorff M, Nevitt MF, Shelton J, Richardson JA, et al. 2000. Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem. 275:25616-24
44. Gottlieb TA, Ivanov IE, Adesnik M, Sabatini DD. 1993. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120:695-710
45. Griffiths G, Simons K. 1986. The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234:438-43
46. Hall A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-14
47. Hasson T, Gillespie PG, Garcia JA, MacDonald RB, Zhao Y, et al. 1997. Unconventional myosins in inner-ear sensory epithelia. J. Cell Biol. 137:1287-307
48. Hasson T, Mooseker MS. 1994. Porcine myosin-VI: characterization of a new mammalian unconventional myosin. J. Cell Biol. 127:425-40
49. Heintzelman MB, Hasson T, Mooseker MS. 1994. Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J. Cell Sci. 107:3535-43
50. Hicks JL, Deng WM, Rogat AD, Miller KG, Bownes M. 1999. Class VI unconventional myosin is required for spermatogenesis in Drosophila. Mol. Biol. Cell 10:4341-53
51. Hirakawa T, Galet C, Kishi M, Ascoli M. 2003. GIPC binds to the human lutropin receptor (LHR) through an unusual PDZ domain binding motif and it regulates the sorting of the internalized human choriogonadotropin (hCG) and the density of cell surface LHR. J. Biol. Chem. 278:49348-57
52. Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED, et al. 1998. Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143:1485-503
53. Hocevar BA, Mou F, Rennolds JL, Morris SM, Cooper JA, Howe PH. 2003. Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J. 22:3084-94
54. Hocevar BA, Smine A, Xu XX, Howe PH. 2001. The adaptor molecule Disabled-2 links the transforming growth factor beta receptors to the Smad pathway. EMBO J. 20:2789-801
55. Hodge T, Cope MJ. 2000. A myosin family tree. J. Cell Sci. 113:3353-54
56. Holmes KC. 1997. The swinging lever-arm hypothesis of muscle contraction. Curr. Biol. 7:R112-18
57. Houdusse A, Kalabokis VN, Himmel D, Szent-Gyorgyi AG, Cohen C. 1999. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97:459-70
58. Hu LA, Chen W, Martin NP, Whalen EJ, Premont RT, Lefkowitz RJ. 2003. GIPC interacts with the beta1-adrenergic receptor and regulates beta1-adrenergic receptor-mediated ERK activation. J. Biol. Chem. 278:26295-301
59. Inoue A, Sato O, Homma K, Ikebe M. 2002. DOC-2/DAB2 is the binding partner of myosin VI. Biochem. Biophys. Res. Commun. 292:300-7
60. Inoue A, Saito J, Ikebe R, Ikebe M. 2002. Myosin IXb is a single-headed minus-end-directed processive motor. Nat. Cell Biol. 4:302-6
61. Jackman MR, Shurety W, Ellis JA, Luzio JP. 1994. Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J. Cell Sci. 107:2547-56
62. Kelleher JF, Mandell MA, Moulder G, Hill KL, L'Hernault SW, et al. 2000. Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis. Curr. Biol. 10:1489-96
63. Kellerman KA, Miller KG. 1992. An unconventional myosin heavy chain gene from Drosophila melanogaster. J. Cell Biol. 119:823-34
64. Ladinsky MS, Mastronarde DN, McIntosh JR, Howell KE, Staehelin LA. 1999. Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144:1135-49
65. Langford GM. 1995. Actin- and microtubule-dependent organelle motors: interrelationships between the two motility systems. Curr. Opin. Cell Biol. 7:82-88
66. 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
67. Leonard AS, Davare MA, Home MC, Garner CC, Hell JW. 1998. SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem. 273:19518-24
68. Lippincott-Schwartz J. 1998. Cytoskeletal proteins and Golgi dynamics. Curr. Opin. Cell Biol. 10:52-59
69. Lister I, Schmitz S, Walker M, Trinick J, Buss F, et al. 2004. A monomeric myosin VI with a large working stroke. EMBO J. 23:1729-38
70. Liu TF, Kandala G, Setaluri V. 2001. PDZ domain protein GIPC interacts with the cytoplasmic tail of melanosomal membrane protein gp75 (tyrosinase-related protein-1). J. Biol. Chem. 276:35768-77
