Cellular and Molecular Life Sciences

, Volume 67, Issue 8, pp 1239–1254

Myosin motor function: the ins and outs of actin-based membrane protrusions

  • Rajalakshmi Nambiar
  • Russell E. McConnell
  • Matthew J. Tyska
Review
  • 574 Downloads

Abstract

Cells build plasma membrane protrusions supported by parallel bundles of F-actin to enable a wide variety of biological functions, ranging from motility to host defense. Filopodia, microvilli and stereocilia are three such protrusions that have been the focus of intense biological and biophysical investigation in recent years. While it is evident that actin dynamics play a significant role in the formation of these organelles, members of the myosin superfamily have also been implicated as key players in the maintenance of protrusion architecture and function. Based on a simple analysis of the physical forces that control protrusion formation and morphology, as well as our review of available data, we propose that myosins play two general roles within these structures: (1) as cargo transporters to move critical regulatory components toward distal tips and (2) as mediators of membrane-cytoskeleton adhesion.

Keywords

Microvilli Stereocilia Filopodia Brush border Tension Transport 

References

  1. 1.
    Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465PubMedGoogle Scholar
  2. 2.
    Weaver AM (2008) Invadopodia. Curr Biol 18:R362–R364PubMedGoogle Scholar
  3. 3.
    Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145:1009–1026PubMedGoogle Scholar
  4. 4.
    Small JV, Stradal T, Vignal E, Rottner K (2002) The lamellipodium: where motility begins. Trends Cell Biol 12:112–120PubMedGoogle Scholar
  5. 5.
    Bretscher A (1986) Purification of the intestinal microvillus cytoskeletal proteins villin, fimbrin, and ezrin. Methods Enzymol 134:24–37PubMedGoogle Scholar
  6. 6.
    Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG (2006) Role of fascin in filopodial protrusion. J Cell Biol 174:863–875PubMedGoogle Scholar
  7. 7.
    Loomis PA, Zheng L, Sekerkova G, Changyaleket B, Mugnaini E, Bartles JR (2003) Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo. J Cell Biol 163:1045–1055PubMedGoogle Scholar
  8. 8.
    Revenu C, Athman R, Robine S, Louvard D (2004) The co-workers of actin filaments: from cell structures to signals. Nat Rev Mol Cell Biol 5:635–646PubMedGoogle Scholar
  9. 9.
    Mattila PK, Lappalainen P (2008) Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9:446–454PubMedGoogle Scholar
  10. 10.
    Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG (2004) Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118:363–373PubMedGoogle Scholar
  11. 11.
    Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB (2002) Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109:509–521PubMedGoogle Scholar
  12. 12.
    Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, Borisy GG (2003) Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160:409–421PubMedGoogle Scholar
  13. 13.
    Applewhite DA, Barzik M, Kojima S, Svitkina TM, Gertler FB, Borisy GG (2007) Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol Biol Cell 18:2579–2591PubMedGoogle Scholar
  14. 14.
    Kerber ML, Jacobs DT, Campagnola L, Dunn BD, Yin T, Sousa AD, Quintero OA, Cheney RE (2009) A novel form of motility in filopodia revealed by imaging myosin-X at the single-molecule level. Curr Biol 19:967–973PubMedGoogle Scholar
  15. 15.
    Berg JS, Cheney RE (2002) Myosin-X is an unconventional myosin that undergoes intrafilopodial motility. Nat Cell Biol 4:246–250PubMedGoogle Scholar
  16. 16.
    Liu R, Woolner S, Johndrow JE, Metzger D, Flores A, Parkhurst SM (2008) Sisyphus, the Drosophila myosin XV homolog, traffics within filopodia transporting key sensory and adhesion cargos. Development 135:53–63PubMedGoogle Scholar
  17. 17.
    Tyska MJ, Mackey AT, Huang JD, Copeland NG, Jenkins NA, Mooseker MS (2005) Myosin-1a is critical for normal brush border structure and composition. Mol Biol Cell 16:2443–2457PubMedGoogle Scholar
  18. 18.
