YgfX (CptA) is a multimeric membrane protein that interacts with the succinate dehydrogenase assembly factor sdhe (YgfY)

Microbiology (United Kingdom)

Volumn 159, Issue PART7, 2013, Pages 1352-1365

  McNeil, Matthew B ^a   Iglesias Cans, Marina C ^a   Clulow, James S ^a   Fineran, Peter C ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ASPARTIC ACID; MEMBRANE PROTEIN; PRODIGIOSIN; SDHE PROTEIN; SUCCINATE DEHYDROGENASE; TRYPTOPHAN; UNCLASSIFIED DRUG; YGFX PROTEIN;

ARTICLE; BACTERIAL GROWTH; CELL STRUCTURE; CELLULAR DISTRIBUTION; CITRIC ACID CYCLE; CITROBACTER; CONTROLLED STUDY; ENTEROBACTER; ENTEROBACTERIACEAE; ENZYME ACTIVATION; ENZYME ACTIVITY; ESCHERICHIA; KLEBSIELLA; MUTAGENESIS; NONHUMAN; OPERON; PECTOBACTERIUM; PHOTORHABDUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEUS; RESPIRATORY CHAIN; SALMONELLA; SERRATIA; SHIGELLA; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; YERSINIA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PRODIGIOSIN; PROTEIN MULTIMERIZATION; SEQUENCE ANALYSIS, DNA; SERRATIA; SUCCINATE DEHYDROGENASE;

ENTEROBACTERIACEAE; SERRATIA SP.;

EID: 84879828826     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.068510-0     Document Type: Article

References (62)

