Structural basis for metal sensing by CnrX

Journal of Molecular Biology

Volumn 408, Issue 4, 2011, Pages 766-779

  Trepreau, Juliette ^a   Girard, Eric ^a   Maillard, Antoine P ^a   De Rosny, Eve ^a   Petit Haertlein, Isabelle ^a   Kahn, Richard ^a   Covès, Jacques ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

CnrX; Cupriavidus metallidurans CH34; extracytoplasmic function; metal sensing; transmembrane signal transduction

Indexed keywords

BACTERIAL PROTEIN; CNRX PROTEIN; COBALT; NICKEL; UNCLASSIFIED DRUG; ZINC;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CUPRIAVIDUS; CUPRIAVIDUS METALLIDURANS; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SENSOR; SIGNAL TRANSDUCTION;

CUPRIAVIDUS METALLIDURANS;

EID: 79955046299     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.014     Document Type: Article

References (52)

1. Giedroc D.P., and Arunkumar A.I. Metal sensor proteins: nature's metalloregulated allosteric switches Dalton Trans. 7 2007 3107 3120 (Pubitemid 47117766)
2. Ma Z., Jacobsen F.E., and Giedroc D.P. Coordination chemistry of bacterial metal transport and sensing Chem. Rev. 109 2009 4644 4681
3. Waldron K.J., Rutherford J.C., Ford D., and Robinson N.J. Metalloproteins and metal sensing Nature 460 2009 823 830
4. Waldron K.J., and Robinson N.J. How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 7 2009 25 35
5. E-dependent envelope stress response Mol. Microbiol. 52 2004 613 619 (Pubitemid 38621733)
6. Brooks B.E., and Buchanan S.K. Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors Biochim. Biophys. Acta 1778 2008 1930 1945
7. Masher T., Helmann J.D., and Unden G. Stimulus perception in bacterial signal-transducing histidine kinases Microbiol. Mol. Biol. Rev. 70 2006 910 938 (Pubitemid 44958261)
8. Raivio T.L., and Silhavy T.J. Periplasmic stress and ECF sigma factors Annu. Rev. Microbiol. 55 2001 591 624 (Pubitemid 32978117)
9. Stock A.M., Robinson V.L., and Goudreau P.N. Two-component signal transduction Annu. Rev. Biochem. 69 2000 183 215
10. Staroń A., Sofia H.J., Dietrich S., Ulrich L.E., Liesegang H., and Mascher T. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family Mol. Microbiol. 74 2009 557 581
11. Burgess R.R., Travers A.A., Dunn J.J., and Bautz E.K. Factor stimulating transcription by RNA polymerase Nature 221 1969 43 46
12. Murakami K.S., Masuda S., and Darst S.A. Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Å resolution Science 296 2002 1280 1284 (Pubitemid 34522777)
13. Helmann J.D. The extracytoplasmic function (ECF) sigma factors Adv. Microb. Physiol. 46 2002 47 110
14. Lonetto M.A., Brown K.L., Rudd K.E., and Buttner M.J. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions Proc. Natl Acad. Sci. USA 91 1994 7573 7577 (Pubitemid 24238227)
15. Paget M.S., and Helmann J.D. The sigma70 family of sigma factors Genome Biol. 4 2003 203
16. Nies D.H. Incidence and function of sigma factors in Ralstonia metallidurans and other bacteria Arch. Microbiol. 181 2004 255 268 (Pubitemid 38471469)
17. Grosse C., Friedrich S., and Nies D.H. Contribution of extracytoplasmic function sigma factors to transition metal homeostasis in Cupriavidus metallidurans strain CH34 J. Mol. Microbiol. Biotechnol. 12 2007 227 240 (Pubitemid 46980131)
18. Janssen P.J., Van Houdt R., Moors H., Monsieurs P., Morin N., and Michaux A. The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments PLoS One 5 2010 e10433
19. von Rozycki T., and Nies D.H. Cupriavidus metallidurans: evolution of a metal-resistant bacterium Antonie Van Leeuwenhoek 96 2009 115 139
20. Mergeay M., Monchy S., Vallaeys T., Auquier V., Benotmane A., and Bertin P. Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes FEMS Microbiol. Rev. 27 2003 385 410 (Pubitemid 36700436)
21. Monchy S., Benotmane M.A., Janssen P., Vallaeys T., Taghavi S., van der Lelie D., and Mergeay M. Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals J. Bacteriol. 189 2007 7417 7425 (Pubitemid 47557358)
22. Liesegang H., Lemke K., Siddiqui R.A., and Schlegel H.G. Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34 J. Bacteriol. 175 1993 767 778 (Pubitemid 23046940)
23. Grass G., Grosse C., and Nies D.H. Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34 J. Bacteriol. 182 2000 1390 1398 (Pubitemid 30104419)
24. Grass G., Fricke B., and Nies D.H. Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations Biometals 18 2005 437 448 (Pubitemid 41298027)
25. Tibazarwa C., Wuertz S., Mergeay M., Wyns L., and van Der Lelie D. Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34 J. Bacteriol. 182 2000 1399 1409 (Pubitemid 30104420)