    Bartles JR, Zheng L, Li A, Wierda A, Chen B (1998) Small espin: a third actin-bundling protein and potential forked protein ortholog in brush border microvilli. J Cell Biol 143:107–119PubMedGoogle Scholar
  19. 19.
    Bretscher A, Weber K (1979) Villin: the major microfilament-associated protein of the intestinal microvillus. Proc Natl Acad Sci USA 76:2321–2325PubMedGoogle Scholar
  20. 20.
    Bretscher A, Weber K (1980) Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J Cell Biol 86:335–340PubMedGoogle Scholar
  21. 21.
    Tyska MJ, Mooseker MS (2002) MYO1A (brush border myosin I) dynamics in the brush border of LLC-PK1-CL4 cells. Biophys J 82:1869–1883PubMedGoogle Scholar
  22. 22.
    Heintzelman M, Hasson T, Mooseker M (1994) Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J Cell Sci 107:3535–3543PubMedGoogle Scholar
  23. 23.
    Mooseker MS, Tilney LG (1975) Organization of an actin filament-membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J Cell Biol 67:725–743PubMedGoogle Scholar
  24. 24.
    Bonilha VL, Rayborn ME, Saotome I, McClatchey AI, Hollyfield JG (2006) Microvilli defects in retinas of ezrin knockout mice. Exp Eye Res 82:720–729PubMedGoogle Scholar
  25. 25.
    Bretscher A, Edwards K, Fehon RG (2002) ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3:586–599PubMedGoogle Scholar
  26. 26.
    Saotome I, Curto M, McClatchey AI (2004) Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell 6:855–864PubMedGoogle Scholar
  27. 27.
    McConnell RE, Higginbotham JN, Shifrin DA Jr, Tabb DL, Coffey RJ, Tyska MJ (2009) The enterocyte microvillus is a vesicle-generating organelle. J Cell Biol 185:1285–1298PubMedGoogle Scholar
  28. 28.
    McConnell RE, Tyska MJ (2007) Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J Cell Biol 177:671–681PubMedGoogle Scholar
  29. 29.
    Bates JM, Akerlund J, Mittge E, Guillemin K (2007) Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2:371–382PubMedGoogle Scholar
  30. 30.
    Goldberg RF, Austen WG Jr, Zhang X, Munene G, Mostafa G, Biswas S, McCormack M, Eberlin KR, Nguyen JT, Tatlidede HS, Warren HS, Narisawa S, Millan JL, Hodin RA (2008) Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc Natl Acad Sci USA 105:3551–3556PubMedGoogle Scholar
  31. 31.
    Guo P, Weinstein AM, Weinbaum S (2000) A hydrodynamic mechanosensory hypothesis for brush border microvilli. Am J Physiol Renal Physiol 279:F698–F712PubMedGoogle Scholar
  32. 32.
    Du Z, Duan Y, Yan Q, Weinstein AM, Weinbaum S, Wang T (2004) Mechanosensory function of microvilli of the kidney proximal tubule. Proc Natl Acad Sci USA 101:13068–13073PubMedGoogle Scholar
  33. 33.
    Wang T (2006) Flow-activated transport events along the nephron. Curr Opin Nephrol Hypertens 15:530–536PubMedGoogle Scholar
  34. 34.
    Manor U, Kachar B (2008) Dynamic length regulation of sensory stereocilia. Semin Cell Dev Biol 19:502–510PubMedGoogle Scholar
  35. 35.
    Flock A, Bretscher A, Weber K (1982) Immunohistochemical localization of several cytoskeletal proteins in inner ear sensory and supporting cells. Hear Res 7:75–89PubMedGoogle Scholar
  36. 36.
    Zheng L, Sekerkova G, Vranich K, Tilney LG, Mugnaini E, Bartles JR (2000) The deaf jerker mouse has a mutation in the gene encoding the espin actin-bundling proteins of hair cell stereocilia and lacks espins. Cell 102:377–385PubMedGoogle Scholar
  37. 37.
    Hirokawa N (1986) Cytoskeletal architecture of the chicken hair cells revealed with the quick-freeze, deep-etch technique. Hear Res 22:41–54PubMedGoogle Scholar
  38. 38.