1. Akiyama, Y., Yoshihisa, T. & Ito, K. (1995). FtsH, a membrane-bound ATPase, forms a complex in the cytoplasmic membrane of Escherichia coli. J Biol Chem 270, 23485-23490.
2. Alteri, C. J., Smith, S. N. & Mobley, H. L. T. (2009). Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5, e1000448.
3. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L. & Mori, H. (2006). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 0008.
4. Bardy, S. L. & Jarrell, K. F. (2003). Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae. Mol Microbiol 50, 1339-1347.
5. Bowden, S. D., Ramachandran, V. K., Knudsen, G. M., Hinton, J. C. D. & Thompson, A. R. (2010). An incomplete TCA cycle increases survival of Salmonella Typhimurium during infection of resting and activated murine macrophages. PLoS ONE 5, e13871.
6. Cecchini, G. (2003). Function and structure of complex II of the respiratory chain. Annu Rev Biochem 72, 77-109.
7. Cecchini, G., Schroder, I., Gunsalus, R. P. & Maklashina, E. (2002). Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim Biophys Acta 1553, 140-157.
8. Cole, C., Barber, J. D. & Barton, G. J. (2008). The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36 (Web Server issue), W197-W201.
9. Cook, G. M., Robson, J. R., Frampton, R. A., McKenzie, J., Przybilski, R., Fineran, P. C. & Arcus, V. L. (2013). Ribonucleases in bacterial toxin-antitoxin systems. Biochem Biophys Acta 1829, 523-531.
10. de Boer, P. A., Crossley, R. E., Hand, A. R. & Rothfield, L. I. (1991). The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J 10, 4371-4380.
11. Edmondson, D. E. & Newton-Vinson, P. (2001). The covalent FAD of monoamine oxidase: structural and functional role and mechanism of the flavinylation reaction. Antioxid Redox Signal 3, 789-806.
12. Fineran, P. C., Everson, L., Slater, H. & Salmond, G. P. (2005a). A GntR family transcriptional regulator (PigT) controls gluconatemediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia. Microbiology 151, 3833-3845.
13. Fineran, P. C., Slater, H., Everson, L., Hughes, K. & Salmond, G. P. (2005b). Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol Microbiol 56, 1495-1517.
14. Fineran, P. C., Williamson, N. R., Lilley, K. S. & Salmond, G. P. (2007). Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX. J Bacteriol 189, 7653-7662.
15. Fineran, P. C., Blower, T. R., Foulds, I. J., Humphreys, D. P., Lilley, K. S. & Salmond, G. P. C. (2009). The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci U S A 106, 894-899.
16. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G. & other authors (2010). The Pfam protein families database. Nucleic Acids Res 38 (Database issue), D211-D222.
17. Gerdes, K. & Wagner, E. G. H. (2007). RNA antitoxins. Curr Opin Microbiol 10, 117-124.
18. Gerdes, K., Christensen, S. K. & Løbner-Olesen, A. (2005). Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3, 371-382.
19. Gristwood, T., Fineran, P. C., Everson, L., Williamson, N. R. & Salmond, G. P. (2009). The PhoBR two-component system regulates antibiotic biosynthesis in Serratia in response to phosphate. BMC Microbiol 9, 112.
20. Gristwood, T., McNeil, M. B., Clulow, J. S., Salmond, G. P. C. & Fineran, P. C. (2011). PigS and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J Bacteriol 193, 1076-1085.
21. Hao, H.-X., Khalimonchuk, O., Schraders, M., Dephoure, N., Bayley, J. P., Kunst, H., Devilee, P., Cremers, C. W., Schiffman, J. D. & other authors (2009). SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325, 1139-1142.
22. Hederstedt, L. (1983). Succinate dehydrogenase mutants of Bacillus subtilis lacking covalently bound flavin in the flavoprotein subunit. Eur J Biochem 132, 589-593.
23. Heuts, D. P. H. M., Scrutton, N. S., McIntire, W. S. & Fraaije, M. W. (2009). What's in a covalent bond? On the role and formation of covalently bound flavin cofactors. FEBS J 276, 3405-3427.
24. Kall, L., Krogh, A. & Sonnhammer, E. L. L. (2007). Advantages of combined transmembrane topology and signal peptide prediction - the Phobius web server. Nucleic Acids Res 35 (Web Server issue), W429-W432.
25. Karimova, G., Pidoux, J., Ullmann, A. & Ladant, D. (1998). A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95, 5752-5756.
26. Kelley, L. A. & Sternberg, M. J. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4, 363-371.
27. Kim, J., Fuller, J. H., Kuusk, V., Cunane, L., Chen, Z. W., Mathews, F. S. & McIntire, W. S. (1995). The cytochrome subunit is necessary for covalent FAD attachment to the flavoprotein subunit of p-cresol methylhydroxylase. J Biol Chem 270, 31202-31209.
28. Kimelman, A., Levy, A., Sberro, H., Kidron, S., Leavitt, A., Amitai, G., Yoder-Himes, D. R., Wurtzel, O., Zhu, Y. & other authors (2012). A vast collection of microbial genes that are toxic to bacteria. Genome Res 22, 802-809.
29. Krell, T., Lacal, J., Busch, A., Silva-Jiménez, H., Guazzaroni, M.-E. & Ramos, J. L. (2010). Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64, 539-559.
30. Kruse, T., Bork-Jensen, J. & Gerdes, K. (2005). The morphogenetic MreBCD proteins of Escherichia coli form an essential membranebound complex. Mol Microbiol 55, 78-89.
31. Langridge, G. C., Phan, M.-D., Turner, D. J., Perkins, T. T., Parts, L., Haase, J., Charles, I., Maskell, D. J., Peters, S. E. & other authors (2009). Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19, 2308-2316.
32. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
