Structure of a myosin•adaptor complex and pairing by cargo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 12, 2014, Pages

  Shi, Hang ^a   Singh, Nimisha ^a   Esselborn, Filipp ^a,b   Blobel, Günter ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Cytoplasmic mRNA localization; Endoplasmic reticulum inheritance; In vitro assembly

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; MYOSIN; MYOSIN 4 PROTEIN; OLIGONUCLEOTIDE; TETRAMER; UNCLASSIFIED DRUG; ZIPCODE BINDING PROTEIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CROSS LINKING; CRYSTAL STRUCTURE; DIMERIZATION; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STOICHIOMETRY;

CYTOPLASMIC MRNA LOCALIZATION; ENDOPLASMIC RETICULUM INHERITANCE; IN VITRO ASSEMBLY;

CRYSTALLOGRAPHY, X-RAY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MUTATION; MYOSIN TYPE IV; PROTEIN CONFORMATION; RIBONUCLEOPROTEINS;

EID: 84896910704     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401428111     Document Type: Article

References (51)

1. Blower MD (2013) Molecular insights into intracellular RNA localization. Int Rev Cell Mol Biol 302:1-39.
2. Holt CE, Bullock SL (2009) Subcellular mRNA localization in animal cells and why it matters. Science 326(5957):1212-1216.
3. Shepard KA, et al. (2003) Widespread cytoplasmic mRNA transport in yeast: Identification of 22 bud-localized transcripts using DNA microarray analysis. Proc Natl Acad Sci USA 100(20):11429-11434. (Pubitemid 37205952)
4. Takizawa PA, Sil A, Swedlow JR, Herskowitz I, Vale RD (1997) Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389(6646):90-93. (Pubitemid 27387697)
5. Bertrand E, et al. (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2(4):437-445. (Pubitemid 128381296)
6. Long RM, et al. (1997) Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277(5324):383-387. (Pubitemid 27450713)
7. Gonzalez I, Buonomo SB, Nasmyth K, von Ahsen U (1999) ASH1 mRNA localization in yeast involves multiple secondary structural elements and Ash1 protein translation. Curr Biol 9(6):337-340. (Pubitemid 29181843)
8. Chartrand P, Meng XH, Huttelmaier S, Donato D, Singer RH (2002) Asymmetric sorting of ash1p in yeast results from inhibition of translation by localization elements in the mRNA. Mol Cell 10(6):1319-1330. (Pubitemid 36050874)
9. Jambhekar A, et al. (2005) Unbiased selection of localization elements reveals cis-acting determinants of mRNA bud localization in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102(50):18005-18010. (Pubitemid 41798492)
10. Olivier C, et al. (2005) Identification of a conserved RNA motif essential for She2p recognition and mRNA localization to the yeast bud. Mol Cell Biol 25(11):4752-4766. (Pubitemid 40705777)
11. Jansen RP, Dowzer C, Michaelis C, Galova M, Nasmyth K (1996) Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Cell 84(5):687-697. (Pubitemid 26094199)
12. Niessing D, Hüttelmaier S, Zenklusen D, Singer RH, Burley SK (2004) She2p is a novel RNA binding protein with a basic helical hairpin motif. Cell 119(4):491-502. (Pubitemid 39482349)
13. Krementsova EB, et al. (2011) Two single-headed myosin V motors bound to a tetrameric adapter protein form a processive complex. J Cell Biol 195(4):631-641.
14. Müller M, et al. (2009) Formation of She2p tetramers is required for mRNA binding, mRNP assembly, and localization. RNA 15(11):2002-2012.
15. Gonsalvez GB, et al. (2003) RNA-protein interactions promote asymmetric sorting of the ASH1 mRNA ribonucleoprotein complex. RNA 9(11):1383-1399. (Pubitemid 37310869)
16. Hodges AR, Krementsova EB, Trybus KM (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(11):6906-6914.
17. Heuck A, et al. (2010) The structure of the Myo4p globular tail and its function in ASH1 mRNA localization. J Cell Biol 189(3):497-510.
18. Shi H, Blobel G (2010) UNC-45/CRO1/She4p (UCS) protein forms elongated dimer and joins two myosin heads near their actin binding region. Proc Natl Acad Sci USA 107(50):21382-21387.
19. Shen Z, St-Denis A, Chartrand P (2010) Cotranscriptional recruitment of She2p by RNA pol II elongation factor Spt4-Spt5/DSIF promotes mRNA localization to the yeast bud. Genes Dev 24(17):1914- 1926.
20. Napetschnig J, et al. (2009) Structural and functional analysis of the interaction between the nucleoporin Nup214 and the DEAD-box helicase Ddx19. Proc Natl Acad Sci USA 106(9):3089-3094.