    Rzadzinska AK, Schneider ME, Davies C, Riordan GP, Kachar B (2004) An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J Cell Biol 164:887–897PubMedGoogle Scholar
  39. 39.
    Tilney LG, Derosier DJ, Mulroy MJ (1980) The organization of actin filaments in the stereocilia of cochlear hair cells. J Cell Biol 86:244–259PubMedGoogle Scholar
  40. 40.
    Hudspeth AJ (1989) How the ear’s works work. Nature 341:397–404PubMedGoogle Scholar
  41. 41.
    Sakaguchi H, Tokita J, Muller U, Kachar B (2009) Tip links in hair cells: molecular composition and role in hearing loss. Curr Opin Otolaryngol Head Neck Surg 17:388–393PubMedGoogle Scholar
  42. 42.
    Corey DP, Hudspeth AJ (1979) Response latency of vertebrate hair cells. Biophys J 26:499–506PubMedGoogle Scholar
  43. 43.
    Howard J, Hudspeth AJ (1988) Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog’s saccular hair cell. Neuron 1:189–199PubMedGoogle Scholar
  44. 44.
    Atilgan E, Wirtz D, Sun SX (2006) Mechanics and dynamics of actin-driven thin membrane protrusions. Biophys J 90:65–76PubMedGoogle Scholar
  45. 45.
    Pronk S, Geissler PL, Fletcher DA (2008) Limits of filopodium stability. Phys Rev Lett 100:258102PubMedGoogle Scholar
  46. 46.
    Derenyi I, Julicher F, Prost J (2002) Formation and interaction of membrane tubes. Phys Rev Lett 88:238101PubMedGoogle Scholar
  47. 47.
    Helfrich W (1973) Elastic properties of lipid bilayers—theory and possible experiments. Z Naturforsch C 28:693–703PubMedGoogle Scholar
  48. 48.
    Hochmuth FM, Shao JY, Dai J, Sheetz MP (1996) Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys J 70:358–369PubMedGoogle Scholar
  49. 49.
    Davenport RW, Dou P, Rehder V, Kater SB (1993) A sensory role for neuronal growth cone filopodia. Nature 361:721–724PubMedGoogle Scholar
  50. 50.
    Peskin CS, Odell GM, Oster GF (1993) Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J 65:316–324PubMedGoogle Scholar
  51. 51.
    Mogilner A, Rubinstein B (2005) The physics of filopodial protrusion. Biophys J 89:782–795PubMedGoogle Scholar
  52. 52.
    Feynman RP (1963) The Feynman lectures on physics. Addison-Wesley, MassachussettsGoogle Scholar
  53. 53.
    Miyata H, Nishiyama S, Akashi K, Kinosita K Jr (1999) Protrusive growth from giant liposomes driven by actin polymerization. Proc Natl Acad Sci USA 96:2048–2053PubMedGoogle Scholar
  54. 54.
    Theriot JA (1995) The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol 11:213–239PubMedGoogle Scholar
  55. 55.
    Shaevitz JW, Fletcher DA (2007) Load fluctuations drive actin network growth. Proc Natl Acad Sci USA 104:15688–15692PubMedGoogle Scholar
  56. 56.
    Goldberg MB, Theriot JA (1995) Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proc Natl Acad Sci USA 92:6572–6576PubMedGoogle Scholar
  57. 57.
    Mogilner A, Oster G (1996) Cell motility driven by actin polymerization. Biophys J 71:3030–3045PubMedGoogle Scholar
  58. 58.
    Mogilner A, Oster G (2003) Force generation by actin polymerization II: the elastic ratchet and tethered filaments. Biophys J 84:1591–1605PubMedGoogle Scholar
  59. 59.
    Howard J (2001) Mechanics of motor proteins and the cytoskeleton. Sinauer Associates, New YorkGoogle Scholar
  60. 60.
    Theriot JA (2000) The polymerization motor. Traffic 1:19–28PubMedGoogle Scholar
  61. 61.
    Kovar DR, Pollard TD (2004) Progressing actin: formin as a processive elongation machine. Nat Cell Biol 6:1158–1159PubMedGoogle Scholar
  62. 62.