71. Lou X, McQuistan T, Orlando RA, Farquhar MG. 2002. GAIP, GIPC and Galphai3 are concentrated in endocytic compartments of proximal tubule cells: putative role in regulating megalin's function. J. Am. Soc. Nephrol. 13:918-27
72. Melchionda S, Ahituv N, Bisceglia L, Sobe T, Glaser F, 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. 69:635-40
73. Mermall V, McNally JG, Miller KG. 1994. Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embryos. Nature 369:560-62
74. Mermall V, Miller KG. 1995. The 95F unconventional myosin is required for proper organization of the Drosophila syncytial blastoderm. J. Cell Biol. 129:1575-88
75. Mishra SK, Keyel PA, Hawryluk MJ, Agostinelli NR, Watkins SC, Traub LM. 2002. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21:4915-26
76. Mitchison TJ, Cramer LP. 1996. Actin-based cell motility and cell locomotion. Cell 84:371-79
77. Mok H, Shin H, Kim S, Lee JR, Yoon J, Kim E. 2002. Association of the kinesin superfamily motor protein KIFlBalpha with postsynaptic density-95 (PSD-95), synapse-associated protein-97, and synaptic scaffolding molecule PSD-95/discs large/zona occludens-1 proteins. J. Neurosci. 22:5253-58
78. Morris CA, Wells AL, Yang Z, Chen LQ, Baldacchino CV, Sweeney HL. 2003. Calcium functionally uncouples the heads of myosin VI. J. Biol. Chem. 278:23324-30
79. Morris SM, Arden SD, Roberts RC, Kendrick-Jones J, Cooper JA, et al. 2002a. Myosin VI binds to and localizes with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3:331-41
80. Morris SM, Cooper JA. 2001. Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2:111-23
81. Morris SM, Tallquist MD, Rock CO, Cooper JA. 2002b. Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J. 21:1555-64
82. Nabi IR. 1999. The polarization of the motile cell. J. Cell Sci. 112:1803-11
83. Nishikawa S, Homma K, Komori Y, Iwaki M, Wazawa T, et al. 2002. Class VI myosin moves processively along actin filaments backward with large steps. Biochem. Biophys. Res. Commun. 290:311-17
84. O'Connell CB, Mooseker MS. 2003. Native Myosin-IXb is a plus-, not a minus-end-directed motor. Nat. Cell Biol. 5:171-72
85. Petritsch C, Tavosanis G, Turck CW, Jan LY, Jan YN. 2003. The Drosophila myosin VI Jaguar is required for basal protein targeting and correct spindle orientation in mitotic neuroblasts. Dev. Cell 4:273-81
86. Pierre P, Scheel J, Rickard JE, Kreis TE. 1992. CLIP-170 links endocytic vesicles to microtubules. Cell 70:887-900
87. Purcell TJ, Morris C, Spudich JA, Sweeney HL. 2002. Role of the lever arm in the processive stepping of myosin V. Proc. Natl. Acad. Sci. USA 99:14159-64
88. Qualmann B, Kessels MM. 2002. Endocytosis and the cytoskeleton. Int. Rev. Cytol. 220:93-144
89. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, et al. 1993. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261:50-58
90. Reck-Peterson SL, Provance DW Jr, Mooseker MS, Mercer JA. 2000. Class V myosins. Biochim. Biophys. Acta 1496:36-51
91. Redowicz MJ. 1999. Myosins and deafness. J. Muscle Res. Cell Motil. 20:241-48
92. Redowicz MJ. 2002. Myosins and pathology: genetics and biology. Acta Biochim. Pol. 49:789-804
93. Reuver SM, Garner CC. 1998. E-cadherin mediated cell adhesion recruits SAP97 into the cortical cytoskeleton. J. Cell Sci. 111:1071-80
94. Rock RS, Rice SE, Wells AL, Purcell TJ, Spudich JA, Sweeney HL. 2001. Myosin VI is a processive motor with a large step size. Proc. Natl. Acad. Sci. USA 98:13655-59
95. Rogalski AA, Singer SJ. 1984. Associations of elements of the Golgi apparatus with microtubules. J. Cell Biol. 99:1092-100
96. Rogat AD, Miller KG. 2002. A role for myosin VI in actin dynamics at sites of membrane remodeling during Drosophila spermatogenesis. J. Cell Sci. 115:4855-65
97. Rosenbauer F, Kallies A, Scheller M, Knobeloch KP, Rock CO, et al. 2002. Disabled-2 is transcriptionally regulated by ICSBP and augments macrophage spreading and adhesion. EMBO J. 21:211-20
98. Sans N, Racca C, Petralia RS, Wang YX, McCallum J, Wenthold RJ. 2001. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J. Neurosci. 21:7506-16
