Lytic Water Dynamics Reveal Evolutionarily Conserved Mechanisms of ATP Hydrolysis by TIP49 AAA+ ATPases

Structure - Tập 22 - Trang 549-559 - 2014
Arina Afanasyeva1,2, Angela Hirtreiter3, Anne Schreiber3, Dina Grohmann4, Georgii Pobegalov1, Adam R. McKay5, Irina Tsaneva3, Michael Petukhov1,2, Emmanuel Käs6,7, Mikhail Grigoriev6,7, Finn Werner3
1Department of Biophysics, Saint Petersburg State Polytechnical University, Saint Petersburg 195251, Russia
2Division of Molecular and Radiation Biophysics, Petersburg Nuclear Physics Institute, Gatchina 188300, Russia
3Division of Biosciences, Institute for Structural and Molecular Biology, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK
4Physikalische und Theoretische Chemie - NanoBioSciences, Technische Universität Braunschweig, Braunschweig 38106, Germany
5Department of Chemistry, University College London, London WC1H 0AJ, UK
6UMR 5099, CNRS, Toulouse F-31000, France
7Laboratoire de Biologie Moléculaire Eucaryote, Université de Toulouse, Toulouse F-31000, France

Tài liệu tham khảo

Ammelburg, 2006, Classification of AAA+ proteins, J. Struct. Biol., 156, 2, 10.1016/j.jsb.2006.05.002 Bellosta, 2005, Myc interacts genetically with Tip48/Reptin and Tip49/Pontin to control growth and proliferation during Drosophila development, Proc. Natl. Acad. Sci. USA, 102, 11799, 10.1073/pnas.0408945102 Erzberger, 2006, Evolutionary relationships and structural mechanisms of AAA+ proteins, Annu. Rev. Biophys. Biomol. Struct., 35, 93, 10.1146/annurev.biophys.35.040405.101933 Etard, 2005, Pontin and Reptin regulate cell proliferation in early Xenopus embryos in collaboration with c-Myc and Miz-1, Mech. Dev., 122, 545, 10.1016/j.mod.2004.11.010 Gorynia, 2011, Structural and functional insights into a dodecameric molecular machine - the RuvBL1/RuvBL2 complex, J. Struct. Biol., 176, 279, 10.1016/j.jsb.2011.09.001 Gribun, 2008, Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex, J. Mol. Biol., 376, 1320, 10.1016/j.jmb.2007.12.049 Grigoletto, 2013, The ATPase activity of reptin is required for its effects on tumor cell growth and viability in hepatocellular carcinoma. Mol. Cancer Res, 11, 133 Grigorenko, 2011, Minimum energy reaction profiles for ATP hydrolysis in myosin, J. Mol. Graph. Model., 31, 1, 10.1016/j.jmgm.2011.07.005 Grigorenko, 2007, Mechanism of the myosin catalyzed hydrolysis of ATP as rationalized by molecular modeling, Proc. Natl. Acad. Sci. USA, 104, 7057, 10.1073/pnas.0701727104 Grigorenko, 2008, Mechanism of the chemical step for the guanosine triphosphate (GTP) hydrolysis catalyzed by elongation factor Tu, Biochim. Biophys. Acta, 1784, 1908, 10.1016/j.bbapap.2008.08.003 Heck, 2004, Investigation of intact protein complexes by mass spectrometry, Mass Spectrom. Rev., 23, 368, 10.1002/mas.10081 Hishida, 2004, 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, 9573, 10.1073/pnas.0403584101 Ikura, 2000, Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis, Cell, 102, 463, 10.1016/S0092-8674(00)00051-9 Iqbal, 2010, Selective depletion of Sulfolobus solfataricus transcription factor E under heat shock conditions, J. Bacteriol., 192, 2887, 10.1128/JB.01534-09 Iyer, 2004, Evolutionary history and higher order classification of AAA+ ATPases, J. Struct. Biol., 146, 11, 10.1016/j.jsb.2003.10.010 Joly, 2012, ATPase site architecture is required for self-assembly and remodeling activity of a hexameric AAA+ transcriptional activator, Mol. Cell, 47, 484, 10.1016/j.molcel.2012.06.012 Jonsson, 2001, Rvb1p and Rvb2p are essential components of a chromatin remodeling complex that regulates transcription of over 5% of yeast genes, J. Biol. Chem., 276, 16279, 10.1074/jbc.M011523200 Kanai, 2010, Identification of the Phr-dependent heat shock regulon in the hyperthermophilic archaeon, Thermococcus kodakaraensis, J. Biochem., 147, 361, 10.1093/jb/mvp177 Kim, 2006, Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis, Nat. Cell Biol., 8, 631, 10.1038/ncb1415 Kim, 2007, SUMOylation of pontin chromatin-remodeling complex reveals a signal integration code in prostate cancer cells, Proc. Natl. Acad. Sci. USA, 104, 20793, 10.1073/pnas.0710343105 Lopez-Perrote, 