Lytic water dynamics reveal evolutionarily conserved mechanisms of ATP hydrolysis by TIP49 AAA+ ATPases

Structure

Volumn 22, Issue 4, 2014, Pages 549-559

  Afanasyeva, Arina ^a,d,g   Hirtreiter, Angela ^b,g   Schreiber, Anne ^b,g   Grohmann, Dina ^c   Pobegalov, Georgii ^a   McKay, Adam R ^b   Tsaneva, Irina ^b   Petukhov, Michael ^a,d   Käs, Emmanuel ^e,f   Grigoriev, Mikhail ^e,f   Werner, Finn ^b  

^a PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^d PETERSBURG NUCLEAR PHYSICS INSTITUTE   (Russian Federation)

^e CNRS   (France)

^f UNIVERSITÉ DE TOULOUSE   (France)

^g INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE TIP 49B; ADENOSINE TRIPHOSPHATASE TIP49A; ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; MONOMER; TRANS ACTING FACTOR; UNCLASSIFIED DRUG; WATER; ARCHAEAL PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; GENETIC CONSERVATION; METHANOPYRUS KANDLERI; MOLECULAR DYNAMICS; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN HYDROLYSIS; SEQUENCE HOMOLOGY; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; EURYARCHAEOTA; EVOLUTION; GENE EXPRESSION; GENETICS; HYDROLYSIS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

ARCHAEA; EUKARYOTA; METHANOPYRUS KANDLERI;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ARCHAEAL PROTEINS; ASPARTIC ACID; BIOLOGICAL EVOLUTION; CONSERVED SEQUENCE; ESCHERICHIA COLI; EURYARCHAEOTA; GENE EXPRESSION; HYDROLYSIS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; WATER;

EID: 84898431978     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.02.002     Document Type: Article

References (50)

