#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

CorE from Is a Copper-Dependent RNA Polymerase Sigma Factor


The dual toxicity/essentiality of copper forces cells to maintain a tightly regulated homeostasis for this metal in all living organisms, from bacteria to humans. Consequently, many genes have previously been reported to participate in copper detoxification in bacteria. Myxococcus xanthus, a prokaryote, encodes many proteins involved in copper homeostasis that are differentially regulated by this metal. A σ factor of the ECF (extracytoplasmic function) family, CorE, has been found to regulate the expression of the multicopper oxidase cuoB, the P1B-type ATPases copA and copB, and a gene encoding a protein with a heavy-metal-associated domain. Characterization of CorE has revealed that it requires copper to bind DNA in vitro. Genes regulated by CorE exhibit a characteristic expression profile, with a peak at 2 h after copper addition. Expression rapidly decreases thereafter to basal levels, although the metal is still present in the medium, indicating that the activity of CorE is modulated by a process of activation and inactivation. The use of monovalent and divalent metals to mimic Cu(I) and Cu(II), respectively, and of additives that favor the formation of the two redox states of this metal, has revealed that CorE is activated by Cu(II) and inactivated by Cu(I). The activation/inactivation properties of CorE reside in a Cys-rich domain located at the C terminus of the protein. Point mutations at these residues have allowed the identification of several Cys involved in the activation and inactivation of CorE. Based on these data, along with comparative genomic studies, a new group of ECF σ factors is proposed, which not only clearly differs mechanistically from the other σ factors so far characterized, but also from other metal regulators.


Vyšlo v časopise: CorE from Is a Copper-Dependent RNA Polymerase Sigma Factor. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002106
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002106

Souhrn

The dual toxicity/essentiality of copper forces cells to maintain a tightly regulated homeostasis for this metal in all living organisms, from bacteria to humans. Consequently, many genes have previously been reported to participate in copper detoxification in bacteria. Myxococcus xanthus, a prokaryote, encodes many proteins involved in copper homeostasis that are differentially regulated by this metal. A σ factor of the ECF (extracytoplasmic function) family, CorE, has been found to regulate the expression of the multicopper oxidase cuoB, the P1B-type ATPases copA and copB, and a gene encoding a protein with a heavy-metal-associated domain. Characterization of CorE has revealed that it requires copper to bind DNA in vitro. Genes regulated by CorE exhibit a characteristic expression profile, with a peak at 2 h after copper addition. Expression rapidly decreases thereafter to basal levels, although the metal is still present in the medium, indicating that the activity of CorE is modulated by a process of activation and inactivation. The use of monovalent and divalent metals to mimic Cu(I) and Cu(II), respectively, and of additives that favor the formation of the two redox states of this metal, has revealed that CorE is activated by Cu(II) and inactivated by Cu(I). The activation/inactivation properties of CorE reside in a Cys-rich domain located at the C terminus of the protein. Point mutations at these residues have allowed the identification of several Cys involved in the activation and inactivation of CorE. Based on these data, along with comparative genomic studies, a new group of ECF σ factors is proposed, which not only clearly differs mechanistically from the other σ factors so far characterized, but also from other metal regulators.


Zdroje

1. WhitworthDE 2008 Myxobacteria. Multicellularity and differentiation Washington DC ASM Press. 520

2. WaldronKJRobinsonNJ 2009 How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 6 25 35

3. TisatoFMarzanoCPorchiaMPelleiMSantiniC 2010 Copper in diseases and treatments, and copper-based anticancer strategies. Med Res Rev 30 708 49

4. OsmanDCavetJS 2008 Copper homeostasis in bacteria. Adv Appl Microbiol 65 217 247

5. SoliozMAbichtHKMermodMManciniS 2010 Response of Gram-positive bacteria to copper stress. J Biol Inorg Chem 15 3 14

6. Moraleda-MuñozAPérezJFontesMMurilloFJMuñoz-DoradoJ 2005 Copper induction of carotenoid synthesis in the bacterium Myxococcus xanthus. Mol Microbiol 56 1159 1168

7. Sánchez-SutilMCGómez-SantosNMoraleda-MuñozAMartinsLOPérezJ 2007 Differential expression of the three multicopper oxidases from Myxococcus xanthus. J Bacteriol 189 4887 4898

8. Moraleda-MuñozAPérezJExtremera-LeónALMuñoz-DoradoJ 2010 Differential regulation of six heavy metal efflux systems in the response of Myxococcus xanthus to copper. Appl Environ Microbiol 76 6069 6076

9. Moraleda-MuñozAPérezJExtremera-LeónALMuñoz-DoradoJ 2010 Expression and physiological role of three Myxococcus xanthus copper-dependent P1B-type ATPases during bacterial growth and development. Appl Environ Microbiol 76 6077 6084

