Nucleotide-induced switch in oligomerization of the AAA+ ATPase ClpB

被引:65
作者
Akoev, V
Gogol, EP
Barnett, ME
Zolkiewski, M
机构
[1] Kansas State Univ, Dept Biochem, Manhattan, KS 66506 USA
[2] Univ Missouri, Sch Biol Sci, Kansas City, MO 64110 USA
关键词
ClpB; AAA ATPase; molecular chaperone; protein association; nucleotide binding; analytical ultracentrifugation;
D O I
10.1110/ps.03422604
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
ClpB is a member of the bacterial protein-disaggregating chaperone machinery and belongs to the AAA(+) superfamily of ATPases associated with various cellular activities. The mechanism of ClpB-assisted reactivation of strongly aggregated proteins is unknown and the oligomeric state of ClpB has been under discussion. Sedimentation equilibrium and sedimentation velocity show that, under physiological ionic strength in the absence of nucleotides, ClpB from Escherichia coli undergoes reversible self-association that involves protein concentration-dependent populations of monomers, heptamers, and intermediate-size oligomers. Under low ionic strength conditions, a heptamer becomes the predominant form of ClpB. In contrast, ATPgammaS, a nonhydrolyzable ATP analog, as well as ADP stabilize hexameric ClpB. Consistently, electron microscopy reveals that ring-type oligomers of ClpB in the absence of nucleotides are larger than those in the presence of ATPgammaS. Thus, the binding of nucleotides without hydrolysis of ATP produces a significant change in the self-association equilibria of ClpB: from reactions supporting formation of a heptamer to those supporting a hexamer. Our results show how ClpB and possibly other related AAA(+) proteins can translate nucleotide binding into a major structural transformation and help explain why previously published electron micrographs of some AAA(+) ATPases detected both six- and sevenfold particle symmetry.
引用
收藏
页码:567 / 574
页数:8
相关论文
共 31 条
[1]   Structure and activity of ClpB from Escherichia coli -: Role of the amino- and carboxyl-terminal domains [J].
Barnett, ME ;
Zolkiewska, A ;
Zolkiewski, M .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2000, 275 (48) :37565-37571
[2]   Site-directed mutagenesis of conserved charged amino acid residues in C1pβ from Escherichia coli [J].
Barnett, ME ;
Zolkiewski, M .
BIOCHEMISTRY, 2002, 41 (37) :11277-11283
[3]   The structures of HsIU and ATP-dependent protease HsIU-HsIV [J].
Bochtler, M ;
Hartmann, C ;
Song, HK ;
Bourenkov, GP ;
Bartunik, HD ;
Huber, R .
NATURE, 2000, 403 (6771) :800-805
[4]   Hsp104, Hsp70, and Hsp40: A novel chaperone system that rescues previously aggregated proteins [J].
Glover, JR ;
Lindquist, S .
CELL, 1998, 94 (01) :73-82
[5]   Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network [J].
Goloubinoff, P ;
Mogk, A ;
Ben Zvi, AP ;
Tomoyasu, T ;
Bukau, B .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1999, 96 (24) :13732-13737
[6]   Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP [J].
Grimaud, R ;
Kessel, M ;
Beuron, F ;
Steven, AC ;
Maurizi, MR .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1998, 273 (20) :12476-12481
[7]   Microtubule disassembly by ATP-dependent oligomerization of the AAA enzyme katanin [J].
Hartman, JJ ;
Vale, RD .
SCIENCE, 1999, 286 (5440) :782-785
[8]   HOMOLOGY IN STRUCTURAL ORGANIZATION BETWEEN ESCHERICHIA-COLI CLPAP PROTEASE AND THE EUKARYOTIC 26S-PROTEASOME [J].
KESSEL, M ;
MAURIZI, MR ;
KIM, B ;
KOCSIS, E ;
TRUS, BL ;
SINGH, SK ;
STEVEN, AC .
JOURNAL OF MOLECULAR BIOLOGY, 1995, 250 (05) :587-594
[9]   Heptameric ring structure of the heat-shock protein ClpB, a protein-activated ATPase in Escherichia coli [J].
Kim, KI ;
Cheong, GW ;
Park, SC ;
Ha, JS ;
Woo, KM ;
Choi, SJ ;
Chung, CH .
JOURNAL OF MOLECULAR BIOLOGY, 2000, 303 (05) :655-666
[10]   AAA proteins [J].
Lupas, AN ;
Martin, J .
CURRENT OPINION IN STRUCTURAL BIOLOGY, 2002, 12 (06) :746-753