Myo2p, a class V myosin in budding yeast, associates with a large ribonucleic acid-protein complex that contains mRNAs and subunits of the RNA-processing body

RNA

Volumn 14, Issue 3, 2008, Pages 491-502

  Chang, Wakam ^a,b   Zaarour, Rania F ^a,b,d   Reck Peterson, Samara ^a,b,e   Rinn, John ^a,f   Singer, Robert H ^c   Snyder, Michael ^a   Novick, Peter ^b   Mooseker, Mark S ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d INSTITUT CURIE   (France)

^e HARVARD MEDICAL SCHOOL   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Myosin V; P body; RNP; Saccharomyces cerevisiae; Unconventional myosin

Indexed keywords

MESSENGER RNA; MYO2P; MYOSIN; UNCLASSIFIED DRUG; ACTIN; ADENOSINE TRIPHOSPHATASE; FUNGAL RNA; MYO2 PROTEIN, S CEREVISIAE; MYO4 PROTEIN, S CEREVISIAE; MYOSIN HEAVY CHAIN; MYOSIN V; PRIMER DNA; RIBONUCLEOPROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ANALYSIS; ARTICLE; BUDDING; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA PROCESSING; SEDIMENTATION; YEAST; CELL ORGANELLE; CELL VACUOLE; CHEMISTRY; DNA MICROARRAY; GENETICS; MACROMOLECULE; METABOLISM; NUCLEOTIDE SEQUENCE; POLYSOME; SACCHAROMYCES CEREVISIAE; SECRETORY VESICLE;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

ACTINS; ADENOSINE TRIPHOSPHATASES; BASE SEQUENCE; DNA PRIMERS; MACROMOLECULAR SUBSTANCES; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGANELLES; POLYRIBOSOMES; RIBONUCLEOPROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SECRETORY VESICLES; VACUOLES;

EID: 40449140744     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.665008     Document Type: Article

References (47)