1. M. Ammelburg, T. Frickey, and A.N. Lupas Classification of AAA+ proteins J. Struct. Biol. 156 2006 2 11
2. P. Bellosta, T. Hulf, S. Balla Diop, F. Usseglio, J. Pradel, D. Aragnol, and P. Gallant Myc interacts genetically with Tip48/Reptin and Tip49/Pontin to control growth and proliferation during Drosophila development Proc. Natl. Acad. Sci. USA 102 2005 11799 11804
3. J.P. Erzberger, and J.M. Berger Evolutionary relationships and structural mechanisms of AAA+ proteins Annu. Rev. Biophys. Biomol. Struct. 35 2006 93 114
4. C. Etard, D. Gradl, M. Kunz, M. Eilers, and D. Wedlich Pontin and Reptin regulate cell proliferation in early Xenopus embryos in collaboration with c-Myc and Miz-1 Mech. Dev. 122 2005 545 556
5. S. Gorynia, T.M. Bandeiras, F.G. Pinho, C.E. McVey, C. Vonrhein, A. Round, D.I. Svergun, P. Donner, P.M. Matias, and M.A. Carrondo Structural and functional insights into a dodecameric molecular machine - the RuvBL1/RuvBL2 complex J. Struct. Biol. 176 2011 279 291
6. A. Gribun, K.L. Cheung, J. Huen, J. Ortega, and W.A. Houry Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex J. Mol. Biol. 376 2008 1320 1333
7. A. Grigoletto, V. Neaud, N. Allain-Courtois, P. Lestienne, and J. Rosenbaum The ATPase activity of reptin is required for its effects on tumor cell growth and viability in hepatocellular carcinoma. Mol. Cancer Res 11 2013 133 139
8. B.L. Grigorenko, I.A. Kaliman, and A.V. Nemukhin Minimum energy reaction profiles for ATP hydrolysis in myosin J. Mol. Graph. Model. 31 2011 1 4
9. B.L. Grigorenko, A.V. Rogov, I.A. Topol, S.K. Burt, H.M. Martinez, and A.V. Nemukhin Mechanism of the myosin catalyzed hydrolysis of ATP as rationalized by molecular modeling Proc. Natl. Acad. Sci. USA 104 2007 7057 7061
10. B.L. Grigorenko, M.S. Shadrina, I.A. Topol, J.R. Collins, and A.V. Nemukhin Mechanism of the chemical step for the guanosine triphosphate (GTP) hydrolysis catalyzed by elongation factor Tu Biochim. Biophys. Acta 1784 2008 1908 1917
11. A.J. Heck, and R.H. Van Den Heuvel Investigation of intact protein complexes by mass spectrometry Mass Spectrom. Rev. 23 2004 368 389
12. T. Hishida, Y.W. Han, S. Fujimoto, H. Iwasaki, and H. Shinagawa Direct evidence that a conserved arginine in RuvB AAA+ ATPase acts as an allosteric effector for the ATPase activity of the adjacent subunit in a hexamer Proc. Natl. Acad. Sci. USA 101 2004 9573 9577
13. T. Ikura, V.V. Ogryzko, M. Grigoriev, R. Groisman, J. Wang, M. Horikoshi, R. Scully, J. Qin, and Y. Nakatani Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis Cell 102 2000 463 473
14. J. Iqbal, and S.A. Qureshi Selective depletion of Sulfolobus solfataricus transcription factor E under heat shock conditions J. Bacteriol. 192 2010 2887 2891
15. L.M. Iyer, D.D. Leipe, E.V. Koonin, and L. Aravind Evolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol. 146 2004 11 31
16. N. Joly, N. Zhang, and M. Buck ATPase site architecture is required for self-assembly and remodeling activity of a hexameric AAA+ transcriptional activator Mol. Cell 47 2012 484 490
17. Z.O. Jonsson, S.K. Dhar, G.J. Narlikar, R. Auty, N. Wagle, D. Pellman, R.E. Pratt, R. Kingston, and A. Dutta Rvb1p and Rvb2p are essential components of a chromatin remodeling complex that regulates transcription of over 5% of yeast genes J. Biol. Chem. 276 2001 16279 16288
18. T. Kanai, S. Takedomi, S. Fujiwara, H. Atomi, and T. Imanaka Identification of the Phr-dependent heat shock regulon in the hyperthermophilic archaeon, Thermococcus kodakaraensis J. Biochem. 147 2010 361 370
19. J.H. Kim, H.J. Choi, B. Kim, M.H. Kim, J.M. Lee, I.S. Kim, M.H. Lee, S.J. Choi, K.I. Kim, and S.I. Kim et al. Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis Nat. Cell Biol. 8 2006 631 639
20. J.H. Kim, J.M. Lee, H.J. Nam, H.J. Choi, J.W. Yang, J.S. Lee, M.H. Kim, S.I. Kim, C.H. Chung, and K.I. Kim et al. SUMOylation of pontin chromatin-remodeling complex reveals a signal integration code in prostate cancer cells Proc. Natl. Acad. Sci. USA 104 2007 20793 20798
21. A. Lopez-Perrote, H. Munoz-Hernandez, D. Gil, and O. Llorca Conformational transitions regulate the exposure of a DNA-binding domain in the RuvBL1-RuvBL2 complex Nucleic Acids Res. 40 2012 11086 11099
22. R. Machado-Pinilla, D. Liger, N. Leulliot, and U.T. Meier Mechanism of the AAA+ ATPases pontin and reptin in the biogenesis of H/ACA RNPs RNA 18 2012 1833 1845
23. V. Marquez, T. Frohlich, J.P. Armache, D. Sohmen, A. Donhofer, A. Mikolajka, O. Berninghausen, M. Thomm, R. Beckmann, and G.J. Arnold et al. Proteomic characterization of archaeal ribosomes reveals the presence of novel archaeal-specific ribosomal proteins J. Mol. Biol. 405 2011 1215 1232
24. P.M. Matias, S. Gorynia, P. Donner, and M.A. Carrondo Crystal structure of the human AAA+ protein RuvBL1 J. Biol. Chem. 281 2006 38918 38929