26. Pompidor G., Maillard A.P., Girard E., Gambarelli S., Kahn R., and Covès J. X-ray structure of the metal-sensor CnrX in both the apo- and copper-bound forms FEBS Lett. 582 2008 3954 3958
27. Pompidor G., Girard E., Maillard A., Ramella-Pairin S., Kahn R., and Covès J. Biostructural analysis of the metal-sensor domain of CnrX from Cupriavidus metallidurans CH34 Antonie van Leeuwenhoek 96 2009 141 148
28. Arnaud J., Touvier M., Galan P., Andriollo-Sanchez M., Ruffieux D., and Roussel A.M. Determinants of serum zinc concentrations in a population of French middle-age subjects (SU.VI.MAX cohort) Eur. J. Clin. Nutr. 64 2010 1057 1064
29. Terwilliger T.C., Grosse-Kunstleve R.W., Afonine P.V., Moriarty N.W., Zwart P.H., and Hung L.W. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Acta Crystallogr. Sect. D 64 2008 61 69 (Pubitemid 350308678)
30. Royant A., Carpentier P., Ohana J., McGeehan J., Paetzold B., and Noirclerc-Savoye M. Advances in spectroscopic methods for biological crystals: Part 1. Fluorescence lifetime measurements J. Appl. Crystallogr. 40 2007 1105 1112 (Pubitemid 350100308)
31. Bertini I., and Luchinat C. High spin cobalt(II) as a probe for the investigation of metalloproteins Adv. Inorg. Biochem. 6 1984 71 111
32. Maret W., and Vallee B.L. Cobalt as probe and label of proteins Methods Enzymol. 226 1993 52 71
33. Collard J.M., Provoost A., Taghavi S., and Mergeay M. A new type of Alcaligenes eutrophus CH34 zinc resistance generated by mutations affecting regulation of the cnr cobalt-nickel resistance system J. Bacteriol. 175 1993 779 784 (Pubitemid 23046941)
34. Irving H., and Williams R.J.P. The stability of transition-metal complexes J. Chem. Soc. 1953 3192 3210
35. Dutta A., and Bahar I. Metal-binding sites are designed to achieve optimal mechanical and signaling properties Structure 18 2010 1140 1148
36. Liu T., Ramesh A., Ma Z., Ward S.K., Zhang L., and George G.N. CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator Nat. Chem. Biol. 3 2007 60 68 (Pubitemid 46005700)
37. Sakamoto K., Agari Y., Agari K., Kuramitsu S., and Shinkai A. Structural and functional characterization of the transcriptional repressor CsoR from Thermus thermophilus HB8 Microbiology 156 2010 1993 2005
38. Ma Z., Cowart D.M., Scott R.A., and Giedroc D.P. Molecular insights into the metal selectivity of the copper(I)-sensing repressor CsoR from Bacillus subtilis Biochemistry 48 2009 3325 3334
39. Iwig J.S., Leitch S.L., Herbst R.W., Maroney M.J., and Chivers P.T. Ni(II) and Co(II) sensing by Escherichia coli RcnR J. Am. Chem. Soc. 130 2008 7592 7606 (Pubitemid 351842123)
40. Berger B.W., Kulp D.W., Span L.M., DeGrado J.L., Billings P.C., and Senes A. Consensus motif for integrin transmembrane helix association Proc. Natl Acad. Sci. USA 107 2010 703 708
41. Melnyk R.A., Kim S., Curran A.R., Engelman D.M., Bowie J.U., and Deber C.M. The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication J. Biol. Chem. 279 2004 16591 16597 (Pubitemid 38509359)
42. Senes A., Engel D.E., and DeGrado W.F. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs Curr. Opin. Struct. Biol. 14 2004 465 479 (Pubitemid 39094354)
43. Zhu J., Luo B.H., Barth P., Schonbrun J., Baker D., and Springer T.A. The structure of a receptor with two associating transmembrane domains on the cell surface: integrin alphaIIbbeta3 Mol. Cell 34 2009 234 249
44. Mergeay M., Nies D., Schlegel H.G., Gerits J., Charles P., and Van Gijsegem F. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals J. Bacteriol. 162 1985 328 334 (Pubitemid 15095872)
45. Kabsch W. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector J. Appl. Crystallogr. 21 1988 916 924
46. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. Sect. D 50 1994 760 763
47. Sheldrick G.M. A short history of SHELX Acta Crystallogr. Sect. A 64 2008 112 122
48. De La Fortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction Methods Enzymol. 276 1997 43 48
49. Cowtan K.D., and Main P. Phase combination and cross validation in iterated density-modification calculations Acta Crystallogr. Sect. D 52 1996 760 763
50. Cowtan K.D. The Buccaneer software for automated model building Acta Crystallogr. Sect. D 62 2006 1002 1011
51. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D 60 2004 2126 2132 (Pubitemid 41742764)
52. Painter J., and Merritt E.A. TLSMD web server for the generation of multi-group TLS models J. Appl. Crystallogr. 39 2006 109 111