Two single-headed myosin V motors bound to a tetrameric adapter protein form a processive complex

Journal of Cell Biology

Volumn 195, Issue 4, 2011, Pages 631-641

  Krementsova, Elena B ^a   Hodges, Alex R ^a   Bookwalter, Carol S ^a   Sladewski, Thomas E ^a   Travaglia, Mirko ^b   Sweeney, H Lee ^b   Trybus, Kathleen M ^b  

^a UNIVERSITY OF VERMONT   (Canada)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADAPTOR PROTEIN; MESSENGER RNA; MYOSIN V; PROTEIN SHE2P; RNA BINDING PROTEIN; TROPOMYOSIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CHROMOSOME MAP; MOTOR ACTIVITY; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; YEAST;

MODELS, MOLECULAR; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PROTEIN CONFORMATION; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES; VERTEBRATA;

EID: 81455147547     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201106146     Document Type: Article

References (54)

1. Ali, M.Y., H. Lu, C.S. Bookwalter, D.M. Warshaw, and K.M. Trybus. 2008. Myosin V and Kinesin act as tethers to enhance each others' processivity. Proc. Natl. Acad. Sci. USA. 105:4691-4696. http://dx.doi.org/10.1073/pnas.0711531105.
2. Baker, J.E., E.B. Krementsova, G.G. Kennedy, A. Armstrong, K.M. Trybus, and D.M. Warshaw. 2004. Myosin V processivity: Multiple kinetic pathways for head-to-head coordination. Proc. Natl. Acad. Sci. USA. 101:5542-5546. http://dx.doi.org/10.1073/pnas.0307247101.
3. Bertrand, E., P. Chartrand, M. Schaefer, S.M. Shenoy, R.H. Singer, and R.M. Long. 1998. Localization of ASH1 mRNA particles in living yeast. Mol. Cell. 2:437-445. http://dx.doi.org/10.1016/S1097-2765(00)80143-4.
4. Bookwalter, C.S., M. Lord, and K.M. Trybus. 2009. Essential features of the class V myosin from budding yeast for ASH1 mRNA transport. Mol. Biol. Cell. 20:3414-3421. http://dx.doi.org/10.1091/mbc.E08-08-0801.
5. Chung, S., and P.A. Takizawa. 2010. Multiple Myo4 motors enhance ASH1 mRNA transport in Saccharomyces cerevisiae. J. Cell Biol. 189:755-767. http://dx.doi.org/10.1083/jcb.200912011.
6. Cook, R.K., D.R. Sheff, and P.A. Rubenstein. 1991. Unusual metabolism of the yeast actin amino terminus. J. Biol. Chem. 266:16825-16833..
7. Cronan, J.E. Jr. 1990. Biotination of proteins in vivo. A post-translational modification to label, purify, and study proteins. J. Biol. Chem. 265: 10327-10333..
8. Du, T.G., S. Jellbauer, M. Müller, M. Schmid, D. Niessing, and R.P. Jansen. 2008. Nuclear transit of the RNA-binding protein She2 is required for translational control of localized ASH1 mRNA. EMBO Rep. 9:781-787. http://dx.doi.org/10.1038/embor.2008.112.
9. Dunn, B.D., T. Sakamoto, M.S. Hong, J.R. Sellers, and P.A. Takizawa. 2007. Myo4p is a monomeric myosin with motility uniquely adapted to transport mRNA. J. Cell Biol. 178:1193-1206. http://dx.doi.org/10.1083/jcb.200707080.
10. Elting, M.W., Z. Bryant, J.C. Liao, and J.A. Spudich. 2011. Detailed tuning of structure and intramolecular communication are dispensable for processive motion of myosin VI. Biophys. J. 100:430-439. http://dx.doi.org/10.1016/j.bpj.2010.11.045.
