Weak interactions between salmonella enterica FlhB and other flagellar export apparatus proteins govern type III secretion dynamics

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  McMurry, Jonathan L ^a   Minamino, Tohru ^b   Furukawa, Yukio ^b   Francis, Joshua W ^a,c   Hill, Stephanie A ^a,d   Helms, Katy A ^a,e   Namba, Keiichi ^b  

^a KENNESAW STATE UNIVERSITY   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

^e MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN FLHAC; BACTERIAL PROTEIN FLHB; BACTERIAL PROTEIN FLII; BACTERIAL PROTEIN FLIK; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; FLHA PROTEIN, BACTERIA; FLHB PROTEIN, BACTERIA; FLIH PROTEIN, BACTERIA; FLII PROTEIN, BACTERIA; FLIK PROTEIN, BACTERIA; MEMBRANE PROTEIN; PROTEIN BINDING; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOPLASM; FLAGELLUM; NONHUMAN; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SALMONELLA ENTERICA; ALGORITHM; CHEMISTRY; COMPUTER SIMULATION; DRUG EFFECTS; GENETICS; IMMUNOBLOTTING; KINETICS; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT;

ADENOSINE TRIPHOSPHATE; ALGORITHMS; BACTERIAL PROTEINS; COMPUTER SIMULATION; FLAGELLA; IMMUNOBLOTTING; KINETICS; MEMBRANE PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; PROTON-TRANSLOCATING ATPASES; SALMONELLA ENTERICA;

EID: 84941991899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134884     Document Type: Article

References (40)