10. Marles-WrightJLewisRJ 2007 Stress responses of bacteria. Curr Opin Struct Biol 17 755 760

11. HelmannJD 2002 The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46 47 110

12. CampbellEAMuzzinOChlenovMSunJLOlsonCA 2002 Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell 9 527 539

13. StarońASofiaHJDietrichSUlrichLELiesegangH 2009 The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol Microbiol 74 557 581

14. BrooksBEBuchananSK 2008 Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors. Biochim Biophys Acta 1778 1930 1945

15. RiaivioTLSilhavyTJ 2001 Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55 591 624

16. HughesKTMatheeK 1998 The anti-sigma factors. Annu Rev Microbiol 52 231 286

17. RodrigueSBrodeurJJacquesPEGervaisALBrzezinskiR 2007 Identification of mycobacterial sigma factor binding sites by chromatin immunoprecipitation assays. J Bacteriol 189 1505 1513

18. Martínez-CañameroMMuñoz-DoradoJFarez-VidalEInouyeMInouyeS 1993 Oar, a 115-kilodalton membrane protein required for development of Myxococcus xanthus. J Bacteriol 175 4756 4763

19. XiaoZDonnellyPSZimmermannMWeddAG 2008 Transfer of copper between bis(thiosemicarbazone) ligands and intracellular copper-binding proteins. Insights into mechanisms of copper uptake and hypoxia selectivity. Inorg Chem 47 4338 4347

20. XiaoZBroseJSchimoSAcklandSMLa FontaineS 2011 Unification of the copper(I) binding affinities of the metallo-chaperones Atx1, Atox1 and related proteins: detection probes and affinity standards. J Biol Chem 286 11047 11055

21. AlvarezHMXueYRobinsonCDCanalizo-HernándezMAMarvinRG 2010 Tetrathiomolybdate inhibits copper trafficking proteins through metal cluster formation. Science 327 331 334

22. DavisAVO'HalloranTV 2008 A place for thioether chemistry in cellular copper ion recognition and trafficking. Nat Chem Biol 4 148 151

23. PaulsenCECarrollKS 2010 Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem Biol 5 47 62

24. ChangelaAChenKXueYHolschenJOuttenCE 2003 Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301 1383 1387

25. PenellaMAGiedrocDP 2005 Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. Biometal 18 413 428

26. GiedrocDPArunkumarAI 2007 Metal sensor proteins: nature's metalloregulated allosteric switches. Dalton Trans 29 3107 3120

27. OsmanDCavetJS 2010 Bacterial metal sensing proteins exemplified by ArsR-SmtB family repressors. Nat Prod Rep 27 668 680

28. SiluvaiGSMayfieldMNilgesMJDeBeer GeorgeSBlackburnNJ 2010 Anatomy of a red copper center: spectroscopic identification and reactivity of the copper centers of Bacillus subtilis Sco and its Cys-to-Ala variants. J Am Chem Soc 132 5215 5226

29. SiluvaiGSNakanoMMayfieldMBlackburnNJ 2011 The essential role of the Cu(II) state of Sco in the maturation of the CuA center of cytochrome oxidase: evidence from H135Met and H135SeM variants of the Bacillus subtilis Sco. J Biol Inorg Chem 16 285 297

30. CooperCEPatelRPBrookesPSDarley-UsmarVM 2002 Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem Sci 27 489 492

31. CampbellEAGreenwellRAnthonyJRWangSLimL 2007 A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol Cell 27 793 805

32. WaldronKJRutherfordJCFordDRobinsonNJ 2009 Metalloproteins and metal sensing. Nature 460 823 830

33. SambrookJRussellDW 2001 Molecular cloning: a laboratory manual Cold Spring Harbor NY Cold Spring Harbor Laboratory Press. 2344

34. JulienBKaiserADGarzaA 2000 Spatial control of cell differentiation in Myxococcus xanthus. Proc Natl Acad Sci U S A 97 9098 9103

35. ChoKZusmanDR 1999 AsgD, a new two-component regulator required for A-signalling and nutrient sensing during early development of Myxococcus xanthus. Mol Microbiol 34 268 281

36. FinnRDMistryJTateJCoggillJPHegerA 2010 The Pfam protein families database. Nucl Acids Res 38 211 222

37. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948

38. PérezJCastañeda-GarcíaAJenke-KodamaHMüllerRMuñoz-DoradoJ 2008 Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome. Proc Natl Acad Sci U S A 105 15950 15955

39. Elías-ArnanzMFontesMPabmanabhanS 2008 Carotenogenesis in Myxococcus xanthus: a complex regulatory network. WhitworthDE Myxobacteria. Multicellularity and differentiation Washington DC ASM Press 211 225

40. MünchRHillerKGroteAScheerMKleinJ 2005 Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21 4187 4189

41. CrooksGEHonGChandoniaJMBrennerSE 2004 WebLogo: A sequence logo generator. Genome Res 14 1188 1190

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 6
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#