Roles of conserved arginines in ATP-binding domains of AAA+ chaperone ClpB from Thermus thermophilus

FEBS Journal

Volumn 278, Issue 13, 2011, Pages 2395-2403

  Yamasaki, Takashi ^a   Nakazaki, Yosuke ^a   Yoshida, Masasuke ^b   Watanabe, Yo Hei ^a  

^a KONAN UNIVERSITY   (Japan)

^b KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

AAA+; aggregation; arginine finger; chaperone; ClpB

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALANINE; ARGININE; CHAPERONE; MUTANT PROTEIN; PROTEIN CLPB;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN STABILITY; THERMUS THERMOPHILUS;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ARGININE; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; THERMUS THERMOPHILUS;

THERMUS THERMOPHILUS;

EID: 79959301708     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08167.x     Document Type: Article

References (38)

1. Neuwald AF, Aravind L, Spouge JL, &, Koonin EV, (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9, 27-43. (Pubitemid 29095146)
2. Ogura T, &, Wilkinson AJ, (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6, 575-597. (Pubitemid 32747198)
3. Ogura T, Whiteheart SW, &, Wilkinson AJ, (2004) Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ ATPases. J Struct Biol 146, 106-112. (Pubitemid 38369023)
4. Mogk A, Schlieker C, Strub C, Rist W, Weibezahn J, &, Bukau B, (2003) Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J Biol Chem 278, 17615-17624. (Pubitemid 36799363)
5. Wang Q, Song C, Irizarry L, Dai R, Zhang X, &, Li CC, (2005) Multifunctional roles of the conserved Arg residues in the second region of homology of p97/valosin-containing protein. J Biol Chem 280, 40515-40523. (Pubitemid 41780540)
6. Yakushiji Y, Nishikori S, Yamanaka K, &, Ogura T, (2006) Mutational analysis of the functional motifs in the ATPase domain of Caenorhabditis elegans fidgetin homologue FIGL-1: firm evidence for an intersubunit catalysis mechanism of ATP hydrolysis by AAA ATPases. J Struct Biol 156, 93-100. (Pubitemid 44486058)
7. Briggs LC, Baldwin GS, Miyata N, Kondo H, Zhang X, &, Freemont PS, (2008) Analysis of nucleotide binding to P97 reveals the properties of a tandem AAA hexameric ATPase. J Biol Chem 283, 13745-13752.
8. Zhao C, Matveeva EA, Ren Q, &, Whiteheart SW, (2010) Dissecting the N-ethylmaleimide-sensitive factor: required elements of the N and D1 domains. J Biol Chem 285, 761-772.
9. Sanchez Y, &, Lindquist SL, (1990) HSP104 required for induced thermotolerance. Science 248, 1112-1115. (Pubitemid 120031537)
10. Thomas JG, &, Baneyx F, (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J Bacteriol 180, 5165-5172. (Pubitemid 28470945)
11. Parsell DA, Kowal AS, Singer MA, &, Lindquist S, (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478.
12. Glover JR, &, Lindquist S, (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82. (Pubitemid 28347471)
13. Motohashi K, Watanabe Y, Yohda M, &, Yoshida M, (1999) Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc Natl Acad Sci USA 96, 7184-7189. (Pubitemid 29299636)
14. Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, &, Bukau B, (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA 96, 13732-13737.
15. Zolkiewski M, (1999) ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J Biol Chem 274, 28083-28086.
16. Mogk A, Tomoyasu T, Goloubinoff P, Rudiger S, Roder D, Langen H, &, Bukau B, (1999) Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J 18, 6934-6949. (Pubitemid 30000447)
17. Krzewska J, Langer T, &, Liberek K, (2001) Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett 489, 92-96. (Pubitemid 32176012)
18. Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, Yoshida M, &, Tsai FT, (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115, 229-240. (Pubitemid 37329586)
