In vitro reconstitution of an mRNA-transport complex reveals mechanisms of assembly and motor activation

Journal of Cell Biology

Volumn 203, Issue 6, 2013, Pages 971-984

  Heym, Roland G ^a,b   Zimmermann, Dennis ^b,c   Edelmann, Franziska T ^a   Israel, Lars ^b   Ökten, Zeynep ^b,d   Kovar, David R ^c   Niessing, Dierk ^a,b  

^a Institute for Diabetes and Obesity   (United Kingdom)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF CHICAGO   (United States)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; MESSENGER RNA; MYO4 PROTEIN, S CEREVISIAE; MYOSIN HEAVY CHAIN; MYOSIN V; RNA BINDING PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SHE2 PROTEIN, S CEREVISIAE; SHE4 PROTEIN, S CEREVISIAE; SWI5 PROTEIN, S CEREVISIAE; TRANSCRIPTION FACTOR;

DIMERIZATION; GENETICS; METABOLISM; PHYSIOLOGY; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CYTOSKELETAL PROTEINS; DIMERIZATION; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; RNA TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84897920994     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201302095     Document Type: Article

References (58)

1. Amrute-Nayak, M., and S.L. Bullock. 2012. Single-molecule assays reveal that RNA localization signals regulate dynein-dynactin copy number on individual transcript cargoes. Nat. Cell Biol. 14:416-423. http://dx.doi.org/10.1038/ncb2446
2. Aronov, S., R. Gelin-Licht, G. Zipor, L. Haim, E. Safran, and J.E. Gerst. 2007. mRNAs encoding polarity and exocytosis factors are cotransported with the cortical endoplasmic reticulum to the incipient bud in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:3441-3455. http://dx.doi.org/10.1128/MCB.01643-06
3. Beach, D.L., E.D. Salmon, and K. Bloom. 1999. Localization and anchoring of mRNA in budding yeast. Curr. Biol. 9:569-578. http://dx.doi.org/10.1016/S0960-9822(99)80260-7
4. Berger, I., D.J. Fitzgerald, and T.J. Richmond. 2004. Baculovirus expression system for heterologous multiprotein complexes. Nat. Biotechnol. 22:1583-1587. http://dx.doi.org/10.1038/nbt1036
5. 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
6. Besse, F., S. López de Quinto, V. Marchand, A. Trucco, and A. Ephrussi. 2009. Drosophila PTB promotes formation of high-order RNP particles and represses oskar translation. Genes Dev. 23:195-207. http://dx.doi.org/10.1101/gad.505709
7. Bobola, N., R.P. Jansen, T.H. Shin, and K. Nasmyth. 1996. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell. 84:699-709. http://dx.doi.org/10.1016/S0092-8674(00)81048-X0114
8. Böhl, F., C. Kruse, A. Frank, D. Ferring, and R.P. Jansen. 2000. She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p. EMBO J. 19:5514-5524. http://dx.doi.org/10.1093/emboj/19.20.5514
9. 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
10. Chartrand, P., X.H. Meng, R.H. Singer, and R.M. Long. 1999. Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo. Curr. Biol. 9:333-336. http://dx.doi.org/10.1016/S0960-9822(99)80144-4
11. Chartrand, P., X.H. Meng, S. Hüttelmaier, D. Donato, and R.H. Singer. 2002. Asymmetric sorting of ash1p in yeast results from inhibition of translation by localization elements in the mRNA. Mol. Cell. 10:1319-1330. http://dx.doi.org/10.1016/S1097-2765(02)00694-9
12. 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
13. 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
14. 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
15. Edelmann, F.T., A. Niedner, and D. Niessing. 2013. Production of pure and functional RNA for in vitro reconstitution experiments. Methods.
16. Ghaemmaghami, S., W.K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O’Shea, and J.S. Weissman. 2003. Global analysis of protein expression in yeast. Nature. 425:737-741. http://dx.doi.org/10.1038/nature02046
