Myosin VI has a one track mind versus myosin va when moving on actin bundles or at an intersection

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Volumn 14, Issue 1, 2013, Pages 70-81

  Ali, M Yusuf ^a   Previs, Samantha B ^a   Trybus, Kathleen M ^a   Sweeney, H Lee ^b   Warshaw, David M ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Anchor; Cargo transporter; Cytoskeleton; Molecular motors; Processivity; Qdot; Single molecule; Tether

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; ALPHA ACTININ; MYOSIN VA; MYOSIN VI; FASCIN; MOLECULAR MOTOR; QUANTUM DOT;

ACTIN FILAMENT; ARTICLE; CELL TRANSPORT; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; BINDING SITE; CHIMERA; CYTOSKELETON; INTRACELLULAR SIGNALING; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; STRESS FIBER;

ACTIN CYTOSKELETON; ACTININ; ANIMALS; CARRIER PROTEINS; CHICKENS; MICE; MICROFILAMENT PROTEINS; MOTION; MUTATION; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; SWINE;

EID: 84873255855     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12017     Document Type: Article

References (59)

1. Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS, Cheney RE. Myosin-V is a processive actin-based motor. Nature 1999;400:590-593.
2. Okten Z, Churchman LS, Rock RS, Spudich JA. Myosin VI walks hand-over-hand along actin. Nat Struct Mol Biol 2004;11:884-887.
3. Rock RS, Rice SE, Wells AL, Purcell TJ, Spudich JA, Sweeney HL. Myosin VI is a processive motor with a large step size. Proc Natl Acad Sci USA 2001;98:13655-13659.
4. Warshaw DM, Kennedy GG, Work SS, Krementsova EB, Beck S, Trybus KM. Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity. Biophys J 2005;88:L30-32.
5. Yildiz A, Forkey JN, McKinney SA, Ha T, Goldman YE, Selvin PR. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 2003;300:2061-2065.
6. Yildiz A, Park H, Safer D, Yang Z, Chen LQ, Selvin PR, Sweeney HL. Myosin VI steps via a hand-over-hand mechanism with its lever arm undergoing fluctuations when attached to actin. J Biol Chem 2004;279:37223-37226.
7. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM, Hasson T, Carragher BO, Milligan RA, Sweeney HL. Myosin VI is an actin-based motor that moves backwards. Nature 1999;401:505-508.
8. Buss F, Kendrick-Jones J. Myosin VI: a multifunctional motor in proteins and cell regulations. In: Coluccio LM, editor. Myosins, A Superfamily of Molecular Motors. Dordrecht, The Netherlands: Spinger; 2008, pp. 325-352.
9. Sellers JR, Weisman LS. Myosin V in proteins and cell regulations. In: Coluccio LM, editor. Myosins, A Superfamily of Molecular Motors. Dordrecht, The Netherlands: Spinger; 2008, pp. 289-323.
10. Park H, Li A, Chen LQ, Houdusse A, Selvin PR, Sweeney HL. The unique insert at the end of themyosin VI motor is the sole determinant of directionality. Proc Natl Acad Sci USA 2007;104:778-783.
11. Mukherjea M, Llinas P, Kim H, Travaglia M, Safer D, Menetrey J, Franzini-Armstrong C, Selvin PR, Houdusse A, Sweeney HL. Myosin VI dimerization triggers an unfolding of a three-helix bundle in order to extend its reach. Mol Cell 2009;35:305-315.
12. Spink BJ, Sivaramakrishnan S, Lipfert J, Doniach S, Spudich JA. Long single alpha-helical tail domains bridge the gap between structure and function of myosin VI. Nat Struct Mol Biol 2008;15:591-597.
13. Rock RS, Ramamurthy B, Dunn AR, Beccafico S, Rami BR, Morris C, Spink BJ, Franzini-Armstrong C, Spudich JA, Sweeney HL. A flexible domain is essential for the large step size and processivity of myosin VI. Mol Cell 2005;17:603-609.
14. Dunn AR, Spudich JA. Dynamics of the unbound head during myosin V processive translocation. Nat Struct Mol Biol 2007;14:246-248.