    Footer MJ, Kerssemakers JW, Theriot JA, Dogterom M (2007) Direct measurement of force generation by actin filament polymerization using an optical trap. Proc Natl Acad Sci USA 104:2181–2186PubMedGoogle Scholar
  63. 63.
    Yasuda R, Miyata H, Kinosita K Jr (1996) Direct measurement of the torsional rigidity of single actin filaments. J Mol Biol 263:227–236PubMedGoogle Scholar
  64. 64.
    Tokuo H, Mabuchi K, Ikebe M (2007) The motor activity of myosin-X promotes actin fiber convergence at the cell periphery to initiate filopodia formation. J Cell Biol 179:229–238PubMedGoogle Scholar
  65. 65.
    Liu AP, Richmond DL, Maibaum L, Pronk S, Geissler PL, Fletcher DA (2008) Membrane-induced bundling of actin filaments. Nat Phys 4:789–793PubMedGoogle Scholar
  66. 66.
    Claessens MM, Bathe M, Frey E, Bausch AR (2006) Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nat Mater 5:748–753PubMedGoogle Scholar
  67. 67.
    Bathe M, Heussinger C, Claessens MM, Bausch AR, Frey E (2008) Cytoskeletal bundle mechanics. Biophys J 94:2955–2964PubMedGoogle Scholar
  68. 68.
    Isambert H, Venier P, Maggs AC, Fattoum A, Kassab R, Pantaloni D, Carlier MF (1995) Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins. J Biol Chem 270:11437–11444PubMedGoogle Scholar
  69. 69.
    Shin JH, Mahadevan L, So PT, Matsudaira P (2004) Bending stiffness of a crystalline actin bundle. J Mol Biol 337:255–261PubMedGoogle Scholar
  70. 70.
    Lange K (1999) Microvillar Ca++ signaling: a new view of an old problem. J Cell Physiol 180:19–34PubMedGoogle Scholar
  71. 71.
    Shin JB, Streijger F, Beynon A, Peters T, Gadzala L, McMillen D, Bystrom C, Van der Zee CE, Wallimann T, Gillespie PG (2007) Hair bundles are specialized for ATP delivery via creatine kinase. Neuron 53:371–386PubMedGoogle Scholar
  72. 72.
    Drees F, Gertler FB (2008) Ena/VASP: proteins at the tip of the nervous system. Curr Opin Neurobiol 18:53–59PubMedGoogle Scholar
  73. 73.
    Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL (1993) A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90:5519–5523PubMedGoogle Scholar
  74. 74.
    Silverman MA, Leroux MR (2009) Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends Cell Biol 19:306–316PubMedGoogle Scholar
  75. 75.
    Pedersen LB, Rosenbaum JL (2008) Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85:23–61PubMedGoogle Scholar
  76. 76.
    Qin H, Diener DR, Geimer S, Cole DG, Rosenbaum JL (2004) Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J Cell Biol 164:255–266PubMedGoogle Scholar
  77. 77.
    Berg JS, Powell BC, Cheney RE (2001) A millennial myosin census. Mol Biol Cell 12:780–794PubMedGoogle Scholar
  78. 78.
    Tyska MJ, Warshaw DM (2002) The myosin power stroke. Cell Motil Cytoskeleton 51:1–15PubMedGoogle Scholar
  79. 79.
    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 93:4459–4464PubMedGoogle Scholar
  80. 80.
    Warshaw DM, Guilford WH, Freyzon Y, Krementsova E, Palmiter KA, Tyska MJ, Baker JE, Trybus KM (2000) The light chain binding domain of expressed smooth muscle heavy meromyosin acts as a mechanical lever. J Biol Chem 275:37167–37172PubMedGoogle Scholar
  81. 81.
    Krendel M, Mooseker MS (2005) Myosins: tails (and heads) of functional diversity. Physiology (Bethesda) 20:239–251Google Scholar
  82. 82.
    Sousa AD, Berg JS, Robertson BW, Meeker RB, Cheney RE (2006) Myo10 in brain: developmental regulation, identification of a headless isoform and dynamics in neurons. J Cell Sci 119:184–194PubMedGoogle Scholar
  83. 83.