1. Anderson, P. and Kedersha, N. 2006. RNA granules. J. Cell Biol. 172: 803-808.
2. Barbee, S.A., Estes, P.S., Cziko, A.M., Hillebrand, J., Luedeman, R.A., Coller, J.M., Johnson, N., Howlett, I.C., Geng, C., Ueda, R., et al. 2006. Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52: 997-1009.
3. Beggs, J.D. 2005. Lsm proteins and RNA processing. Biochem. Soc. Trans. 33: 433-438.
4. Boldogh, I.R., Ramcharan, S.L., Yang, H.C., and Pon, L.A. 2004. A Type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division. Mol. Biol. Cell 15: 3994-4002.
5. Brengues, M., Teixeira, D., and Parker, R. 2005. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489.
6. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. 99: 7877-7882.
7. Catlett, N.L. and Weisman, L.S. 1998. The terminal tail region of a yeast myosin-V mediates its attachment to vacuole membranes and sites of polarized growth. Proc. Natl. Acad. Sci. 95: 14799-14804.
8. Coller, J. and Parker, R. 2004. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73: 861-890.
9. Coller, J. and Parker, R. 2005. General translational repression by activators of mRNA decapping. Cell 122: 875-886.
10. Estrada, P., Kim, J., Coleman, J., Walker, L., Dunn, B., Takizawa, P., Novick, P., and Ferro-Novick, S. 2003. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163: 1255-1266.
11. Fagarasanu, A., Fagarasanu, M., Eitzen, G.A., Aitchison, J.D., and Rachubinski, R.A. 2006. The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae. Dev. Cell 10: 587-600.
12. Gavin, A.C., Bosche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J.M., Michon, A.M., Cruciat, C.M., et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141-147.
13. Ghaemmaghami, S., Huh, W.K., Bower, K., Howson, R.W., Belle, A., Dephoure, N., O'Shea, E.K., and Weissman, J.S. 2003. Global analysis of protein expression in yeast. Nature 425: 737-741.
14. Gill, T., Aulds, J., and Schmitt, M.E. 2006. A specialized processing body that is temporally and asymmetrically regulated during the cell cycle in Saccharomyces cerevisiae. J. Cell Biol. 173: 35-45.
15. Gonsalvez, G.B., Urbinati, C.R., and Long, R.M. 2005. RNA localization in yeast: Moving towards a mechanism. Biol. Cell. 97: 75-86.
16. Govindan, B., Bowser, R., and Novick, P. 1995. The role of Myo2, a yeast class-V myosin, in vesicular transport. J. Cell Biol. 128: 1055-1068.
17. Gundersen, G.G. and Bretscher, A. 2003. Cell biology: Microtubule asymmetry. Science 300: 2040-2041.
18. Hanson, J. 1973. Evidence from electron microscope studies on actin paracrystals concerning the origin of the cross-striation in the thin filaments of vertebrate skeletal muscle. Proc. R. Soc. Lond. B. Biol. Sci. 183: 39-58.
19. Hill, K.L., Catlett, N.L., and Weisman, L.S. 1996. Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae. J. Cell Biol. 135: 1535-1549.
20. Hoepfner, D., van den Berg, M., Philippsen, P., Tabak, H.F., and Hettema, E.H. 2001. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155: 979-990.
21. Itoh, T., Watabe, A., Toh, E.A., and Matsui, Y. 2002. Complex formation with Ypt11p, a rab-type small GTPase, is essential to facilitate the function of Myo2p, a class V myosin, in mitochondrial distribution in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 7744-7757.
22. Itoh, T., Toh, E.A., and Matsui, Y. 2004. Mmr1p is a mitochondrial factor for Myo2p-dependent inheritance of mitochondria in the budding yeast. EMBO J. 23: 2520-2530.
23. Jang, L.T., Buu, L.M., and Lee, F.J. 2006. Determinants of Rbp1p localization in specific cytoplasmic mRNA-processing foci, P-bodies. J. Biol. Chem. 281: 29379-29390.
24. Johnston, G.C., Prendergast, J.A., and Singer, R.A. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113: 539-551.
25. Long, R.M., Singer, R.H., Meng, X., Gonzalez, I., Nasmyth, K., and Jansen, R.P. 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277: 383-387.
26. Long, R.M., Gu, W., Lorimer, E., Singer, R.H., and Chartrand, P. 2000. She2p is a novel RNA-binding protein that recruits the Myo4p-She3p complex to ASH1 mRNA. EMBO J. 19: 6592-6601.
27. Longtine, M.S., McKenzie III., A., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J.R. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
28. Mangus, D.A. and Jacobson, A. 1999. Linking mRNA turnover and translation: Assessing the polyribosomal association of mRNA decay factors and degradative intermediates. Methods 17: 28-37.
29. Nelson, R.J., Ziegelhoffer, T., Nicolet, C., Werner-Washburne, M., and Craig, E.A. 1992. The translation machinery and 70 kDa heat shock protein cooperate in protein synthesis. Cell 71: 97-105.
30. Ohashi, S., Koike, K., Omori, A., Ichinose, S., Ohara, S., Kobayashi, S., Sato, T.A., and Anzai, K. 2002. Identification of mRNA/protein (mRNP) complexes containing Puralpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor. J. Biol. Chem. 277: 37804-37810.
31. Parker, R. and Sheth, U. 2007. P bodies and the control of mRNA translation and degradation. Mol. Cell 25: 635-646.
32. Pruyne, D.W., Schott, D.H., and Bretscher, A. 1998. Tropomyosin- containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143: 1931-1945.
33. Reck-Peterson, S.L., Novick, P.J., and Mooseker, M.S. 1999. The tail of a yeast class V myosin, Myo2p, functions as a localization domain. Mol. Biol. Cell 10: 1001-1017.
34. Reck-Peterson, S.L., Tyska, M.J., Novick, P.J., and Mooseker, M.S. 2001. The yeast class V myosins, Myo2p and Myo4p, are non-processive actin-based motors. J. Cell Biol. 153: 1121-1126.
35. Rossanese, O.W., Reinke, C.A., Bevis, B.J., Hammond, A.T., Sears, I.B., O'Connor, J., and Glick, B.S. 2001. A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J. Cell Biol. 153: 47-62.
36. Rossi, G., Salminen, A., Rice, L.M., Brunger, A.T., and Brennwald, P. 1997. Analysis of a yeast SNARE complex reveals remarkable similarity to the neuronal SNARE complex and a novel function for the C terminus of the SNAP-25 homolog, Sec9. J. Biol. Chem. 272: 16610-16617.
37. Shepard, K.A., Gerber, A.P., Jambhekar, A., Takizawa, P.A., Brown, P.O., Herschlag, D., DeRisi, J.L., and Vale, R.D. 2003. Widespread cytoplasmic mRNA transport in yeast: Identification of 22 bud-localized transcripts using DNA microarray analysis. Proc. Natl. Acad. Sci. 100: 11429-11434.
38. Sotelo-Silveira, J.R., Calliari, A., Cardenas, M., Koenig, E., and Sotelo, J.R. 2004. Myosin Va and kinesin II motor proteins are concentrated in ribosomal domains (periaxoplasmic ribosomal plaques) of myelinated axons. J. Neurobiol. 60: 187-196.
39. Sotelo-Silveira, J.R., Calliari, A., Kun, A., Koenig, E., and Sotelo, J.R. 2006. RNA trafficking in axons. Traffic 7: 508-515.
40. Takizawa, P.A. and Vale, R.D. 2000. The myosin motor, Myo4p, binds Ash1 mRNA via the adapter protein, She3p. Proc. Natl. Acad. Sci. 97: 5273-5278.
41. Takizawa, P.A., Sil, A., Swedlow, J.R., Herskowitz, I., and Vale, R.D. 1997. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389: 90-93.
42. Takizawa, P.A., DeRisi, J.L., Wilhelm, J.E., and Vale, R.D. 2000. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290: 341-344.
43. Teixeira, D. and Parker, R. 2007. Analysis of P-body assembly in Saccharomyces cerevisiae. 18: 2274-2287.
44. Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M., and Parker, R. 2005. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11: 371-382.
45. Thomas, M.G., Martinez Tosar, L.J., Loschi, M., Pasquini, J.M., Correale, J., Kindler, S., and Boccaccio, G.L. 2005. Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Mol. Biol. Cell 16: 405-420.
46. Wettstein, F.O., Noll, H., and Penman, S. 1964. Effect of cycloheximide on ribosomal aggregates engaged in protein synthesis in vitro. Biochim. Biophys. Acta 87: 525-528.
47. Yoshimura, A., Fujii, R., Watanabe, Y., Okabe, S., Fukui, K., and Takumi, T. 2006. Myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr. Biol. 16: 2345-2351.