Evolution and diversity of periplasmic proteins involved in copper homeostasis in gamma proteobacteria

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Hernández Montes, Georgina ^a   Argüello, José M ^b   Valderrama, Brenda ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^b Life Science and Bioengineering Center   (United States)

Author keywords

Copper homeostasis; Evolution; Gamma proteobacteria

Indexed keywords

CELL PROTEIN; COPPER; CUSC PROTEIN; PERIPLASMIC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BIODIVERSITY; CONTROLLED STUDY; COPPER HOMEOSTASIS; CYTOGENETICS; CYTOPLASM; EVOLUTIONARY ADAPTATION; EXTRACELLULAR SPACE; GAMMAPROTEOBACTERIA; GENE CLUSTER; ORTHOLOGY; PHYLOGENOMICS; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

COMPUTATIONAL BIOLOGY; COPPER; EVOLUTION, MOLECULAR; GAMMAPROTEOBACTERIA; GENETIC VARIATION; GENOME, BACTERIAL; HOMEOSTASIS; PERIPLASMIC PROTEINS; PHYLOGENY;

GAMMAPROTEOBACTERIA;

EID: 84872600114     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-249     Document Type: Article

References (57)

1. Old iron, young copper: from Mars to Venus. Crichton RR, Pierre JL, BioMetals 2001 14 99 112 10.1023/A:1016710810701 11508852 (Pubitemid 32656569)
2. Hydroxyl radical formation from cuprous ion and hydrogen peroxide: A spin-trapping study. Gunther MR, Hanna PM, Mason RP, Cohen MS, Arch Biochem Biophys 1995 316 515 522 10.1006/abbi.1995.1068 7840659
3. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. Macomber L, Rensing C, Imlay JA, J Bact 2007 189 1616 1626 10.1128/JB.01357-06 17189367 (Pubitemid 46446123)
4. Copper metallochaperones. Robinson NJ, Winge DR, Annu Rev Biochem 2010 79 537 562 10.1146/annurev-biochem-030409-143539 20205585
5. Alternative periplasmic copper resistance mechanisms in Gram negative bacteria. Pontel LB, Soncini FC, Mol Microbiol 2009 73 212 225 10.1111/j.1365-2958.2009.06763.x 19538445
6. Purification and preliminary crystallographic studies of CutC, a novel copper homeostasis protein from Shigella flexneri. Zhu YQ, Zhu DY, Lu HX, Yang N, Li GP, Wang DC, Protein Pept Lett 2005 12 823 826 10.2174/0929866054864184 16305556 (Pubitemid 41634865)
7. Escherichia coli mechanisms of copper homeostasis in a changing environment. Rensing C, Grass G, FEMS Microbiol Rev 2003 27 197 213 10.1016/S0168-6445(03)00049-4 12829268 (Pubitemid 36694656)
8. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. Munson GP, Lam DL, Outten FW, O'Halloran TV, J Bact 2000 182 5864 5871 10.1128/JB.182.20.5864-5871.2000 11004187
9. CopA: an Escherichia coli Cu (I)-translocating P-type ATPase. Rensing C, Fan B, Sharma R, Mitra B, Rosen BP, Proc Natl Acad Sci USA 2000 97 652 656 10.1073/pnas.97.2.652 10639134 (Pubitemid 30070364)
10. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Grass G, Rensing C, Biochem Biophys Res Commun 2001 286 902 908 10.1006/bbrc.2001.5474 11527384 (Pubitemid 32924857)
11. The Independent cue and cus Systems Confer Copper Tolerance during Aerobic and Anaerobic Growth in Escherichia coli. Outten FW, Huffman DL, Hale JA, O'Halloran TV, J Biol Chem 2001 276 30670 30677 10.1074/jbc.M104122200 11399769
12. Switch or funnel: how RND-type transport systems control periplasmic metal homeostasis. Kim EH, Nies DH, McEvoy MM, Rensing C, J Bact 2011 193 2381 2387 10.1128/JB.01323-10 21398536
13. Molecular genetics and transport analysis of the copper-resistance determinant (pco) from Escherichia coli plasmid pRJ1004. Brown NL, Barrett SR, Camakaris J, Lee BTO, Rouch DA, Mol Microbiol 1995 17 1153 1166 10.1111/j.1365-2958.1995.mmi-17061153.x 8594334
14. Copper transport in E. coli. Rouch D, Camakaris J, Lee BTO, Metal Ion Homeostasis:Molecular Biology and Chemistry New York: Alan R.Liss, Hamer DH, Winge DR, 1989 477
15. Identification of cutC and cutF (nlpE) genes involved in copper tolerance in Escherichia coli. Gupta SD, Lee BT, Camakaris J, Wu HC, J Bact 1995 177 4207 4215 7635807