    Homma K, Ikebe M (2005) Myosin X is a high duty ratio motor. J Biol Chem 280:29381–29391PubMedGoogle Scholar
  84. 84.
    Berg JS, Derfler BH, Pennisi CM, Corey DP, Cheney RE (2000) Myosin-X, a novel myosin with pleckstrin homology domains, associates with regions of dynamic actin. J Cell Sci 113(Pt 19):3439–3451PubMedGoogle Scholar
  85. 85.
    Knight PJ, Thirumurugan K, Xu Y, Wang F, Kalverda AP, Stafford WF 3rd, Sellers JR, Peckham M (2005) The predicted coiled-coil domain of myosin 10 forms a novel elongated domain that lengthens the head. J Biol Chem 280:34702–34708PubMedGoogle Scholar
  86. 86.
    Nagy S, Ricca BL, Norstrom MF, Courson DS, Brawley CM, Smithback PA, Rock RS (2008) A myosin motor that selects bundled actin for motility. Proc Natl Acad Sci USA 105:9616–9620PubMedGoogle Scholar
  87. 87.
    Bohil AB, Robertson BW, Cheney RE (2006) Myosin-X is a molecular motor that functions in filopodia formation. Proc Natl Acad Sci USA 103:12411–12416PubMedGoogle Scholar
  88. 88.
    Pi X, Ren R, Kelley R, Zhang C, Moser M, Bohil AB, Divito M, Cheney RE, Patterson C (2007) Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. J Cell Biol 179:1569–1582PubMedGoogle Scholar
  89. 89.
    Weber KL, Sokac AM, Berg JS, Cheney RE, Bement WM (2004) A microtubule-binding myosin required for nuclear anchoring and spindle assembly. Nature 431:325–329PubMedGoogle Scholar
  90. 90.
    Zhang H, Berg JS, Li Z, Wang Y, Lang P, Sousa AD, Bhaskar A, Cheney RE, Stromblad S (2004) Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat Cell Biol 6:523–531PubMedGoogle Scholar
  91. 91.
    Tokuo H, Ikebe M (2004) Myosin X transports Mena/VASP to the tip of filopodia. Biochem Biophys Res Commun 319:214–220PubMedGoogle Scholar
  92. 92.
    Hayden SM, Wolenski JS, Mooseker MS (1990) Binding of brush border myosin I to phospholipid vesicles. J Cell Biol 111:443–451PubMedGoogle Scholar
  93. 93.
    Chen ZY, Hasson T, Zhang DS, Schwender BJ, Derfler BH, Mooseker MS, Corey DP (2001) Myosin-VIIb, a novel unconventional myosin, is a constituent of microvilli in transporting epithelia. Genomics 72:285–296PubMedGoogle Scholar
  94. 94.
    Heintzelman MB, Hasson T, Mooseker MS (1994) Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J Cell Sci 107(Pt 12):3535–3543PubMedGoogle Scholar
  95. 95.
    Henn A, De La Cruz EM (2005) Vertebrate myosin VIIb is a high duty ratio motor adapted for generating and maintaining tension. J Biol Chem 280:39665–39676PubMedGoogle Scholar
  96. 96.
    Yang Y, Kovacs M, Xu Q, Anderson JB, Sellers JR (2005) Myosin VIIB from Drosophila is a high duty ratio motor. J Biol Chem 280:32061–32068PubMedGoogle Scholar
  97. 97.
    Trybus KM (2008) Myosin V from head to tail. Cell Mol Life Sci 65:1378–1389PubMedGoogle Scholar
  98. 98.
    Park H, Ramamurthy B, Travaglia M, Safer D, Chen LQ, Franzini-Armstrong C, Selvin PR, Sweeney HL (2006) Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering. Mol Cell 21:331–336PubMedGoogle Scholar
  99. 99.
    Yu C, Feng W, Wei Z, Miyanoiri Y, Wen W, Zhao Y, Zhang M (2009) Myosin VI undergoes cargo-mediated dimerization. Cell 138:537–548PubMedGoogle Scholar
  100. 100.