11. Estrada, P., J. Kim, J. Coleman, L. Walker, B. Dunn, P. Takizawa, P. Novick, and S. Ferro-Novick. 2003. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163:1255-1266. http://dx.doi.org/10.1083/jcb.200304030.
12. Haarer, B.K., A. Petzold, S.H. Lillie, and S.S. Brown. 1994. Identification of MYO4, a second class V myosin gene in yeast. J. Cell Sci. 107: 1055-1064..
13. Heuck, A., I. Fetka, D.N. Brewer, D. Hüls, M. Munson, R.P. Jansen, and D. Niessing. 2010. The structure of the Myo4p globular tail and its function in ASH1 mRNA localization. J. Cell Biol. 189:497-510. http://dx.doi.org/10.1083/jcb.201002076.
14. Hodges, A.R., E.B. Krementsova, and K.M. Trybus. 2007. Engineering the processive run length of Myosin V. J. Biol. Chem. 282:27192-27197. http://dx.doi.org/10.1074/jbc.M703968200.
15. Hodges, A.R., E.B. Krementsova, and K.M. Trybus. 2008. She3p binds to the rod of yeast myosin V and prevents it from dimerizing, forming a single-headed motor complex. J. Biol. Chem. 283:6906-6914. http://dx.doi.org/10.1074/jbc.M708865200.
16. Jambhekar, A., K. McDermott, K. Sorber, K.A. Shepard, R.D. Vale, P.A. Takizawa, and J.L. DeRisi. 2005. Unbiased selection of localization elements reveals cis-acting determinants of mRNA bud localization in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 102:18005-18010. http://dx.doi.org/10.1073/pnas.0509229102.
17. Kerssemakers, J.W., E.L. Munteanu, L. Laan, T.L. Noetzel, M.E. Janson, and M. Dogterom. 2006. Assembly dynamics of microtubules at molecular resolution. Nature. 442:709-712. http://dx.doi.org/10.1038/nature04928.
18. Krementsova, E.B., A.R. Hodges, H. Lu, and K.M. Trybus. 2006. Processivity of chimeric class V myosins. J. Biol. Chem. 281:6079-6086. http://dx.doi.org/10.1074/jbc.M510041200.
19. Landers, S.M., M.R. Gallas, J. Little, and R.M. Long. 2009. She3p possesses a novel activity required for ASH1 mRNA localization in Saccharomyces cerevisiae. Eukaryot. Cell. 8:1072-1083. http://dx.doi.org/10.1128/EC.00084-09.
20. Lange, S., Y. Katayama, M. Schmid, O. Burkacky, C. Bräuchle, D.C. Lamb, and R.P. Jansen. 2008. Simultaneous transport of different localized mRNA species revealed by live-cell imaging. Traffic. 9:1256-1267. http://dx.doi.org/10.1111/j.1600-0854.2008.00763.x.
21. Li, S.J., and J.E. Cronan Jr. 1992. The gene encoding the biotin carboxylase subunit of Escherichia coli acetyl-CoA carboxylase. J. Biol. Chem. 267:855-863..
22. Long, R.M., R.H. Singer, X. Meng, I. Gonzalez, K. Nasmyth, and R.P. Jansen. 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science. 277:383-387. http://dx.doi.org/10.1126/science.277.5324.383.
23. Maytum, R., M.A. Geeves, and M. Konrad. 2000. Actomyosin regulatory properties of yeast tropomyosin are dependent upon N-terminal modification. Biochemistry. 39:11913-11920. http://dx.doi.org/10.1021/bi000977g.
24. Maytum, R., M. Konrad, S.S. Lehrer, and M.A. Geeves. 2001. Regulatory properties of tropomyosin effects of length, isoform, and N-terminal sequence. Biochemistry. 40:7334-7341. http://dx.doi.org/10.1021/bi010072i.
25. Miller, B.M., and K.M. Trybus. 2008. Functional effects of nemaline myopathy mutations on human skeletal alpha-actin. J. Biol. Chem. 283:19379-19388. http://dx.doi.org/10.1074/jbc.M801963200.