25. K.S. McKeegan, C.M. Debieux, and N.J. Watkins Evidence that the AAA+ proteins TIP48 and TIP49 bridge interactions between 15.5K and the related NOP56 and NOP58 proteins during box C/D snoRNP biogenesis Mol. Cell. Biol. 29 2009 4971 4981
26. C. Mezard, A.A. Davies, A. Stasiak, and S.C. West Biochemical properties of RuvBD113N: a mutation in helicase motif II of the RuvB hexamer affects DNA binding and ATPase activities J. Mol. Biol. 271 1997 704 717
27. N. Nano, and W.A. Houry Chaperone-like activity of the AAA+ proteins Rvb1 and Rvb2 in the assembly of various complexes Philos. Trans. R. Soc. Lond. B Biol. Sci. 368 2013 20110399
28. A. Niewiarowski, A.S. Bradley, J. Gor, A.R. McKay, S.J. Perkins, and I.R. Tsaneva Oligomeric assembly and interactions within the human RuvB-like RuvBL1 and RuvBL2 complexes Biochem. J. 429 2010 113 125
29. C.T. Parusel, E.A. Kritikou, M.O. Hengartner, W. Krek, and M. Gotta URI-1 is required for DNA stability in C. elegans Development 133 2006 621 629
30. M. Petukhov, A. Dagkessamanskaja, M. Bommer, T. Barrett, I. Tsaneva, A. Yakimov, R. Queval, A. Shvetsov, M. Khodorkovskiy, and E. Käs et al. Large-scale conformational flexibility determines the properties of AAA+ TIP49 ATPases Structure 20 2012 1321 1331
31. T. Puri, P. Wendler, B. Sigala, H. Saibil, and I.R. Tsaneva Dodecameric structure and ATPase activity of the human TIP48/TIP49 complex J. Mol. Biol. 366 2007 179 192
32. C.D. Putnam, S.B. Clancy, H. Tsuruta, S. Gonzalez, J.G. Wetmur, and J.A. Tainer Structure and mechanism of the RuvB Holliday junction branch migration motor J. Mol. Biol. 311 2001 297 310
33. M. Rappas, J. Schumacher, F. Beuron, H. Niwa, P. Bordes, S. Wigneshweraraj, C.A. Keetch, C.V. Robinson, M. Buck, and X. Zhang Structural insights into the activity of enhancer-binding proteins Science 307 2005 1972 1975
34. J. Rosenbaum, S.H. Baek, A. Dutta, W.A. Houry, O. Huber, T.R. Hupp, and P.M. Matias The Emergence of the Conserved AAA+ ATPases Pontin and Reptin on the Signaling Landscape Sci. Signal. 6 2013 mr1
35. W. Rottbauer, A.J. Saurin, H. Lickert, X. Shen, C.G. Burns, Z.G. Wo, R. Kemler, R. Kingston, C. Wu, and M. Fishman Reptin and pontin antagonistically regulate heart growth in zebrafish embryos Cell 111 2002 661 672
36. B. Rousseau, L. Menard, V. Haurie, D. Taras, J.F. Blanc, F. Moreau-Gaudry, P. Metzler, M. Hugues, S. Boyault, and S. Lemiere et al. Overexpression and role of the ATPase and putative DNA helicase RuvB-like 2 in human hepatocellular carcinoma Hepatology 46 2007 1108 1118
37. T. Schweins, R. Langen, and A. Warshel Why have mutagenesis studies not located the general base in ras p21 Nat. Struct. Biol. 1 1994 476 484
38. A.E. Senior, S. Nadanaciva, and J. Weber The molecular mechanism of ATP synthesis by F1F0-ATP synthase Biochim. Biophys. Acta 1553 2002 188 211
39. X. Shen, G. Mizuguchi, A. Hamiche, and C. Wu A chromatin remodelling complex involved in transcription and DNA processing Nature 406 2000 541 544
40. E. Torreira, S. Jha, J.R. Lopez-Blanco, E. Arias-Palomo, P. Chacon, C. Canas, S. Ayora, A. Dutta, and O. Llorca Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes Structure 16 2008 1511 1520
41. C. Uetrecht, C. Versluis, N.R. Watts, W.H. Roos, G.J. Wuite, P.T. Wingfield, A.C. Steven, and A.J. Heck High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids Proc. Natl. Acad. Sci. USA 105 2008 9216 9220
42. A.S. Venteicher, Z. Meng, P.J. Mason, T.D. Veenstra, and S.E. Artandi Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly Cell 132 2008 945 957
43. N.J. Watkins, I. Lemm, D. Ingelfinger, C. Schneider, M. Hossbach, H. Urlaub, and R. Luhrmann Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex Mol. Cell 16 2004 789 798
44. J. Weiske, and O. Huber The histidine triad protein Hint1 triggers apoptosis independent of its enzymatic activity J. Biol. Chem. 281 2006 27356 27366
45. P. Wendler, S. Ciniawsky, M. Kock, and S. Kube Structure and function of the AAA+ nucleotide binding pocket Biochim. Biophys. Acta 1823 2012 2 14
46. F. Werner Structure and function of archaeal RNA polymerases Mol. Microbiol. 65 2007 1395 1404
47. F. Werner, and R.O. Weinzierl A recombinant RNA polymerase II-like enzyme capable of promoter-specific transcription Mol. Cell 10 2002 635 646
48. F. Werner, and R.O. Weinzierl Direct modulation of RNA polymerase core functions by basal transcription factors Mol. Cell. Biol. 25 2005 8344 8355
49. M.A. Wood, S.B. McMahon, and M.D. Cole An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc Mol. Cell 5 2000 321 330
50. X. Zhang, and D.B. Wigley The 'glutamate switch' provides a link between ATPase activity and ligand binding in AAA+ proteins Nat. Struct. Mol. Biol. 15 2008 1223 1227