15. Shiroguchi K, Kinosita K Jr. Myosin V walks by lever action and Brownian motion. Science 2007;316:1208-1212.
16. Wu X, Bowers B, Rao K, Wei Q, Hammer JA 3rd. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function In vivo. J Cell Biol 1998;143:1899-1918.
17. Menasche G, Feldmann J, Houdusse A, Desaymard C, Fischer A, Goud B. de Saint Basile G. Biochemical and functional characterization of Rab27a mutations occurring in Griscelli syndrome patients. Blood 2003;101:2736-2742.
18. Provance DW Jr, Addison EJ, Wood PR, Chen DZ, Silan CM, Mercer JA. Myosin-Vb functions as a dynamic tether for peripheral endocytic compartments during transferrin trafficking. BMC Cell Biol 2008;9:44.
19. 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. 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 2008;4:e1000207.
20. Altman D, Sweeney HL, Spudich JA. The mechanism of myosin VI translocation and its load-induced anchoring. Cell 2004;116:737-749.
21. Ikezaki K, Komori T, Sugawa M, Arai Y, Nishikawa S, Iwane AH, Yanagida T. Simultaneous observation of the lever arm and head explains myosin VI dual function. Small 2012; 8:3035-3040.
22. Sweeney HL, Houdusse A. What can myosin VI do in cells? Curr Opin Cell Biol 2007;19:57-66.
23. Cohan CS, Welnhofer EA, Zhao L, Matsumura F, Yamashiro S. Role of the actin bundling protein fascin in growth cone morphogenesis: localization in filopodia and lamellipodia. Cell Motil Cytoskeleton 2001;48:109-120.
24. Ali MY, Krementsova EB, Kennedy GG, Mahaffy R, Pollard TD, Trybus KM, Warshaw DM. Myosin Va maneuvers through actin intersections and diffuses along microtubules. Proc Natl Acad Sci USA 2007;104:4332-4336.
25. Fujita K, Iwaki M, Iwane AH, Marcucci L, Yanagida T. Switching of myosin-V motion between the lever-arm swing and Brownian search-and-catch. Nat Commun 2012;3:956.
26. Reifenberger JG, Toprak E, Kim H, Safer D, Sweeney HL, Selvin PR. Myosin VI undergoes a 180 degrees power stroke implying an uncoupling of the front lever arm. Proc Natl Acad Sci USA 2009;106:18255-18260.
27. Brawley CM, Rock RS. Unconventional myosin traffic in cells reveals a selective actin cytoskeleton. Proc Natl Acad Sci USA 2009;106:9685-9690.
28. Ishikawa R, Sakamoto T, Ando T, Higashi-Fujime S, Kohama K. Polarized actin bundles formed by human fascin-1: their sliding and disassembly on myosin II and myosin V in vitro. J Neurochem 2003;87:676-685.
29. Meyer RK, Aebi U. Bundling of actin filaments by alpha-actinin depends on its molecular length. J Cell Biol 1990;110:2013-2024.
30. Nagy S, Rock RS. Structured post-IQ domain governs selectivity of myosin X for fascin-actin bundles. J Biol Chem 2010;285:26608-26617.
31. Nagy S, Ricca BL, NorstromMF, Courson DS, Brawley CM, Smithback PA, Rock RS. A myosin motor that selects bundled actin for motility. Proc Natl Acad Sci USA 2008;105:9616-9620.
32. Sun Y, Sato O, Ruhnow F, Arsenault ME, Ikebe M, Goldman YE. Single-molecule stepping and structural dynamics of myosin X. Nat Struct Mol Biol 2010;17:485-491.
33. Kodera N, Yamamoto D, Ishikawa R, Ando T. Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 2010;468:72-76.
34. Gebhardt JC, Clemen AE, Jaud J, Rief M. Myosin-V is a mechanical ratchet. Proc Natl Acad Sci USA 2006;103:8680-8685.
35. Kad NM, Trybus KM, Warshaw DM. Load and Pi control flux through the branched kinetic cycle of myosin V. J Biol Chem 2008;283:17477-17484.
36. Lu H, Kennedy GG, Warshaw DM, Trybus KM. Simultaneous observation of tail and head movements ofmyosin V during processive motion. J Biol Chem 2010;285:42068-42074.
37. Sun Y, SchroederHW3rd, Beausang JF, Homma K, Ikebe M, Goldman YE. Myosin VI walks "wiggly" on actin with large and variable tilting. Mol Cell 2007;28:954-964.