21. Long RM, Gu W, Lorimer E, Singer RH, Chartrand P (2000) She2p is a novel RNA-binding protein that recruits the Myo4p-She3p complex to ASH1 mRNA. EMBO J 19(23):6592-6601.
22. Takizawa PA, Vale RD (2000) The myosin motor, Myo4p, binds Ash1 mRNA via the adapter protein, She3p. Proc Natl Acad Sci USA 97(10):5273-5278. (Pubitemid 30313708)
23. Bookwalter CS, Lord M, Trybus KM (2009) Essential features of the class V myosin from budding yeast for ASH1 mRNA transport. Mol Biol Cell 20(14):3414-3421.
24. Hodges AR, Bookwalter CS, Krementsova EB, Trybus KM (2009) A nonprocessive class V myosin drives cargo processively when a kinesin- related protein is a passenger. Curr Biol 19(24):2121-2125.
25. Müller M, et al. (2011) A cytoplasmic complex mediates specific mRNA recognition and localization in yeast. PLoS Biol 9(4):e1000611.
26. Sladewski TE, Bookwalter CS, Hong MS, Trybus KM (2013) Single-molecule reconstitution of mRNA transport by a class V myosin. Nat Struct Mol Biol 20(8):952-957.
27. Genz C, Fundakowski J, Hermesh O, Schmid M, Jansen RP (2013) Association of the yeast RNA-binding protein She2p with the tubular endoplasmic reticulum depends on membrane curvature. J Biol Chem 288(45):32384-32393.
28. Aronov S, et al. (2007) mRNAs encoding polarity and exocytosis factors are co-transported with the cortical endoplasmic reticulum to the incipient bud in Saccharomyces cerevisiae. Mol Cell Biol 27(9):3441-3455. (Pubitemid 46685219)
29. Estrada P, et al. (2003) Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J Cell Biol 163(6):1255-1266. (Pubitemid 38032087)
30. Landers SM, Gallas MR, Little J, Long RM (2009) She3p possesses a novel activity required for ASH1 mRNA localization in Saccharomyces cerevisiae. Eukaryot Cell 8(7):1072-1083.
31. Böhl F, Kruse C, Frank A, Ferring D, Jansen RP (2000) She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p. EMBO J 19(20):5514-5524.
32. Schmid M, Jaedicke A, Du TG, Jansen RP (2006) Coordination of endoplasmic reticulum and mRNA localization to the yeast bud. Curr Biol 16(15):1538-1543. (Pubitemid 44142979)
33. Heuck A, et al. (2007) Monomeric myosin V uses two binding regions for the assembly of stable translocation complexes. Proc Natl Acad Sci USA 104(50):19778-19783.
34. Chung S, Takizawa PA (2010) Multiple Myo4 motors enhance ASH1 mRNA transport in Saccharomyces cerevisiae. J Cell Biol 189(4):755-767.
35. Kruse C, et al. (2002) Ribonucleoprotein-dependent localization of the yeast class V myosin Myo4p. J Cell Biol 159(6):971-982. (Pubitemid 36055752)
36. Niedner A, Müller M, Moorthy BT, Jansen RP, Niessing D (2013) Role of Loc1p in assembly and reorganization of nuclear ASH1 messenger ribonucleoprotein particles in yeast. Proc Natl Acad Sci USA 110(52):E5049-E5058.
37. Yu C, et al. (2009) Myosin VI undergoes cargo-mediated dimerization. Cell 138(3):537-548.
38. Wu L, Pan L, Wei Z, Zhang M (2011) Structure of MyTH4-FERM domains in myosin VIIa tail bound to cargo. Science 331(6018):757-760.
39. Fundakowski J, Hermesh O, Jansen RP (2012) Localization of a subset of yeast mRNAs depends on inheritance of endoplasmic reticulum. Traffic 13(12):1642-1652.
40. Shi H, Rojas R, Bonifacino JS, Hurley JH (2006) The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat Struct Mol Biol 13(6):540-548. (Pubitemid 43848909)
41. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M (2006) HKL-3000: The integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62(Pt 8):859-866. (Pubitemid 44125661)
42. Terwilliger T (2004) SOLVE and RESOLVE: Automated structure solution, density modification and model building. J Synchrotron Radiat 11(Pt 1):49-52.
43. Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64(Pt 1):112-122.
44. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674. (Pubitemid 47080256)
45. McCoy AJ (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63(Pt 1):32-41.
46. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50(Pt 5):760-763.
47. Brünger AT, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54(Pt 5):905-921.
48. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
49. Schrodinger, LLC (2010) The PyMOL Molecular Graphics System (Schrödinger, LLC, Cambridge, MA), Version 1.3r1.
50. Chen VB, et al. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66(Pt 1):12-21.
51. Knobloch JE, Shaklee PN (1997) Absolute molecular weight distribution of low-molecular-weight heparins by size-exclusion chromatography with multiangle laser light scattering detection. Anal Biochem 245(2):231-241. (Pubitemid 27082256)