99. Schafer DA. 2002. Coupling actin dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14:76-81
100. Schwahn DJ, Medina D. 1998. p96, a MAPK-related protein, is consistently downregulated during mouse mammary carcinogenesis. Oncogene 17:1173-78
101. 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. 214:331-41
102. Sellers JR. 2000. Myosins: a diverse superfamily. Biochim. Biophys. Acta 1496:3-22
103. Sells MA, Boyd JT, Chernoff J. 1999. p21-activated kinase 1 (Pak1) regulates cell motility in mammalian fibroblasts. J. Cell Biol. 145:837-49
104. Shurety W, Luzio JP. 1995. Differential modulation of apical and basolateral endocytosis in Caco-2 cells. Biochem. Soc. Trans. 23:184S
105. Smith CA, Rayment I. 1996. Active site comparisons highlight structural similarities between myosin and other P-loop proteins. Biophys. J. 70:1590-602
106. Soldati T, Geissler H, Schwarz EC. 1999. How many is enough? Exploring the myosin repertoire in the model eukaryote Dictyostelium discoideum. Cell Biochem. Biophys. 30:389-411
107. Tanaka H, Homma K, Iwane AH, Katayama E, Ikebe R, et al. 2002. The motor domain determines the large step of myosin-V. Nature 415:192-95
108. Thyberg J, Moskalewski S. 1985. Microtubules and the organization of the Golgi complex. Exp. Cell Res. 159:1-16
109. Tomishige M, Klopfenstein DR, Vale RD. 2002. Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 297:2263-67
110. Traub LM. 2003. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163:203-8
111. Tzolovsky G, Millo H, Pathirana S, Wood T, Bownes M. 2002. Identification and phylogenetic analysis of Drosophila melanogaster myosins. Mol. Biol. Evol. 19:1041-52
112. Uyeda TQ, Abramson PD, Spudich JA. 1996. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl. Acad. Sci. USA 93:4459-64
113. Valderrama F, Babia T, Ayala I, Kok JW, Renau-Piqueras J, Egea G. 1998. Actin microfilaments are essential for the cytological positioning and morphology of the Golgi complex. Eur. J. Cell Biol. 76:9-17
114. Valderrama F, Duran JM, Babia T, Barth H, Renau-Piqueras J, Egea G. 2001. Actin microfilaments facilitate the retrograde transport from the Golgi complex to the endoplasmic reticulum in mammalian cells. Traffic 2:717-26
115. Vale RD. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467-80
116. Veigel C, Coluccio LM, Jontes JD, Sparrow JC, Milligan RA, Molloy JE. 1999. The motor protein myosin-I produces its working stroke in two steps. Nature 398:530-33
117. Wang LH, Kalb RG, Strittmatter SM. 1999. A PDZ protein regulates the distribution of the transmembrane semaphorin, M-SemF. J. Biol. Chem. 274:14137-46
118. Warner CL, Stewart A, Luzio JP, Steel KP, Libby RT, et al. 2003. Loss of myosin VI reduces secretion and the size of the Golgi in fibroblasts from Snell's waltzer mice. EMBO J. 22:569-79
119. Warshaw DM, Guilford WH, Freyzon Y, Krementsova E, Palmiter KA, et al. 2000. The light chain binding domain of expressed smooth muscle heavy meromyosin acts as a mechanical lever. J. Biol. Chem. 275:37167-72
120. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM, et al. 1999. Myosin VI is an actin-based motor that moves backwards. Nature 401:505-8
121. Woods DF, Bryant PJ. 1991. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66:451-64
122. Wu H, Nash JE, Zamorano P, Garner CC. 2002. Interaction of SAP97 with minus-end-directed actin motor myosin VI. Implications for AMPA receptor trafficking. J. Biol. Chem. 277:30928-34
123. Wu H, Reuver SM, Kuhlendahl S, Chung WJ, Garner CC. 1998. Subcellular targeting and cytoskeletal attachment of SAP97 to the epithelial lateral membrane. J. Cell Sci. 111:2365-76
124. Xu XX, Yi T, Tang B, Lambeth JD. 1998. Disabled-2 (Dab2) is an SH3 domain-binding partner of Grb2. Oncogene 16:1561-69
125. Yamashita RA, Sellers JR, Anderson JB. 2000. Identification and analysis of the myosin superfamily in Drosophila: a database approach. J. Muscle Res. Cell Motil. 21:491-505