Home LiteratureArticle Details
PMID: 17573470 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Integration of rotation and piston motions in coiled-coil signal transduction.

Journal of bacteriology ·Vol. 189 ·No. 16 ·2007-08-00 ·Pages 6048-56

Gao R, Lynn DG

Abstract

A coordinated response to a complex and dynamic environment requires an organism to simultaneously monitor and interpret multiple signaling cues. In bacteria and some eukaryotes, environmental responses depend on the histidine autokinases (HKs). For example, VirA, a large integral membrane HK from Agrobacterium tumefaciens, regulates the expression of virulence genes in response to signals from multiple molecular classes (phenol, pH, and sugar). The ability of this pathogen to perceive inputs from different known host signals within a single protein receptor provides an opportunity to understand the mechanisms of signal integration. Here we exploited the conserved domain organization of the HKs and engineered chimeric kinases to explore the signaling mechanisms of phenol sensing and pH/sugar integration. Our data implicate a piston-assisted rotation of coiled coils for integration of multiple inputs and regulation of critical responses during pathogenesis.

MeSH Terms
Agrobacterium tumefaciens/enzymology,genetics Bacterial Proteins/chemistry,genetics,metabolism DNA-Binding Proteins Gene Expression Regulation, Bacterial Motion Protein Kinases/chemistry,genetics,metabolism Rotation Signal Transduction/genetics,physiology Transcription Factors/genetics,metabolism Virulence Virulence Factors
Chemicals
Bacterial Proteins DNA-Binding Proteins Transcription Factors Virulence Factors Protein Kinases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gao Rong
Center for Fundamental and Applied Molecular Evolution, Departments of Chemistry and Biology, Emory University, Atlanta, GA 30322, USA.
Lynn David G
References (56)
56 references, click to expand
  1. Histidine kinases and response regulator proteins in two-component signaling systems.
    Trends Biochem Sci. 2001 Jun;26(6):369-76 PMID: 11406410
  2. Environmental pH sensing: resolving the VirA/VirG two-component system inputs for Agrobacterium pathogenesis.
    J Bacteriol. 2005 Mar;187(6):2182-9 PMID: 15743967
  3. Ratcheting up vir gene expression in Agrobacterium tumefaciens: coiled coils in histidine kinase signal transduction.
    Chembiochem. 2002 Apr 2;3(4):311-7 PMID: 11933231
  4. Crystal structure of the tandem GAF domains from a cyanobacterial adenylyl cyclase: modes of ligand binding and dimerization.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3082-7 PMID: 15708973
  5. Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB.
    J Biol Chem. 1995 Sep 29;270(39):23143-9 PMID: 7559459
  6. The structure of CodY, a GTP- and isoleucine-responsive regulator of stationary phase and virulence in gram-positive bacteria.
    J Biol Chem. 2006 Apr 21;281(16):11366-73 PMID: 16488888
  7. Receptor sensitivity in bacterial chemotaxis.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):123-7 PMID: 11742065
  8. The GAF domain: an evolutionary link between diverse phototransducing proteins.
    Trends Biochem Sci. 1997 Dec;22(12):458-9 PMID: 9433123
  9. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins.
    FEMS Microbiol Lett. 1999 Jul 1;176(1):111-6 PMID: 10418137
  10. The HAMP domain structure implies helix rotation in transmembrane signaling.
    Cell. 2006 Sep 8;126(5):929-40 PMID: 16959572
  11. A NarX-Tar chimera mediates repellent chemotaxis to nitrate and nitrite.
    Mol Microbiol. 2002 May;44(3):709-19 PMID: 11994152
  12. Mutants of Agrobacterium VirA that activate vir gene expression in the absence of the inducer acetosyringone.
    J Biol Chem. 1994 Jan 28;269(4):2645-51 PMID: 8300595
  13. Transmembrane signaling in bacterial chemoreceptors.
    Trends Biochem Sci. 2001 Apr;26(4):257-65 PMID: 11295559
  14. Kinase-phosphatase competition regulates Bacillus subtilis development.
    Trends Microbiol. 1998 Sep;6(9):366-70 PMID: 9778730
  15. Functional roles assigned to the periplasmic, linker, and receiver domains of the Agrobacterium tumefaciens VirA protein.
    J Bacteriol. 1992 Nov;174(21):7033-9 PMID: 1400253
  16. Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor.
    EMBO J. 2000 Oct 16;19(20):5288-99 PMID: 11032796
  17. Integrating input from multiple signals: the VirA/VirG two-component system of Agrobacterium tumefaciens.
    Chembiochem. 2004 Nov 5;5(11):1535-42 PMID: 15515087
  18. Construction of an efficient expression system for Agrobacterium tumefaciens based on the coliphage T5 promoter.
    Gene. 2000 Jan 25;242(1-2):105-14 PMID: 10721702
  19. Development of the signal in sensory rhodopsin and its transfer to the cognate transducer.
    Nature. 2006 Mar 2;440(7080):115-9 PMID: 16452929
  20. Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains.
    J Mol Biol. 2001 Apr 13;307(5):1271-92 PMID: 11292341
  21. Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoM-open reading frame 2.
    J Bacteriol. 1990 Nov;172(11):6300-7 PMID: 2228961
  22. Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein.
    Proc Natl Acad Sci U S A. 1990 Sep;87(17):6708-12 PMID: 2118656
  23. Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction.
    Mol Microbiol. 1999 Sep;33(6):1093-102 PMID: 10510225