26. Müller, M., K. Richter, A. Heuck, E. Kremmer, J. Buchner, R.P. Jansen, and D. Niessing. 2009. Formation of She2p tetramers is required for mRNA binding, mRNP assembly, and localization. RNA. 15:2002-2012. http://dx.doi.org/10.1261/rna.1753309.
27. Müller, M., R.G. Heym, A. Mayer, K. Kramer, M. Schmid, P. Cramer, H. Urlaub, R.P. Jansen, and D. Niessing. 2011. A cytoplasmic complex mediates specific mRNA recognition and localization in yeast. PLoS Biol. 9:e1000611. http://dx.doi.org/10.1371/journal.pbio.1000611.
28. Mutch, S.A., B.S. Fujimoto, C.L. Kuyper, J.S. Kuo, S.M. Bajjalieh, and D.T. Chiu. 2007. Deconvolving single-molecule intensity distributions for quantitative microscopy measurements. Biophys. J. 92:2926-2943. http://dx.doi.org/10.1529/biophysj.106.101428.
29. Niessing, D., S. Hüttelmaier, D. Zenklusen, R.H. Singer, and S.K. Burley. 2004. She2p is a novel RNA binding protein with a basic helical hairpin motif. Cell. 119:491-502. http://dx.doi.org/10.1016/j.cell.2004.10.018.
30. Oguchi, Y., S.V. Mikhailenko, T. Ohki, A.O. Olivares, E.M. De La Cruz, and S. Ishiwata. 2008. Load-dependent ADP binding to myosins V and VI: implications for subunit coordination and function. Proc. Natl. Acad. Sci. USA. 105:7714-7719. http://dx.doi.org/10.1073/pnas.0800564105.
31. Oke, O.A., S.A. Burgess, E. Forgacs, P.J. Knight, T. Sakamoto, J.R. Sellers, H. White, and J. Trinick. 2010. Influence of lever structure on myosin 5a walking. Proc. Natl. Acad. Sci. USA. 107:2509-2514. http://dx.doi.org/10.1073/pnas.0906907107.
32. Pardee, J.D., and J.A. Spudich. 1982. Purification of muscle actin. Methods Enzymol. 85(Pt B):164-181. http://dx.doi.org/10.1016/0076-6879(82) 85020-9.
33. Phichith, D., M. Travaglia, Z. Yang, X. Liu, A.B. Zong, D. Safer, and H.L. Sweeney. 2009. Cargo binding induces dimerization of myosin VI. Proc. Natl. Acad. Sci. USA. 106:17320-17324. http://dx.doi.org/10.1073/pnas.0909748106.
34. Philo, J.S. 2000. A method for directly fitting the time derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions. Anal. Biochem. 279:151-163. http://dx.doi.org/10.1006/abio.2000.4480.
35. Purcell, T.J., H.L. Sweeney, and J.A. Spudich. 2005. A force-dependent state controls the coordination of processive myosin V. Proc. Natl. Acad. Sci. USA. 102:13873-13878. http://dx.doi.org/10.1073/pnas.0506441102.
36. Reck-Peterson, S.L., M.J. Tyska, P.J. Novick, and M.S. Mooseker. 2001. The yeast class V myosins, Myo2p and Myo4p, are nonprocessive actin-based motors. J. Cell Biol. 153:1121-1126. http://dx.doi.org/10.1083/jcb.153.5.1121.
37. Sage, D., F.R. Neumann, F. Hediger, S.M. Gasser, and M. Unser. 2005. Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE Trans. Image Process. 14:1372-1383. http://dx.doi.org/10.1109/TIP.2005.852787.
38. Sakai, T., N. Umeki, R. Ikebe, and M. Ikebe. 2011. Cargo binding activates myosin VIIA motor function in cells. Proc. Natl. Acad. Sci. USA. 108:7028-7033. http://dx.doi.org/10.1073/pnas.1009188108.
39. Schmid, M., A. Jaedicke, T.G. Du, and R.P. Jansen. 2006. Coordination of endoplasmic reticulum and mRNA localization to the yeast bud. Curr. Biol. 16:1538-1543. http://dx.doi.org/10.1016/j.cub.2006.06.025.