38. Warshaw DM. Tilting and twirling as myosin V steps along actin filaments as detected by fluorescence polarization. J Gen Physiol 2012;139:97-100.
39. De La Cruz EM, Wells AL, Rosenfeld SS, Ostap EM, Sweeney HL. The kinetic mechanism of myosin V. Proc Natl Acad Sci USA 1999;96:13726-13731.
40. Oguchi Y, Mikhailenko SV, Ohki T, Olivares AO, De La Cruz EM, Ishiwata S. Robust processivity of myosin V under off-axis loads. Nat Chem Biol 2010;6:300-305.
41. WuXS, Rao K, Zhang H, Wang F, Sellers JR, Matesic LE, Copeland NG, Jenkins NA, Hammer JA 3rd. Identification of an organelle receptor for myosin-Va. Nat Cell Biol 2002;4:271-278.
42. Buss F, Kendrick-Jones J, Lionne C, Knight AE, Cote GP, Paul Luzio J. 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 1998;143:1535-1545.
43. Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol 2005;169:285-295.
44. De La Cruz EM, Ostap EM, Sweeney HL. Kinetic mechanism and regulation of myosin VI. J Biol Chem 2001;276:32373-32381.
45. Bahloul A, Chevreux G, Wells AL, Martin D, Nolt J, Yang Z, Chen LQ, Potier N, Van Dorsselaer A, Rosenfeld S, Houdusse A, Sweeney HL. The unique insert in myosin VI is a structural calcium-calmodulin binding site. Proc Natl Acad Sci USA 2004;101:4787-4792.
46. Menetrey J, Bahloul A, Wells AL, Yengo CM, Morris CA, Sweeney HL, Houdusse A. The structure of the myosin VI motor reveals the mechanism of directionality reversal. Nature 2005;435:779-785.
47. Sweeney HL, Rosenfeld SS, Brown F, Faust L, Smith J, Xing J, Stein LA, Sellers JR. Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J Biol Chem 1998;273:6262-6270.
48. Baker JE, Krementsova EB, Kennedy GG, Armstrong A, Trybus KM, Warshaw DM. Myosin V processivity: multiple kinetic pathways for head-to-head coordination. Proc Natl Acad Sci USA 2004;101:5542-5546.
49. Cronan JE Jr. Biotination of proteins in vivo. A post-translational modification to label, purify, and study proteins. J Biol Chem 1990;265:10327-10333.
50. Krementsov DN, Krementsova EB, Trybus KM. Myosin V: regulation by calcium, calmodulin, and the tail domain. J Cell Biol 2004;164:877-886.
51. Krementsova EB, Hodges AR, Lu H, Trybus KM. Processivity of chimeric class V myosins. J Biol Chem 2006;281:6079-6086.
52. Lu H, Krementsova EB, Trybus KM. Regulation of myosin V processivity by calcium at the single molecule level. J Biol Chem 2006;281:31987-31994.
53. Warshaw DM, Desrosiers JM, Work SS, Trybus KM. Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro. J Cell Biol 1990;111:453-463.
54. Hodges AR, Bookwalter CS, Krementsova EB, Trybus KM. A nonprocessive class V myosin drives cargo processively when a kinesin- related protein is a passenger. Curr Biol 2009;19:2121-2125.
55. Ali MY, Kennedy GG, Safer D, Trybus KM, Sweeney HL, Warshaw DM. Myosin Va and myosin VI coordinate their steps while engaged in an in vitro tug of war during cargo transport. Proc Natl Acad Sci USA 2011;108:E535-541.
56. Ali MY, Lu H, Bookwalter CS, Warshaw DM, Trybus KM. Myosin V and Kinesin act as tethers to enhance each others' processivity. Proc Natl Acad Sci USA 2008;105:4691-4696.
57. Press WH, Teukolsky SA, Vetterling WT, Flannery BP. Numerical Recipes in C: The Art of Scientific Computing. Cambridge, UK: Cambridge University Press; 1992.
58. Kerssemakers JW, Munteanu EL, Laan L, Noetzel TL, Janson ME, Dogterom M. Assembly dynamics of microtubules at molecular resolution. Nature 2006;442:709-712.
59. Nelson SR, Ali MY, Trybus KM, Warshaw DM. Random walk of processive, quantum dot-labeled myosin Va molecules within the actin cortex of COS-7 cells. Biophys J 2009;97:509-518