19. Parsell DA, Kowal AS, &, Lindquist S, (1994) Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. J Biol Chem 269, 4480-4487.
20. Zolkiewski M, Kessel M, Ginsburg A, &, Maurizi MR, (1999) Nucleotide-dependent oligomerization of ClpB from Escherichia coli. Protein Sci 8, 1899-1903. (Pubitemid 29430490)
21. Schlee S, Groemping Y, Herde P, Seidel R, &, Reinstein J, (2001) The chaperone function of ClpB from Thermus thermophilus depends on allosteric interactions of its two ATP-binding sites. J Mol Biol 306, 889-899. (Pubitemid 33027708)
22. Krzewska J, Konopa G, &, Liberek K, (2001) Importance of two ATP-binding sites for oligomerization, ATPase activity and chaperone function of mitochondrial Hsp78 protein. J Mol Biol 314, 901-910. (Pubitemid 34087856)
23. Watanabe YH, Motohashi K, &, Yoshida M, (2002) Roles of the two ATP binding sites of ClpB from Thermus thermophilus. J Biol Chem 277, 5804-5809. (Pubitemid 34968358)
24. Akoev V, Gogol EP, Barnett ME, &, Zolkiewski M, (2004) Nucleotide-induced switch in oligomerization of the AAA+ ATPase ClpB. Protein Sci 13, 567-574. (Pubitemid 38252553)
25. Werbeck ND, Zeymer C, Kellner JN, &, Reinstein J, (2011) Coupling of oligomerization and nucleotide binding in the AAA+ chaperone ClpB. Biochemistry 50, 899-909.
26. Weibezahn J, Tessarz P, Schlieker C, Zahn R, Maglica Z, Lee S, Zentgraf H, Weber-Ban EU, Dougan DA, Tsai FT, et al. (2004) Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119, 653-665. (Pubitemid 39535753)
27. Watanabe YH, Takano M, &, Yoshida M, (2005) ATP binding to nucleotide binding domain (NBD)1 of the ClpB chaperone induces motion of the long coiled-coil, stabilizes the hexamer, and activates NBD2. J Biol Chem 280, 24562-24567. (Pubitemid 40934543)
28. Watanabe YH, Nakazaki Y, Suno R, &, Yoshida M, (2009) Stability of the two wings of the coiled-coil domain of ClpB chaperone is critical for its disaggregation activity. Biochem J 421, 71-77.
29. Lee S, Choi JM, &, Tsai FT, (2007) Visualizing the ATPase cycle in a protein disaggregating machine: structural basis for substrate binding by ClpB. Mol Cell 25, 261-271. (Pubitemid 46109613)
30. Karata K, Inagawa T, Wilkinson AJ, Tatsuta T, &, Ogura T, (1999) 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 274, 26225-26232.
31. Higuchi R, Krummel B, &, Saiki RK, (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16, 7351-7367.
32. Ho SN, Hunt HD, Horton RM, Pullen JK, &, Pease LR, (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59. (Pubitemid 19125653)
33. Motohashi K, Yohda M, Endo I, &, Yoshida M, (1996) A novel factor required for the assembly of the DnaK and DnaJ chaperones of Thermus thermophilus. J Biol Chem 271, 17343-17348. (Pubitemid 26244294)
34. Motohashi K, Yohda M, Odaka M, &, Yoshida M, (1997) K+ is an indispensable cofactor for GrpE stimulation of ATPase activity of DnaK × DnaJ complex from Thermus thermophilus. FEBS Lett 412, 633-636. (Pubitemid 27337124)
35. Watanabe YH, &, Yoshida M, (2004) Trigonal DnaK-DnaJ complex versus free DnaK and DnaJ: heat stress converts the former to the latter, and only the latter can do disaggregation in cooperation with ClpB. J Biol Chem 279, 15723-15727. (Pubitemid 38509256)
36. Mizutani T, Nemoto S, Yoshida M, &, Watanabe YH, (2009) Temperature-dependent regulation of Thermus thermophilus DnaK/DnaJ chaperones by DafA protein. Genes Cells 14, 1405-1413.
37. Toyo'oka T, &, Imai K, (1985) Isolation and characterization of cysteine-containing regions of proteins using 4-(aminosulfonyl)-7-fluoro-2,1,3- benzoxadiazole and high-performance liquid chromatography. Anal Chem 57, 1931-1937.
38. Chen H, Xie M-H, Liu W, Yang B, Yang F, Huang J, Huang J, Wu Q, Fu X-D, &, Zhang Y, (2011) A structured RNA in hepatitis B virus post-transcriptional regulatory element represses alternative splicing in a sequence-independent and position-dependent manner. Febs J 278, 1533-1546.