16. Direct Metal Transfer between Periplasmic Proteins Identifies a Bacterial Copper Chaperone. Bagai I, Rensing C, Blackburn NJ, McEvoy MM, Biochemistry 2008 47 11408 11414 10.1021/bi801638m 18847219
17. Copper delivery by metallochaperone proteins. Rosenzweig AC, Acc Chem Res 2001 34 119 128 10.1021/ar000012p 11263870 (Pubitemid 32167861)
18. Conserved mechanism of copper binding and transfer. A comparison of the copper-resistance proteins PcoC from Escherichia coli and CopC from Pseudomonas syringae. Djoko KY, Xiao Z, Huffman DL, Wedd AG, Inorg Chem 2007 46 4560 4568 10.1021/ic070107o 17477524
19. The use of gene clusters to infer functional coupling. Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N, Proc Natl Acad Sci USA 1999 96 2896 901 10.1073/pnas.96.6.2896 10077608 (Pubitemid 29148815)
20. Coexpression of Nuclear Receptors and Histone Methylation Modifying Genes in the Testis: Implications for Endocrine Disruptor Modes of Action. Anderson AM, Carter KW, Anderson D, Wise MJ, PLoS One 2012 7 34158 10.1371/journal.pone. 0034158 22496781
21. Quantifying the relationship between co-expression, co-regulation and gene function. Allocco D, Kohane I, Butte A, BMC Bioinforma 2004 5 18 10.1186/1471-2105-5-18 (Pubitemid 38751317)
22. Bioinformatics strategies for lipidomics analysis: characterization of obesity related hepatic steatosis. Yetukuri L, Katajamaa M, Medina-Gomez G, Seppänen-Laakso T, Vidal-Puig A, Oresic M, BMC Syst Biol 2007 1 12 10.1186/1752-0509-1-12 17408502
23. Consensus clustering and functional interpretation of gene-expression data. Swift S, Tucker A, Vinciotti V, Martin N, Orengo C, Liu X, Kellam P, Genome Biol 2004 5 94 10.1186/gb-2004-5-11-r94 15535870
24. Clustering gene expression patterns. Ben-Dor A, Shamir R, Yakhini Z, J Comput Biol 1999 6 281 297 10.1089/106652799318274 10582567
25. The structure and function of heavy metal transport P1B-ATPases. Argüello JM, Eren E, González-Guerrero M, BioMetals 2007 20 233 248 10.1007/s10534-006-9055-6 17219055 (Pubitemid 46776570)
26. Copper homeostasis in bacteria. Osman D, Cavet JS, Adv Appl Microbiol 2008 65 217 247 19026867
27. Response of Gram-positive bacteria to copper stress. Solioz M, Abicht HK, Mermod M, Mancini S, J Biol Inorg Chem 2010 15 3 14 10.1007/s00775-009-0588-3 19774401
28. The p-type ATPase superfamily. Chan H, Babayan V, Blyumin E, Gandhi C, Hak K, Harake D, Kumar K, Lee P, Li TT, Liu HY, J Mol Microbiol Biotechnol 2010 19 5 104 10.1159/000319588 20962537
29. The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function. Raimunda D, González-Guerrero M, Leeber BW, Argüello JM, BioMetals 2011 24 467 475 10.1007/s10534-010-9404-3 21210186
30. New findings on evolution of metal homeostasis genes: evidence from comparative genome analysis of bacteria and archaea. Coombs JM, Barkay T, Appl Environ Microbiol 2005 71 7083 7091 10.1128/AEM.71.11.7083-7091.2005 16269744 (Pubitemid 43194198)
31. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, Saier MH Jr, J Mol Microbiol Biotechnol 1999 1 107 125 10941792 (Pubitemid 129491932)
32. Efflux mediated heavy metal resistance in prokaryotes. Nies DH, FEMS Microbiol Rev 2003 27 313 339 10.1016/S0168-6445(03)00048-2 12829273 (Pubitemid 36700434)
33. Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Su CC, Long F, Zimmermann MT, Rajashankar KR, Jernigan RL, Edward WY, Nature 2011 470 558 562 10.1038/nature09743 21350490
34. Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. Goldberg M, Pribyl T, Juhnke S, Nies DH, J Biol Chem 1999 274 26065 26070 10.1074/jbc.274.37.26065 10473554 (Pubitemid 29437048)
35. Cuprous oxidase activity of CueO from Escherichia coli. Singh SK, Grass G, Rensing C, Montfort WR, J Bact 2004 186 7815 7817 10.1128/JB.186.22.7815- 7817.2004 15516598 (Pubitemid 39463750)
36. Crystal structure of Escherichia coli CusC, the outer membrane component of a heavy metal efflux pump. Kulathila R, Kulathila R, Indic M, van den Berg B, PLoS One 2011 6 15610 10.1371/journal.pone.0015610 21249122