40. Shen, Z., N. Paquin, A. Forget, and P. Chartrand. 2009. Nuclear shuttling of She2p couples ASH1 mRNA localization to its translational repression by recruiting Loc1p and Puf6p. Mol. Biol. Cell. 20:2265-2275. http://dx.doi.org/10.1091/mbc.E08-11-1151.
41. Shepard, K.A., A.P. Gerber, A. Jambhekar, P.A. Takizawa, P.O. Brown, D. Herschlag, J.L. DeRisi, and R.D. Vale. 2003. Widespread cytoplasmic mRNA transport in yeast: Identification of 22 bud-localized transcripts using DNA microarray analysis. Proc. Natl. Acad. Sci. USA. 100:11429-11434. http://dx.doi.org/10.1073/pnas.2033246100.
42. Sil, A., and I. Herskowitz. 1996. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell. 84:711-722. http://dx.doi.org/10.1016/S0092-8674(00)81049-1.
43. Sivaramakrishnan, S., and J.A. Spudich. 2009. Coupled myosin VI motors facilitate unidirectional movement on an F-actin network. J. Cell Biol. 187:53-60. http://dx.doi.org/10.1083/jcb.200906133.
44. Sweeney, H.L., and A. Houdusse. 2010. Myosin VI rewrites the rules for myosin motors. Cell. 141:573-582. http://dx.doi.org/10.1016/j.cell.2010.04.028.
45. Takagi, Y., Y. Yang, I. Fujiwara, D. Jacobs, R.E. Cheney, J.R. Sellers, and M. Kovács. 2008. Human myosin Vc is a low duty ratio, nonprocessive molecular motor. J. Biol. Chem. 283:8527-8537. http://dx.doi.org/10.1074/jbc.M709150200.
46. Takizawa, P.A., A. Sil, J.R. Swedlow, I. Herskowitz, and R.D. Vale. 1997. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature. 389:90-93. http://dx.doi.org/10.1038/38015.
47. Tóth, J., M. Kovács, F. Wang, L. Nyitray, and J.R. Sellers. 2005. Myosin V from Drosophila reveals diversity of motor mechanisms within the myosin V family. J. Biol. Chem. 280:30594-30603. http://dx.doi.org/10.1074/jbc.M505209200.
48. Veigel, C., F. Wang, M.L. Bartoo, J.R. Sellers, and J.E. Molloy. 2002. The gated gait of the processive molecular motor, myosin V. Nat. Cell Biol. 4:59-65. http://dx.doi.org/10.1038/ncb732.
49. Veigel, C., S. Schmitz, F. Wang, and J.R. Sellers. 2005. Load-dependent kinetics of myosin-V can explain its high processivity. Nat. Cell Biol. 7:861-869. http://dx.doi.org/10.1038/ncb1287.
50. Walker, M.L., S.A. Burgess, J.R. Sellers, F. Wang, J.A. Hammer III, J. Trinick, and P.J. Knight. 2000. Two-headed binding of a processive myosin to F-actin. Nature. 405:804-807. http://dx.doi.org/10.1038/35015592.
51. Warshaw, D.M., G.G. Kennedy, S.S. Work, E.B. Krementsova, S. Beck, and K.M. Trybus. 2005. Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity. Biophys. J. 88:L30-L32. http://dx.doi.org/10.1529/biophysj.105.061903.
52. Watanabe, S., T.M. Watanabe, O. Sato, J. Awata, K. Homma, N. Umeki, H. Higuchi, R. Ikebe, and M. Ikebe. 2008. Human myosin Vc is a low duty ratio nonprocessive motor. J. Biol. Chem. 283:10581-10592. http://dx.doi.org/10.1074/jbc.M707657200.
53. Yildiz, A., J.N. Forkey, S.A. McKinney, T. Ha, Y.E. Goldman, and P.R. Selvin. 2003. Myosin V walks hand-over-hand: Single fluorophore imaging with 1.5-nm localization. Science. 300:2061-2065. http://dx.doi.org/10.1126/science.1084398.
54. Yu, C., W. Feng, Z. Wei, Y. Miyanoiri, W. Wen, Y. Zhao, and M. Zhang. 2009. Myosin VI undergoes cargo-mediated dimerization. Cell. 138:537-548. http://dx.doi.org/10.1016/j.cell.2009.05.030.