33. Lim, K., Doseeva, V., Demirkan, E. S., Pullalarevu, S., Krajewski, W., Galkin, A., Howard, A. & Herzberg, O. (2005). Crystal structure of the YgfY from Escherichia coli, a protein that may be involved in transcriptional regulation. Proteins 58, 759-763.
34. Mascher, T. (2006). Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol Lett 264, 133-144.
35. Mascher, T., Helmann, J. D. & Unden, G. (2006). Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70, 910-938.
36. Masuda, H., Tan, Q., Awano, N., Wu, K. P. & Inouye, M. (2012a). YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol Microbiol 84, 979-989.
37. Masuda, H., Tan, Q., Awano, N., Yamaguchi, Y. & Inouye, M. (2012b). A novel membrane-bound toxin for cell division, CptA (YgfX), inhibits polymerization of cytoskeleton proteins, FtsZ and MreB, in Escherichia coli. FEMS Microbiol Lett 328, 174-181.
38. McNeil, M. B. & Fineran, P. C. (2013). Prokaryotic assembly factors for the attachment of flavin to complex II. Biochim Biophys Acta 1827, 637-647.
39. McNeil, M. B., Clulow, J. S., Wilf, N. M., Salmond, G. P. C. & Fineran, P. C. (2012). SdhE is a conserved protein required for flavinylation of succinate dehydrogenase in bacteria. J Biol Chem 287, 18418-18428.
40. Mercado-Lubo, R., Gauger, E. J., Leatham, M. P., Conway, T. & Cohen, P. S. (2008). A Salmonella enterica serovar typhimurium succinate dehydrogenase/fumarate reductase double mutant is avirulent and immunogenic in BALB/c mice. Infect Immun 76, 1128-1134.
41. Mewies, M., McIntire, W. S. & Scrutton, N. S. (1998). Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci 7, 7-21.
42. Miller, J. (1972). Experiments in Molecular Genetics, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
43. Park, S.-J., Tseng, C.-P. & Gunsalus, R. P. (1995). Regulation of succinate dehydrogenase (sdhCDAB) operon expression in Escherichia coli in response to carbon supply and anaerobiosis: role of ArcA and Fnr. Mol Microbiol 15, 473-482.
44. Park, S. J., Chao, G. & Gunsalus, R. P. (1997). Aerobic regulation of the sucABCD genes of Escherichia coli, which encode alphaketoglutarate dehydrogenase and succinyl coenzyme A synthetase: roles of ArcA, Fnr, and the upstream sdhCDAB promoter. J Bacteriol 179, 4138-4142.
45. Przybilski, R., Richter, C., Gristwood, T., Clulow, J. S., Vercoe, R. B. & Fineran, P. C. (2011). Csy4 is responsible for CRISPR RNA processing in Pectobacterium atrosepticum. RNA Biol 8, 517-528.
46. Robinson, K. M., Rothery, R. A., Weiner, J. H. & Lemire, B. D. (1994). The covalent attachment of FAD to the flavoprotein of Saccharomyces cerevisiae succinate dehydrogenase is not necessary for import and assembly into mitochondria. Eur J Biochem 222, 983-990.
47. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Saraste, M. (1999). Oxidative phosphorylation at the fin de siècle. Science 283, 1488-1493.
49. Sberro, H., Leavitt, A., Kiro, R., Koh, E., Peleg, Y., Qimron, U. & Sorek, R. (2013). Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol Cell 50, 136-148.
50. Schiffer, M., Chang, C. H. & Stevens, F. J. (1992). The functions of tryptophan residues in membrane proteins. Protein Eng 5, 213-214.
51. Sevin, E. W. & Barloy-Hubler, F. (2007). RASTA-Bacteria: a web-based tool for identifying toxin-antitoxin loci in prokaryotes. Genome Biol 8, R155.
52. Shi, J., Blundell, T. L. & Mizuguchi, K. (2001). FUGUE: sequencestructure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310, 243-257.
53. Slater, H., Crow, M., Everson, L. & Salmond, G. P. (2003). Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol 47, 303-320.
54. Smeitink, J., van den Heuvel, L. & DiMauro, S. (2001). The genetics and pathology of oxidative phosphorylation. Nat Rev Genet 2, 342-352.
55. Tchawa Yimga, M., Leatham, M. P., Allen, J. H., Laux, D. C., Conway, T. & Cohen, P. S. (2006). Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect Immun 74, 1130-1140.
56. Thomson, N. R., Crow, M. A., McGowan, S. J., Cox, A. & Salmond, G. P. (2000). Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36, 539-556.
57. Vasudevan, S. G., Tang, P., Dixon, N. E. & Poole, R. K. (1995). Distribution of the flavohaemoglobin, HMP, between periplasm and cytoplasm in Escherichia coli. FEMS Microbiol Lett 125, 219-224.
58. Wang, X., Lord, D. M., Cheng, H.-Y., Osbourne, D. O., Hong, S. H., Sanchez-Torres, V., Quiroga, C., Zheng, K., Herrmann, T. & other authors (2012). A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat Chem Biol 8, 855-861.
59. Williamson, N. R., Simonsen, H. T., Ahmed, R. A., Goldet, G., Slater, H., Woodley, L., Leeper, F. J. & Salmond, G. P. (2005). Biosynthesis of the red antibiotic, prodigiosin, in Serratia: identification of a novel 2-methyl-3-n-amyl-pyrrole (MAP) assembly pathway, definition of the terminal condensing enzyme, and implications for undecylprodigiosin biosynthesis in Streptomyces. Mol Microbiol 56, 971-989.
60. Williamson, N. R., Fineran, P. C., Leeper, F. J. & Salmond, G. P. (2006). The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4, 887-899.
61. Williamson, N. R., Fineran, P. C., Ogawa, W., Woodley, L. R. & Salmond, G. P. (2008). Integrated regulation involving quorum sensing, a two-component system, a GGDEF/EAL domain protein and a post-transcriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia. Environ Microbiol 10, 1202-1217.
62. Yankovskaya, V., Horsefield, R., Tornroth, S., Luna-Chavez, C., Miyoshi, H., Léger, C., Byrne, B., Cecchini, G. & Iwata, S. (2003). Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299, 700-704.