17. Gonzalez, I., S.B. Buonomo, K. Nasmyth, and U. von Ahsen. 1999. ASH1 mRNA localization in yeast involves multiple secondary structural elements and Ash1 protein translation. Curr. Biol. 9:337-340. http://dx.doi.org/10.1016/S0960-9822(99)80145-6
18. Graebsch, A., S. Roche, and D. Niessing. 2009. X-ray structure of Pur-alpha reveals a Whirly-like fold and an unusual nucleic-acid binding surface. Proc. Natl. Acad. Sci. USA. 106:18521-18526. http://dx.doi.org/10.1073/pnas.0907990106
19. Haim, L., G. Zipor, S. Aronov, and J.E. Gerst. 2007. A genomic integration method to visualize localization of endogenous mRNAs in living yeast. Nat. Methods. 4:409-412.
20. Heuck, A., T.G. Du, S. Jellbauer, K. Richter, C. Kruse, S. Jaklin, M. Müller, J. Buchner, R.P. Jansen, and D. Niessing. 2007. Monomeric myosin V uses two binding regions for the assembly of stable translocation complexes. Proc. Natl. Acad. Sci. USA. 104:19778-19783. http://dx.doi.org/10.1073/pnas.0706780104
21. 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
22. Heym, R.G., and D. Niessing. 2012. Principles of mRNA transport in yeast. Cell. Mol. Life Sci. 69:1843-1853. http://dx.doi.org/10.1007/s00018-011-0902-4
23. 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 singleheaded motor complex. J. Biol. Chem. 283:6906-6914. http://dx.doi.org/10.1074/jbc.M708865200
24. Hogan, D.J., D.P. Riordan, A.P. Gerber, D. Herschlag, and P.O. Brown. 2008. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 6: e255. http://dx.doi.org/10.1371/journal.pbio.0060255
25. 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
26. Jansen, R.P., and D. Niessing. 2012. Assembly of mRNA-protein complexes for directional mRNA transport in eukaryotes-an overview. Curr. Protein Pept. Sci. 13:284-293. http://dx.doi.org/10.2174/138920312801619493
27. Jansen, R.P., C. Dowzer, C. Michaelis, M. Galova, and K. Nasmyth. 1996. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Cell. 84:687-697. http://dx.doi.org/10.1016/S0092-8674(00)81047-8
28. Krementsova, E.B., A.R. Hodges, C.S. Bookwalter, T.E. Sladewski, M. Travaglia, H.L. Sweeney, and K.M. Trybus. 2011. Two single-headed myosin V motors bound to a tetrameric adapter protein form a processive complex. J. Cell Biol. 195:631-641. http://dx.doi.org/10.1083/jcb.201106146
29. Kruse, C., A. Jaedicke, J. Beaudouin, F. Böhl, D. Ferring, T. Güttler, J. Ellenberg, and R.P. Jansen. 2002. Ribonucleoprotein-dependent localization of the yeast class V myosin Myo4p. J. Cell Biol. 159:971-982. http://dx.doi.org/10.1083/jcb.200207101
30. 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.x0114
31. Lescoute, A., and E. Westhof. 2006. Topology of three-way junctions in folded RNAs. RNA. 12:83-93. http://dx.doi.org/10.1261/rna.2208106
32. Li, J.F., and A. Nebenführ. 2008. The tail that wags the dog: the globular tail domain defines the function of myosin V/XI. Traffic. 9:290-298. http://dx.doi.org/10.1111/j.1600-0854.2007.00687.x
33. 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
34. Long, R.M., W. Gu, E. Lorimer, R.H. Singer, and P. Chartrand. 2000. She2p is a novel RNA-binding protein that recruits the Myo4p-She3p complex to ASH1 mRNA. EMBO J. 19:6592-6601. http://dx.doi.org/10.1093/emboj/19.23.6592
35. Marchand, V., I. Gaspar, and A. Ephrussi. 2012. An intracellular transmission control protocol: assembly and transport of ribonucleoprotein complexes. Curr. Opin. Cell Biol. 24:202-210. http://dx.doi.org/10.1016/j.ceb.2011.12.014
36. Martin, K.C., and A. Ephrussi. 2009. mRNA localization: gene expression in the spatial dimension. Cell. 136:719-730. http://dx.doi.org/10.1016/j.cell.2009.01.044
