A structural analysis of the AAA+ domains in Saccharomyces cerevisiae cytoplasmic dynein

Journal of Structural Biology

Volumn 186, Issue 3, 2014, Pages 367-375

  Gleave, Emma S ^a   Schmidt, Helgo ^a   Carter, Andrew P ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Coiled coil; Cytoskeleton; Dynein; Microtubule; Motor protein

Indexed keywords

CYTOPLASMIC DYNEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DICTYOSTELIUM DISCOIDEUM; MICROTUBULE; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CYTOPLASMIC DYNEINS; EVOLUTION, MOLECULAR; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84901603352     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2014.03.019     Document Type: Article

References (55)

1. Alva V., Ammelburg M., Söding J., Lupas A.N. On the origin of the histone fold. BMC Struct. Biol. 2007, 7:17.
2. Ammelburg M., Frickey T., Lupas A.N. Classification of AAA+ proteins. J. Struct. Biol. 2006, 156:2-11.
3. Asai D.J., Koonce M.P. The dynein heavy chain: structure, mechanics and evolution. Trends Cell Biol. 2001, 11:196-202.
4. Babst M., Wendland B., Estepa E.J., Emr S.D. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 1998, 17:2982-2993.
5. Baumeister W., Lupas A. The proteasome. Curr. Opin. Struct. Biol. 1997, 7:273-278.
6. Buck M., Gallegos M.T., Studholme D.J., Guo Y., Gralla J.D. The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J. Bacteriol. 2000, 182:4129-4136.
7. Burgess S.A., Walker M.L., Sakakibara H., Knight P.J., Oiwa K. Dynein structure and power stroke. Nature 2003, 421:715-718.
8. Burgess S.A., Walker M.L., Sakakibara H., Oiwa K., Knight P.J. The structure of dynein-c by negative stain electron microscopy. J. Struct. Biol. 2004, 146:205-216.
9. Carter A.P. Crystal clear insights into how the dynein motor moves. J. Cell Sci. 2013, 126:705-713.
10. Carter A.P., Cho C., Jin L., Vale R.D. Crystal structure of the dynein motor domain. Science 2011, 331:1159-1165.
11. Chen B., Sysoeva T.A., Chowdhury S., Guo L., De Carlo S., Hanson J.A., Yang H., Nixon B.T. Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA+ ATPase for remodeling bacterial RNA polymerase. Structure 2010, 18:1420-1430.
12. Cho C., Vale R.D. The mechanism of dynein motility: insight from crystal structures of the motor domain. Biochim. Biophys. Acta 2012, 1823:182-191.
13. DiBella L.M., King S.M. Dynein motors of the Chlamydomonas flagellum. Int. Rev. Cytol. 2001, 210:227-268.
14. El Bakkouri M., Gutsche I., Kanjee U., Zhao B., Yu M., Goret G., Schoehn G., Burmeister W.P., Houry W.A. Structure of RavA MoxR AAA+ protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity. Proc. Natl. Acad. Sci. USA 2010, 107:22499-22504.
15. Erzberger J.P., Berger J.M. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:93-114.
16. Garbarino J.E., Gibbons I.R. Expression and genomic analysis of midasin, a novel and highly conserved AAA protein distantly related to dynein. BMC Genomics 2002, 3:18.
17. Gee M.A., Heuser J.E., Vallee R.B. An extended microtubule-binding structure within the dynein motor domain. Nature 1997, 390:636-639.
18. Gibbons I.R. Dynein family of motor proteins: present status and future questions. Cell Motil. Cytoskel. 1995, 32:136-144.
19. Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symposium Series No. 41, pp. 95-98.
20. Huang J., Roberts A.J., Leschziner A.E., Reck-Peterson S.L. Lis1 acts as a "clutch" between the ATPase and microtubule-binding domains of the dynein motor. Cell 2012, 150:975-986.
21. Iyer L.M., Leipe D.D., Koonin E.V., Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 2004, 146:11-31.
22. Karata K., Inagawa T., Wilkinson A.J., Tatsuta T., Ogura T. Dissecting the role of a conserved motif (the second region of homology) in the AAA family of ATPases. Site-directed mutagenesis of the ATP-dependent protease FtsH. J. Biol. Chem. 1999, 274:26225-26232.
23. Kardon J.R., Vale R.D. Regulators of the cytoplasmic dynein motor. Nat. Rev. Mol. Cell Biol. 2009, 10:854-865.
24. Kon T., Kurisu G. Structure and mechanism of cytoplasmic dynein. Seikagaku 2013, 85:272-275.
25. Kon T., Nishiura M., Ohkura R., Toyoshima Y.Y., Sutoh K. Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein. Biochemistry 2004, 43:11266-11274.
26. Kon T., Sutoh K., Kurisu G. X-ray structure of a functional full-length dynein motor domain. Nat. Struct. Mol. Biol. 2011, 18:638-642.
27. Kon T., Oyama T., Shimo-Kon R., Imamula K., Shima T., Sutoh K., Kurisu G. The 2.8Å crystal structure of the dynein motor domain. Nature 2012, 484:345-350.
28. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
29. Lee S.Y., De La Torre A., Yan D., Kustu S., Nixon B.T., Wemmer D.E. Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev. 2003, 17:2552-2563.
30. Lundqvist J., Elmlund H., Wulff R.P., Berglund L., Elmlund D., Emanuelsson C., Hebert H., Willows R.D., Hansson M., Lindahl M., Al-Karadaghi S. ATP-induced conformational dynamics in the AAA+ motor unit of magnesium chelatase. Structure 2010, 18:354-365.
31. Lupas A.N., Martin J. AAA proteins. Curr. Opin. Struct. Biol. 2002, 12:746-753.
32. Lye R.J., Porter M.E., Scholey J.M., McIntosh J.R. Identification of a microtubule-based cytoplasmic motor in the nematode C. elegans. Cell 1987, 51:309-318.
33. McNally F.J., Vale R.D. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 1993, 75:419-429.
34. Mizuno N., Dramićanin M., Mizuuchi M., Adam J., Wang Y., Han Y.W., Yang W., Steven A.C., Mizuuchi K., Ramón-Maiques S. MuB is an AAA+ ATPase that forms helical filaments to control target selection for DNA transposition. Proc. Natl. Acad. Sci. USA 2013, 110:E2441-E2450.
35. Neuwald A.F. Evolutionary clues to eukaryotic DNA clamp-loading mechanisms: analysis of the functional constraints imposed on replication factor C AAA+ ATPases. Nucleic Acids Res. 2005, 33:3614-3628.
36. Numata N., Shima T., Ohkura R., Kon T., Sutoh K. C-sequence of the Dictyostelium cytoplasmic dynein participates in processivity modulation. FEBS Lett. 2011, 585:1185-1190.
37. Piperno G., Ramanis Z., Smith E.F., Sale W.S. Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J. Cell Biol. 1990, 110:379-389.
38. Rappas M., Schumacher J., Niwa H., Buck M., Zhang X. Structural basis of the nucleotide driven conformational changes in the AAA+ domain of transcription activator PspF. J. Mol. Biol. 2006, 357:481-492.
39. Roberts E., Eargle J., Wright D., Luthey-Schulten Z. MultiSeq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 2006, 7:382.
40. Roberts A.J., Malkova B., Walker M.L., Sakakibara H., Numata N., Kon T., Ohkura R., Edwards T.A., Knight P.J., Sutoh K., Oiwa K., Burgess S.A. ATP-driven remodeling of the linker domain in the dynein motor. Structure 2012, 20:1670-1680.
41. Roberts A.J., Kon T., Knight P.J., Sutoh K., Burgess S.A. Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol. 2013, 14:713-726.
42. Schmidt H., Gleave E.S., Carter A.P. Insights into dynein motor domain function from a 3.3-Å crystal structure. Nat. Struct. Mol. Biol. 2012, 19:492-497. S491.
43. Schrodinger, LLC. 2010. The PyMOL molecular graphics system, Version 1.3 r1.
44. Siddiqui S.M., Sauer R.T., Baker T.A. Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates. Genes Dev. 2004, 18:369-374.
45. Simonetta K.R., Kazmirski S.L., Goedken E.R., Cantor A.J., Kelch B.A., McNally R., Seyedin S.N., Makino D.L., O'Donnell M., Kuriyan J. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 2009, 137:659-671.
46. Singleton M.R., Dillingham M.S., Wigley D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 2007, 76:23-50.
47. Slaymaker I.M., Fu Y., Toso D.B., Ranatunga N., Brewster A., Forsburg S.L., Zhou Z.H., Chen X.S. Mini-chromosome maintenance complexes form a filament to remodel DNA structure and topology. Nucleic Acids Res. 2013, 41:3446-3456.
48. Studholme D.J., Dixon R. Domain architectures of sigma54-dependent transcriptional activators. J. Bacteriol. 2003, 185:1757-1767.
49. Vallee R.B., Williams J.C., Varma D., Barnhart L.E. Dynein: an ancient motor protein involved in multiple modes of transport. J. Neurobiol. 2004, 58:189-200.
50. Vaughan K.T. Roles of cytoplasmic dynein during mitosis. Dyneins: Structure, Biology and Disease 2012, 523. Academic Press, Amsterdam, Boston. S.J. King (Ed.).
51. Waterhouse A.M., Procter J.B., Martin D.M., Clamp M., Barton G.J. Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191.
52. Wendler P., Ciniawsky S., Kock M., Kube S. Structure and function of the AAA+ nucleotide binding pocket. Biochim. Biophys. Acta 2012, 1823:2-14.
53. Wickstead B., Gull K. Dyneins across eukaryotes: a comparative genomic analysis. Traffic 2007, 8:1708-1721.
54. Wilkes D.E., Watson H.E., Mitchell D.R., Asai D.J. Twenty-five dyneins in Tetrahymena: a re-examination of the multidynein hypothesis. Cell Motil. Cytoskel. 2008, 65:342-351.
55. Zhang X., Wigley D.B. The 'glutamate switch' provides a link between ATPase activity and ligand binding in AAA+ proteins. Nat. Struct. Mol. Biol. 2008, 15:1223-1227.