    Phichith D, Travaglia M, Yang Z, Liu X, Zong AB, Safer D, Sweeney HL (2009) Cargo binding induces dimerization of myosin VI. Proc Natl Acad Sci USA 106:17320–17324PubMedGoogle Scholar
  101. 101.
    Altman D, Sweeney HL, Spudich JA (2004) The mechanism of myosin VI translocation and its load-induced anchoring. Cell 116:737–749PubMedGoogle Scholar
  102. 102.
    De La Cruz EM, Ostap EM, Sweeney HL (2001) Kinetic mechanism and regulation of myosin VI. J Biol Chem 276:32373–32381PubMedGoogle Scholar
  103. 103.
    Yang LE, Maunsbach AB, Leong PK, McDonough AA (2005) Redistribution of myosin VI from top to base of proximal tubule microvilli during acute hypertension. J Am Soc Nephrol 16:2890–2896PubMedGoogle Scholar
  104. 104.
    Hasson T (2003) Myosin VI: two distinct roles in endocytosis. J Cell Sci 116:3453–3461PubMedGoogle Scholar
  105. 105.
    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–F794PubMedGoogle Scholar
  106. 106.
    Ameen N, Apodaca G (2007) Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8:998–1006PubMedGoogle Scholar
  107. 107.
    Blaine J, Okamura K, Arnal H, Breusegem S, Caldas Y, Millard A, Barry N, Levi M (2009) PTH-induced internalization of apical membrane NaPi2a: role of actin and myosin VI. Am J Physiol Cell Physiol 297:C1339–C1346PubMedGoogle Scholar
  108. 108.
    Redowicz MJ (1999) Myosins and deafness. J Muscle Res Cell Motil 20:241–248PubMedGoogle Scholar
  109. 109.
    Redowicz MJ (2002) Myosins and pathology: genetics and biology. Acta Biochim Pol 49:789–804PubMedGoogle Scholar
  110. 110.
    Belyantseva IA, Boger ET, Friedman TB (2003) Myosin XVa localizes to the tips of inner ear sensory cell stereocilia and is essential for staircase formation of the hair bundle. Proc Natl Acad Sci USA 100:13958–13963PubMedGoogle Scholar
  111. 111.
    Belyantseva IA, Boger ET, Naz S, Frolenkov GI, Sellers JR, Ahmed ZM, Griffith AJ, Friedman TB (2005) Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 7:148–156PubMedGoogle Scholar
  112. 112.
    Mburu P, Kikkawa Y, Townsend S, Romero R, Yonekawa H, Brown SD (2006) Whirlin complexes with p55 at the stereocilia tip during hair cell development. Proc Natl Acad Sci USA 103:10973–10978PubMedGoogle Scholar
  113. 113.
    Schneider ME, Dose AC, Salles FT, Chang W, Erickson FL, Burnside B, Kachar B (2006) A new compartment at stereocilia tips defined by spatial and temporal patterns of myosin IIIa expression. J Neurosci 26:10243–10252PubMedGoogle Scholar
  114. 114.
    Rzadzinska AK, Nevalainen EM, Prosser HM, Lappalainen P, Steel KP (2009) MyosinVIIa interacts with Twinfilin-2 at the tips of mechanosensory stereocilia in the inner ear. PLoS One 4:e7097PubMedGoogle Scholar
  115. 115.
    Dose AC, Burnside B (2000) Cloning and chromosomal localization of a human class III myosin. Genomics 67:333–342PubMedGoogle Scholar
  116. 116.
    Dose AC, Ananthanarayanan S, Moore JE, Corsa AC, Burnside B, Yengo CM (2008) The kinase domain alters the kinetic properties of the myosin IIIA motor. Biochemistry 47:2485–2496PubMedGoogle Scholar
  117. 117.
    Dose AC, Ananthanarayanan S, Moore JE, Burnside B, Yengo CM (2007) Kinetic mechanism of human myosin IIIA. J Biol Chem 282:216–231PubMedGoogle Scholar
  118. 118.
    Salles FT, Merritt RC Jr, Manor U, Dougherty GW, Sousa AD, Moore JE, Yengo CM, Dose AC, Kachar B (2009) Myosin IIIa boosts elongation of stereocilia by transporting espin 1 to the plus ends of actin filaments. Nat Cell Biol 11:443–450PubMedGoogle Scholar
  119. 119.