  24. Making informed decisions: regulatory interactions between two-component systems.
    Trends Microbiol. 2003 Aug;11(8):359-66 PMID: 12915093
  25. The chimeric VirA-tar receptor protein is locked into a highly responsive state.
    J Bacteriol. 1993 Sep;175(17):5706-9 PMID: 8366057
  26. Agrobacterium tumefaciens and plant cell interactions and activities required for interkingdom macromolecular transfer.
    Annu Rev Cell Dev Biol. 2006;22:101-27 PMID: 16709150
  27. Chemical biology of multi-host/pathogen interactions: chemical perception and metabolic complementation.
    Annu Rev Phytopathol. 2004;42:439-64 PMID: 15283673
  28. Two-component signal transduction.
    Annu Rev Biochem. 2000;69:183-215 PMID: 10966457
  29. Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein.
    EMBO J. 2005 Dec 21;24(24):4247-59 PMID: 16319927
  30. Sugar-mediated induction of Agrobacterium tumefaciens virulence genes: structural specificity and activities of monosaccharides.
    J Bacteriol. 1990 Nov;172(11):6442-6 PMID: 2121715
  31. Adaptation mechanism of the aspartate receptor: electrostatics of the adaptation subdomain play a key role in modulating kinase activity.
    Biochemistry. 2005 Feb 8;44(5):1550-60 PMID: 15683239
  32. Mechanism of activation of Agrobacterium virulence genes: identification of phenol-binding proteins.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8666-70 PMID: 1528878
  33. Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ.
    J Bacteriol. 1994 Feb;176(4):1157-63 PMID: 8106326
  34. Control of expression of Agrobacterium vir genes by synergistic actions of phenolic signal molecules and monosaccharides.
    Proc Natl Acad Sci U S A. 1990 Sep;87(17):6684-8 PMID: 11607097
  35. The bases of crown gall tumorigenesis.
    J Bacteriol. 2000 Jul;182(14):3885-95 PMID: 10869063
  36. Imitation of Escherichia coli aspartate receptor signaling in engineered dimers of the cytoplasmic domain.
    Science. 1996 Feb 23;271(5252):1113-6 PMID: 8599087
  37. A small protein that mediates the activation of a two-component system by another two-component system.
    EMBO J. 2000 Apr 17;19(8):1861-72 PMID: 10775270
  38. Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium.
    Trends Cell Biol. 2002 Mar;12(3):121-9 PMID: 11859024
  39. Plasmid required for virulence of Agrobacterium tumefaciens.
    J Bacteriol. 1975 Jul;123(1):255-64 PMID: 1141196
  40. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure.
    J Mol Biol. 2001 Nov 2;313(4):903-19 PMID: 11697912
  41. Rotational on-off switching of a hybrid membrane sensor kinase Tar-ArcB in Escherichia coli.
    J Biol Chem. 2003 Apr 11;278(15):13192-5 PMID: 12562763
  42. PCR-ligation-PCR mutagenesis: a protocol for creating gene fusions and mutations.
    Biotechniques. 1995 May;18(5):746-50 PMID: 7619468
  43. Host recognition by the VirA, VirG two-component regulatory proteins of agrobacterium tumefaciens.
    Res Microbiol. 1994 Jun-Aug;145(5-6):461-73 PMID: 7855433
  44. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate.
    Science. 1989 Sep 15;245(4923):1246-9 PMID: 2476847
  45. Membrane topology and functional analysis of the sensory protein VirA of Agrobacterium tumefaciens.
    EMBO J. 1989 Jul;8(7):1919-25 PMID: 2792074
  46. The Pfam protein families database.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D138-41 PMID: 14681378
  47. Role of threonine residue 154 in ligand recognition of the tar chemoreceptor in Escherichia coli.
    J Bacteriol. 1990 Jan;172(1):377-82 PMID: 2104606
  48. Modeling the transmembrane domain of bacterial chemoreceptors.
    Protein Sci. 2002 Apr;11(4):912-23 PMID: 11910034
  49. A cytoplasmic coiled-coil domain is required for histidine kinase activity of the yeast osmosensor, SLN1.
    Mol Microbiol. 2002 Jan;43(2):459-73 PMID: 11985722
  50. Computational learning reveals coiled coil-like motifs in histidine kinase linker domains.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2738-43 PMID: 9501159
  51. Genetic analysis of the signal-sensing region of the histidine protein kinase VirA of Agrobacterium tumefaciens.
    Mol Gen Genet. 2000 Jul;263(6):939-47 PMID: 10954079
  52. PAS domains: internal sensors of oxygen, redox potential, and light.
    Microbiol Mol Biol Rev. 1999 Jun;63(2):479-506 PMID: 10357859
  53. Evidence that the adaptation region of the aspartate receptor is a dynamic four-helix bundle: cysteine and disulfide scanning studies.
    Biochemistry. 2005 Sep 27;44(38):12655-66 PMID: 16171380
  54. Genetic analysis of Agrobacterium.
    Methods Enzymol. 1991;204:384-97 PMID: 1658565
  55. Pleiotropic phenotypes caused by genetic ablation of the receiver module of the Agrobacterium tumefaciens VirA protein.
    J Bacteriol. 1996 Aug;178(15):4710-6 PMID: 8755904
  56. Genetic evidence for an interaction between the VirA sensor protein and the ChvE sugar-binding protein of Agrobacterium.
    J Biol Chem. 1993 Dec 15;268(35):26552-8 PMID: 8253785
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.00459-07
Published
2007-08-00
Epub
2007-00-15
Pages
6048-56
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1952043
Subset
IM
Grants
NIGMS NIH HHS · R01 GM047369 · United States
NIGMS NIH HHS · GM 47369 · United States
External Links
PubMed source DOI: 10.1128/JB.00459-07 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2