37. Meeusen, R.L., and W.Z. Cande. 1979. N-ethylmaleimide-modified heavy meromyosin. A probe for actomyosin interactions. J. Cell Biol. 82:57-65. http://dx.doi.org/10.1083/jcb.82.1.57
38. Miura, F., N. Kawaguchi, M. Yoshida, C. Uematsu, K. Kito, Y. Sakaki, and T. Ito. 2008. Absolute quantification of the budding yeast transcriptome by means of competitive PCR between genomic and complementary DNAs. BMC Genomics. 9:574. http://dx.doi.org/10.1186/1471-2164-9-574
39. 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
40. 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
41. Nagalakshmi, U., Z. Wang, K. Waern, C. Shou, D. Raha, M. Gerstein, and M. Snyder. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science. 320:1344-1349. http://dx.doi.org/10.1126/science.1158441
42. 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
43. Oeffinger, M., K.E. Wei, R. Rogers, J.A. DeGrasse, B.T. Chait, J.D. Aitchison, and M.P. Rout. 2007. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods. 4:951-956. http://dx.doi.org/10.1038/nmeth1101
44. Olivier, C., G. Poirier, P. Gendron, A. Boisgontier, F. Major, and P. Chartrand. 2005. Identification of a conserved RNA motif essential for She2p recognition and mRNA localization to the yeast bud. Mol. Cell. Biol. 25:4752-4766. http://dx.doi.org/10.1128/MCB.25.11.4752-4766.2005
45. Pelechano, V., S. Chávez, and J.E. Pérez-Ortín. 2010. A complete set of nascent transcription rates for yeast genes. PLoS ONE. 5: e15442. http://dx.doi.org/10.1371/journal.pone.0015442
46. Ponchon, L., and F. Dardel. 2007. Recombinant RNA technology: the tRNA scaffold. Nat. Methods. 4:571-576. http://dx.doi.org/10.1038/nmeth1058
47. Ponchon, L., G. Beauvais, S. Nonin-Lecomte, and F. Dardel. 2009. A generic protocol for the expression and purification of recombinant RNA in Escherichia coli using a tRNA scaffold. Nat. Protoc. 4:947-959. http://dx.doi.org/10.1038/nprot.2009.67
48. Rambo, R.P., and J.A. Doudna. 2004. Assembly of an active group II intronmaturase complex by protein dimerization. Biochemistry. 43:6486-6497. http://dx.doi.org/10.1021/bi049912u0114
49. 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
50. Shen, Z., A. St-Denis, and P. Chartrand. 2010. Cotranscriptional recruitment of She2p by RNA pol II elongation factor Spt4-Spt5/DSIF promotes mRNA localization to the yeast bud. Genes Dev. 24:1914-1926. http://dx.doi.org/10.1101/gad.1937510
51. 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
52. Sil, A., and I. Herskowitz. 1996. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HOgene. Cell. 84:711-722. http://dx.doi.org/10.1016/S0092-8674(00)81049-1
53. Sladewski, T.E., C.S. Bookwalter, M.S. Hong, and K.M. Trybus. 2013. Singlemolecule reconstitution of mRNA transport by a class V myosin. Nat. Struct. Mol. Biol. 20:952-957. http://dx.doi.org/10.1038/nsmb.2614
54. Spudich, J.A., and S. Watt. 1971. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosintroponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246:4866-4871.
55. 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
56. Takizawa, P.A., J.L. DeRisi, J.E. Wilhelm, and R.D. Vale. 2000. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science. 290:341-344. http://dx.doi.org/10.1126/science.290.5490.341
57. Trcek, T., J.A. Chao, D.R. Larson, H.Y. Park, D. Zenklusen, S.M. Shenoy, and R.H. Singer. 2012. Single-mRNA counting using fluorescent in situ hybridization in budding yeast. Nat. Protoc. 7:408-419. http://dx.doi.org/10.1038/nprot.2011.451
58. Trybus, K.M. 2008. Myosin V from head to tail. Cell. Mol. Life Sci. 65:1378-1389. http://dx.doi.org/10.1007/s00018-008-7507-6