    Sakaguchi H, Tokita J, Naoz M, Bowen-Pope D, Gov NS, Kachar B (2008) Dynamic compartmentalization of protein tyrosine phosphatase receptor Q at the proximal end of stereocilia: implication of myosin VI-based transport. Cell Motil Cytoskeleton 65:528–538PubMedGoogle Scholar
  120. 120.
    Sheetz MP (2001) Cell control by membrane-cytoskeleton adhesion. Nat Rev Mol Cell Biol 2:392–396PubMedGoogle Scholar
  121. 121.
    Dai J, Sheetz MP (1999) Membrane tether formation from blebbing cells. Biophys J 77:3363–3370PubMedGoogle Scholar
  122. 122.
    Nambiar R, McConnell RE, Tyska MJ (2009) Control of cell membrane tension by myosin-I. Proc Natl Acad Sci USA 106:11972–11977PubMedGoogle Scholar
  123. 123.
    Laakso JM, Lewis JH, Shuman H, Ostap EM (2008) Myosin I can act as a molecular force sensor. Science 321:133–136PubMedGoogle Scholar
  124. 124.
    Donaudy F, Ferrara A, Esposito L, Hertzano R, Ben-David O, Bell RE, Melchionda S, Zelante L, Avraham KB, Gasparini P (2003) Multiple mutations of MYO1A, a cochlear-expressed gene, in sensorineural hearing loss. Am J Hum Genet 72:1571–1577PubMedGoogle Scholar
  125. 125.
    Gillespie PG, Wagner MC, Hudspeth AJ (1993) Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron 11:581–594PubMedGoogle Scholar
  126. 126.
    Stauffer EA, Scarborough JD, Hirono M, Miller ED, Shah K, Mercer JA, Holt JR, Gillespie PG (2005) Fast adaptation in vestibular hair cells requires myosin-1c activity. Neuron 47:541–553PubMedGoogle Scholar
  127. 127.
    Gillespie PG, Cyr JL (2004) Myosin-1c, the hair cell’s adaptation motor. Annu Rev Physiol 66:521–545PubMedGoogle Scholar
  128. 128.
    Holt JR, Gillespie SK, Provance DW, Shah K, Shokat KM, Corey DP, Mercer JA, Gillespie PG (2002) A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108:371–381PubMedGoogle Scholar
  129. 129.
    Garcia JA, Yee AG, Gillespie PG, Corey DP (1998) Localization of myosin-Ibeta near both ends of tip links in frog saccular hair cells. J Neurosci 18:8637–8647PubMedGoogle Scholar
  130. 130.
    Dumont RA, Zhao YD, Holt JR, Bahler M, Gillespie PG (2002) Myosin-I isozymes in neonatal rodent auditory and vestibular epithelia. J Assoc Res Otolaryngol 3:375–389PubMedGoogle Scholar
  131. 131.
    Raucher D, Sheetz MP (2001) Phospholipase C activation by anesthetics decreases membrane-cytoskeleton adhesion. J Cell Sci 114:3759–3766PubMedGoogle Scholar
  132. 132.
    Hokanson DE, Ostap EM (2006) Myo1c binds tightly and specifically to phosphatidylinositol 4, 5-bisphosphate and inositol 1, 4, 5-trisphosphate. Proc Natl Acad Sci USA 103:3118–3123PubMedGoogle Scholar
  133. 133.
    Hirono M, Denis CS, Richardson GP, Gillespie PG (2004) Hair cells require phosphatidylinositol 4, 5-bisphosphate for mechanical transduction and adaptation. Neuron 44:309–320PubMedGoogle Scholar
  134. 134.
    Etournay R, El-Amraoui A, Bahloul A, Blanchard S, Roux I, Pezeron G, Michalski N, Daviet L, Hardelin JP, Legrain P, Petit C (2005) PHR1, an integral membrane protein of the inner ear sensory cells, directly interacts with myosin 1c and myosin VIIa. J Cell Sci 118:2891–2899PubMedGoogle Scholar
  135. 135.