37. Enzyme recruitment in evolution of new function. Jensen RA, Annu Rev Microbiol 1976 30 409 425 10.1146/annurev.mi.30.100176.002205 791073
38. On the evolution of biochemical syntheses. Horowitz NH, Proc Natl Acad Sci USA 1945 31 153 7 10.1073/pnas.31.6.153 16578152
39. Copper Resistance in E. coli: The Multicopper Oxidase PcoA Catalyzes Oxidation of Copper (I) in Cu(I)Cu(II)-PcoC. Djoko KY, Xiao Z, Wedd AG, ChemBioChem 2008 9 1579 1582 10.1002/cbic.200800100 18536063
40. Crystal Structure of the Membrane Fusion Protein CusB from Escherichia coli. Su CC, Yang F, Long F, Reyon D, Routh MD, Kuo DW, Mokhtari AK, Van Ornam JD, Rabe KL, Hoy JA, J Mol Biol 2009 393 342 355 10.1016/j.jmb.2009.08.029 19695261
41. Structure and mechanism of the tripartite CusCBA heavy-metal efflux complex. Long F, Su CC, Lei HT, Bolla JR, Do SV, Edward WY, Philos Trans R Soc Lond B Biol Sci 2012 367 1047 1058 10.1098/rstb.2011.0203 22411977
42. Interactions between CusF and CusB identified by NMR spectroscopy and chemical cross-linking coupled to mass spectrometry. Mealman TD, Bagai I, Singh P, Goodlet DR, Rensing C, Zhou H, Wysocki VH, McEvoy MM, Biochemistry 2011 50 2559 2566 10.1021/bi102012j 21323389
43. Fitting periplasmic membrane fusion proteins to inner membrane transporters: mutations that enable Escherichia coli AcrA to function with Pseudomonas aeruginosa MexB. Krishnamoorthy G, Tikhonova EB, Zgurskaya HI, J Bact 2008 190 691 698 10.1128/JB.01276-07 18024521 (Pubitemid 351360085)
44. Laccases: structure, reactions, distribution. Claus H, Micron 2004 35 93 96 10.1016/j.micron.2003.10.029 15036303 (Pubitemid 38214830)
45. A network perspective on the evolution of metabolism by gene duplication. Diaz-Mejia JJ, Perez-Rueda E, Segovia L, Genome Biol 2007 8 26 10.1186/gb-2007-8-2-r26 17326820 (Pubitemid 351851030)
46. KEGG: kyoto encyclopedia of genes and genomes. Kanehisa M, Goto S, Nucleic Acids Res 2000 28 27 30 10.1093/nar/28.1.27 10592173 (Pubitemid 30047706)
47. KEGG for integration and interpretation of large-scale molecular data sets. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M, Nucleic Acids Res 2012 40 109 D114 10.1093/nar/gkr988 22080510
48. Phylogenetic and functional assessment of orthologs inference projects and methods. Altenhoff AM, Dessimoz C, PLoS Comput Biol 2009 5 1000262 10.1371/journal.pcbi.1000262 19148271
49. Hierarchical clustering algorithm for comprehensive orthologous-domain classification in multiple genomes. Uchiyama I, Nucleic Acids Res 2006 34 647 658 10.1093/nar/gkj448 16436801 (Pubitemid 43240251)
50. Using whole genome presence/absence data to untangle function in 12 Drosophila genomes. Rosenfeld JA, DeSalle R, Lee EK, O'Grady P, Fly 2008 2 291 299 19139635
51. TM4: a free, open-source system for microarray data management and analysis. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Biotechniques 2003 34 374 378 12613259 (Pubitemid 36184095)
52. TM4 Microarray Software Suite. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J, Methods Enzymol 2006 411 134 193 16939790 (Pubitemid 44291425)
53. Database resources of the national center for biotechnology information. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Federhen S, Nucleic Acids Res 2011 39 38 D51 10.1093/nar/gkq1172 21097890
54. GenBanK. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, Nucleic Acids Res 2009 37 26 D31 10.1093/nar/gkn723 18940867
55. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Letunic I, Bork P, Bioinformatics 2007 23 127 128 10.1093/bioinformatics/btl529 17050570 (Pubitemid 46017867)
56. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Letunic I, Bork P, Nucleic Acids Res 2011 39 475 W478 10.1093/nar/gkr201 21470960
57. Dendroscope: An interactive viewer for large phylogenetic trees. Huson D, Richter D, Rausch C, Dezulian T, Franz M, Rupp R, BMC Bioinforma 2007 8 460 10.1186/1471-2105-8-460 (Pubitemid 351168201)