The structural basis of cyclic diguanylate signal transduction by PilZ domains

被引:174
作者
Benach, Jordi [1 ]
Swaminathan, Swarup S. [1 ]
Tamayo, Rita [2 ]
Handelman, Samuel K. [1 ]
Folta-Stogniew, Ewa [3 ]
Ramos, John E. [1 ]
Forouhar, Farhad [1 ]
Neely, Helen [1 ]
Seetharaman, Jayaraman [1 ]
Camilli, Andrew [2 ]
Hunt, John F. [1 ]
机构
[1] Columbia Univ, Dept Biol Sci, NE Struct Genom Consortium, Fairchild Ctr 702A, New York, NY 10027 USA
[2] Tufts Univ, Sch Med, Howard Hughes Med Inst, Dept Mol Microbiol, Boston, MA 02111 USA
[3] Yale Univ, Sch Med, Wm Keck Biotechnol Res Lab, New Haven, CT USA
关键词
allostery; bacterial pathogenesis; cyclic diguanylate (cyclic-di-GMP); fluorescence resonance energy transfer; X-ray crystallography;
D O I
10.1038/sj.emboj.7601918
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
The second messenger cyclic diguanylate (c-di-GMP) controls the transition between motile and sessile growth in eubacteria, but little is known about the proteins that sense its concentration. Bioinformatics analyses suggested that PilZ domains bind c-di-GMP and allosterically modulate effector pathways. We have determined a 1.9 angstrom crystal structure of c-di-GMP bound to VCA0042/PlzD, a PilZ domain-containing protein from Vibrio cholerae. Either this protein or another specific PilZ domain-containing protein is required for V. cholerae to efficiently infect mice. VCA0042/PlzD comprises a C-terminal PilZ domain plus an N-terminal domain with a similar beta-barrel fold. C-di-GMP contacts seven of the nine strongly conserved residues in the PilZ domain, including three in a seven-residue long N-terminal loop that undergoes a conformational switch as it wraps around c-di-GMP. This switch brings the PilZ domain into close apposition with the N-terminal domain, forming a new allosteric interaction surface that spans these domains and the c-di-GMP at their interface. The very small size of the N-terminal conformational switch is likely to explain the facile evolutionary diversification of the PilZ domain.
引用
收藏
页码:5153 / 5166
页数:14
相关论文
共 46 条
[1]  
ADES SE, 1995, THESIS MIT CAMBRIDGE
[2]   Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa [J].
Alm, RA ;
Bodero, AJ ;
Free, PD ;
Mattick, JS .
JOURNAL OF BACTERIOLOGY, 1996, 178 (01) :46-53
[3]   Gapped BLAST and PSI-BLAST: a new generation of protein database search programs [J].
Altschul, SF ;
Madden, TL ;
Schaffer, AA ;
Zhang, JH ;
Zhang, Z ;
Miller, W ;
Lipman, DJ .
NUCLEIC ACIDS RESEARCH, 1997, 25 (17) :3389-3402
[4]   PilZ domain is part of the bacterial c-di-GMP binding protein [J].
Amikam, D ;
Galperin, MY .
BIOINFORMATICS, 2006, 22 (01) :3-6
[5]  
Ausmees N, 2001, FEMS MICROBIOL LETT, V204, P163, DOI 10.1111/j.1574-6968.2001.tb10880.x
[6]   Crystallography & NMR system:: A new software suite for macromolecular structure determination [J].
Brunger, AT ;
Adams, PD ;
Clore, GM ;
DeLano, WL ;
Gros, P ;
Grosse-Kunstleve, RW ;
Jiang, JS ;
Kuszewski, J ;
Nilges, M ;
Pannu, NS ;
Read, RJ ;
Rice, LM ;
Simonson, T ;
Warren, GL .
ACTA CRYSTALLOGRAPHICA SECTION D-BIOLOGICAL CRYSTALLOGRAPHY, 1998, 54 :905-921
[7]   Structural basis of activity and allosteric control of diguanylate cyclase [J].
Chan, C ;
Paul, R ;
Samoray, D ;
Amiot, NC ;
Giese, B ;
Jenal, U ;
Schirmer, T .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (49) :17084-17089
[8]   Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP [J].
Christen, M ;
Christen, B ;
Folcher, M ;
Schauerte, A ;
Jenal, U .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2005, 280 (35) :30829-30837
[9]   DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus [J].
Christen, Matthias ;
Christen, Beat ;
Allan, Martin G. ;
Folcher, Marc ;
Jenoe, Paul ;
Grzesiek, Stephan ;
Jenal, Urs .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (10) :4112-4117
[10]   c-di-GMP-mediated regulation of virulence and biofilm formation [J].
Cotter, Peggy A. ;
Stibitz, Scott .
CURRENT OPINION IN MICROBIOLOGY, 2007, 10 (01) :17-23