    Inoue A, Ikebe M (2003) Characterization of the motor activity of mammalian myosin VIIA. J Biol Chem 278:5478–5487PubMedGoogle Scholar
  136. 136.
    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 37:127–138PubMedGoogle Scholar
  137. 137.
    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 137:1287–1307PubMedGoogle Scholar
  138. 138.
    Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J, Mburu P, Varela A, Levilliers J, Weston MD, Kelley PM, Kimberling WJ, Wagenaar M, Levi-Acobas F, Larget-Piet D, Munnich A, Steel KP, Brown SDM, Petit C (1995) Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374:60–61PubMedGoogle Scholar
  139. 139.
    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 374:62–64PubMedGoogle Scholar
  140. 140.
    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 125:557–566PubMedGoogle Scholar
  141. 141.
    Boeda B, El-Amraoui A, Bahloul A, Goodyear R, Daviet L, Blanchard S, Perfettini I, Fath KR, Shorte S, Reiners J, Houdusse A, Legrain P, Wolfrum U, Richardson G, Petit C (2002) Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J 21:6689–6699PubMedGoogle Scholar
  142. 142.
    Senften M, Schwander M, Kazmierczak P, Lillo C, Shin JB, Hasson T, Geleoc GS, Gillespie PG, Williams D, Holt JR, Muller U (2006) Physical and functional interaction between protocadherin 15 and myosin VIIa in mechanosensory hair cells. J Neurosci 26:2060–2071PubMedGoogle Scholar
  143. 143.
    Kussel-Andermann P, El-Amraoui A, Safieddine S, Nouaille S, Perfettini I, Lecuit M, Cossart P, Wolfrum U, Petit C (2000) Vezatin, a novel transmembrane protein, bridges myosin VIIA to the cadherin–catenins complex. EMBO J 19:6020–6029PubMedGoogle Scholar
  144. 144.
    Siemens J, Kazmierczak P, Reynolds A, Sticker M, Littlewood-Evans A, Muller U (2002) The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions. Proc Natl Acad Sci USA 99:14946–14951PubMedGoogle Scholar
  145. 145.
    Muller U (2008) Cadherins and mechanotransduction by hair cells. Curr Opin Cell Biol 20:557–566PubMedGoogle Scholar
  146. 146.
    Tuxworth RI, Stephens S, Ryan ZC, Titus MA (2005) Identification of a myosin VII-talin complex. J Biol Chem 280:26557–26564PubMedGoogle Scholar
  147. 147.
    Tuxworth RI, Weber I, Wessels D, Addicks GC, Soll DR, Gerisch G, Titus MA (2001) A role for myosin VII in dynamic cell adhesion. Curr Biol 11:318–329PubMedGoogle Scholar
  148. 148.
    Deol MS, Green MC (1966) Snell’s waltzer, a new mutation affecting behaviour and the inner ear in the mouse. Genet Res 8:339–345PubMedGoogle Scholar
  149. 149.
    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 11:369–375PubMedGoogle Scholar
  150. 150.
    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 214:331–341PubMedGoogle Scholar
  151. 151.
    Hertzano R, Shalit E, Rzadzinska AK, Dror AA, Song L, Ron U, Tan JT, Shitrit AS, Fuchs H, Hasson T, Ben-Tal N, Sweeney HL, de Angelis MH, Steel KP, Avraham KB (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:e1000207PubMedGoogle Scholar
  152. 152.
    Holme RH, Kiernan BW, Brown SD, Steel KP (2002) Elongation of hair cell stereocilia is defective in the mouse mutant whirler. J Comp Neurol 450:94–102PubMedGoogle Scholar
  153. 153.
    Probst FJ et al (1998) Correction of deafness in shaker-2 mice by an unconventional myosin in a BAC transgene. Science 280:1444–1447PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2010

Authors and Affiliations

  • Rajalakshmi Nambiar
    • 1
  • Russell E. McConnell
    • 1
  • Matthew J. Tyska
    • 1
  1. 1.Department of Cell and Developmental BiologyVanderbilt University Medical CenterNashvilleUSA

Personalised recommendations