2012, Conformational transitions regulate the exposure of a DNA-binding domain in the RuvBL1-RuvBL2 complex, Nucleic Acids Res., 40, 11086, 10.1093/nar/gks871 Machado-Pinilla, 2012, Mechanism of the AAA+ ATPases pontin and reptin in the biogenesis of H/ACA RNPs, RNA, 18, 1833, 10.1261/rna.034942.112 Marquez, 2011, Proteomic characterization of archaeal ribosomes reveals the presence of novel archaeal-specific ribosomal proteins, J. Mol. Biol., 405, 1215, 10.1016/j.jmb.2010.11.055 Matias, 2006, Crystal structure of the human AAA+ protein RuvBL1, J. Biol. Chem., 281, 38918, 10.1074/jbc.M605625200 McKeegan, 2009, 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, 4971, 10.1128/MCB.00752-09 Mezard, 1997, Biochemical properties of RuvBD113N: a mutation in helicase motif II of the RuvB hexamer affects DNA binding and ATPase activities, J. Mol. Biol., 271, 704, 10.1006/jmbi.1997.1225 Nano, 2013, 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, 20110399, 10.1098/rstb.2011.0399 Niewiarowski, 2010, Oligomeric assembly and interactions within the human RuvB-like RuvBL1 and RuvBL2 complexes, Biochem. J., 429, 113, 10.1042/BJ20100489 Parusel, 2006, URI-1 is required for DNA stability in C. elegans, Development, 133, 621, 10.1242/dev.02235 Petukhov, 2012, Large-scale conformational flexibility determines the properties of AAA+ TIP49 ATPases, Structure, 20, 1321, 10.1016/j.str.2012.05.012 Puri, 2007, Dodecameric structure and ATPase activity of the human TIP48/TIP49 complex, J. Mol. Biol., 366, 179, 10.1016/j.jmb.2006.11.030 Putnam, 2001, Structure and mechanism of the RuvB Holliday junction branch migration motor, J. Mol. Biol., 311, 297, 10.1006/jmbi.2001.4852 Rappas, 2005, Structural insights into the activity of enhancer-binding proteins, Science, 307, 1972, 10.1126/science.1105932 Rosenbaum, 2013, The Emergence of the Conserved AAA+ ATPases Pontin and Reptin on the Signaling Landscape, Sci. Signal., 6, mr1 Rottbauer, 2002, Reptin and pontin antagonistically regulate heart growth in zebrafish embryos, Cell, 111, 661, 10.1016/S0092-8674(02)01112-1 Rousseau, 2007, Overexpression and role of the ATPase and putative DNA helicase RuvB-like 2 in human hepatocellular carcinoma, Hepatology, 46, 1108, 10.1002/hep.21770 Schweins, 1994, Why have mutagenesis studies not located the general base in ras p21, Nat. Struct. Biol., 1, 476, 10.1038/nsb0794-476 Senior, 2002, The molecular mechanism of ATP synthesis by F1F0-ATP synthase, Biochim. Biophys. Acta, 1553, 188, 10.1016/S0005-2728(02)00185-8 Shen, 2000, A chromatin remodelling complex involved in transcription and DNA processing, Nature, 406, 541, 10.1038/35020123 Torreira, 2008, Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes, Structure, 16, 1511, 10.1016/j.str.2008.08.009 Uetrecht, 2008, High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids, Proc. Natl. Acad. Sci. USA, 105, 9216, 10.1073/pnas.0800406105 Venteicher, 2008, Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly, Cell, 132, 945, 10.1016/j.cell.2008.01.019 Watkins, 2004, Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex, Mol. Cell, 16, 789, 10.1016/j.molcel.2004.11.012 Weiske, 2006, The histidine triad protein Hint1 triggers apoptosis independent of its enzymatic activity, J. Biol. Chem., 281, 27356, 10.1074/jbc.M513452200 Wendler, 2012, Structure and function of the AAA+ nucleotide binding pocket, Biochim. Biophys. Acta, 1823, 2, 10.1016/j.bbamcr.2011.06.014 Werner, 2007, Structure and function of archaeal RNA polymerases, Mol. Microbiol., 65, 1395, 10.1111/j.1365-2958.2007.05876.x Werner, 2002, A recombinant RNA polymerase II-like enzyme capable of promoter-specific transcription, Mol. Cell, 10, 635, 10.1016/S1097-2765(02)00629-9 Werner, 2005, Direct modulation of RNA polymerase core functions by basal transcription factors, Mol. Cell. Biol., 25, 8344, 10.1128/MCB.25.18.8344-8355.2005 Wood, 2000, An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc, Mol. Cell, 5, 321, 10.1016/S1097-2765(00)80427-X Zhang, 2008, The ‘glutamate switch’ provides a link between ATPase activity and ligand binding in AAA+ proteins, Nat. Struct. Mol. Biol., 15, 1223, 10.1038/nsmb.1501