1. Zhao X, Norris SJ, Liu J (2014) Molecular architecture of the bacterial flagellar motor in cells. Biochemistry 53: 4323-4333. doi: 10.1021/bi500059y PMID: 24697492
2. Terashima H, Kojima S, Homma M (2008) Flagellar motility in bacteria structure and function of flagellar motor. Int Rev Cell Mol Biol 270: 39-85. doi: 10.1016/S1937-6448(08)01402-0 PMID: 19081534
3. Minamino T, Imada K, Namba K (2008) Molecular motors of the bacterial flagella. Curr Opin Struct Biol 18: 693-701. doi: 10.1016/j.sbi.2008.09.006 PMID: 18848888
4. Minamino T (2014) Protein export through the bacterial flagellar type III export pathway. Biochim Biophys Acta 1843: 1642-1648. doi: 10.1016/j.bbamcr.2013.09.005 PMID: 24064315
5. Evans LDB, Hughes C, Fraser GM (2014) Building a flagellum outside the bacterial cell. Trends Microbiol 10: 566-572.
6. Minamino T, Namba K (2008) Distinct roles of the flagellar ATPase and proton motive force in bacterial flagellar protein export. Nature (London) 451: 485-488.
7. Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT (2008) Energy source of flagellar type III secretion. Nature (London) 451: 489-492.
8. Minamino T, Morimoto YV, Hara N, Namba K (2011) An energy transduction mechanism used in bacterial flagellar type III protein export. Nat Commun 2: 475. doi: 10.1038/ncomms1488 PMID: 21934659
9. Evans LDB, Poulter S, Terentjev T, Hughes C, Fraser GM (2013) A chain mechanism for flagellar growth. Nature 504: 287-290. doi: 10.1038/nature12682 PMID: 24213633
10. Burkinshaw BJ, Strydnaka NCJ (2014) Assembly and structure of he T3SS. Biochim Biophys Acta 1843: 1649-1663. doi: 10.1016/j.bbamcr.2014.01.035 PMID: 24512838
11. Ferris HU, Minamino T (2006) Flipping the switch: bringing order to flagellar assembly. Trends in Microbiol 14: 519-525.
12. Ferris HU, Furukawa Y, Minamino T, Kroetz MB, Kihara M, Namba K, et al. (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280.
13. Morris DP, Roush ED, Thompson JW, Moseley MA, Murphy JW, McMurry JL (2010) Kinetic characterization of Salmonella FliK-FlhB interactions demonstrates complexity of the type III secretion substratespecificity switch. Biochemistry 49: 6386-6393. doi: 10.1021/bi100487p PMID: 20586476
14. Fraser GM, Hirano T, Ferris HU, Devgan LL, Kihara M, Macnab RM (2003) Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol Microbiol 48: 1043-1057. PMID: 12753195
15. Minamino T, González-Pedrajo B, Yamaguchi K, Aizawa S-I, Macnab RM (1999) FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol Microbiol 34: 295-304. PMID: 10564473
16. Williams AW, Yamaguchi S, Togashi F, Aizawa S-I, Kawagishi I, Macnab RM (1996) Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J Bacteriol 178: 2960-2970. PMID: 8631688
17. Hirano T, Minamino T, Namba K, Macnab RM (2003) Substrate specificity classes and the recognition signal for Salmonella type III flagellar export. J Bacteriol 185: 2485-2492. PMID: 12670972
18. Moriya N, Minamino T, Hughes KT, Macnab RM, Namba K (2006) The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J Mol Biol 359: 466-477. PMID: 16630628
19. Erhardt M, Singer HM, Wee DH, Keener JP, Hughes KT (2011) An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. EMBO J 30: 2948-2961. doi: 10.1038/emboj.2011.185 PMID: 21654632
20. Uchida K, Aizawa S (2014) The flagellar soluble protein FliK determines the minimal length of the hook in Salmonella enterica Serovar Typhimuriu. J Bact 196: 1753-1758. doi: 10.1128/JB.00050-14 PMID: 24563036
21. Minamino T, Macnab RM (2000) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35: 1052-1064. PMID: 10712687
22. McMurry JL, Van Arnam JS, Kihara M, Macnab RM (2004) Analysis of the cytoplasmic domains of Salmonella FlhA and interactions with components of the flagellar export machinery. J Bacteriol 186: 7586-7592. PMID: 15516571
23. Concepcion J, Witte K, Wartchow C, Choo S, Yao D, Persson H, et al. (2009) Label-free detection of biomolecular interactions using biolayer interferometry for kinetic characterization. Comb Chem High Throughput Screen 12: 791-800. PMID: 19758119
24. Abdiche Y, Malashock D, Pinkerton A, Pons J (2008) Determining kinetics and affinities of protein interactions using a parallel real-time label-free biosensor, the Octet. Anal Biochem 377: 209-217. doi: 10. 1016/j.ab.2008.03.035 PMID: 18405656
25. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72: 248-254. PMID: 942051
26. Fleming KG, Ackerman AL, Engelman DM (1997) The effect of point mutations on the free energy of transmembrane α-helix dimerization. J Mol Biol 272: 266-275. PMID: 9299353
27. Minamino T, Saijo-Hamano Y, Furukawa Y, Gonzalez-Pedrajo B, Macnab RM, Namba K (2004) Domain organization and function of Salmonella FliK, a flagellar hook-length control protein. J Mol Biol 341: 491-502. PMID: 15276839
28. Patterson-Delafield J, Martinez RJ, Stocker BAD, Yamaguchi S (1973) A new fla gene in Salmonella typhimurium - flaR - and its mutant phenotype - superhooks. Arch Mikrobiol 90: 107-120. PMID: 4575053
29. Francis NR, Sosinsky GE, Thomas D, DeRosier DJ (1994) Isolation, characterization and structure of bacterial flagellar motors containing the switch complex. J Mol Biol 235: 1261-1270. PMID: 8308888
30. Kihara M, Minamino T, Yamaguchi S, Macnab RM (2001) Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J Bacteriol 183: 1655-1662. PMID: 11160096
31. Minamino T, Macnab RM (2000) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate-specificity switching. J Bacteriol 182: 4906-4914. PMID: 10940035
32. McMurry JL, Chrestensen CA, Scott IM, Lee EW, Rahn AM, Johansen AM, et al. (2011) Rate, affinity and calcium dependence of CaM binding to eNOS and nNOS: effects of phosphorylation. FEBS J 278: 4943-4954. doi: 10.1111/j.1742-4658.2011.08395.x PMID: 22004458
33. Benoit SL, McMurry JL, Hill SA, Maier RJ (2012) Helicobacter pylori hdrogenase accessory protein HypA and urase accessory protein UreG compete for UreE recognition". Biochim Biophys Acta 1820: 1519-1525.
34. Meshcheryakov VA, Barker CS, Kostyukova AS, Samatey FA (2013) Function of FlhB, a membrane potein impocated in the bacterial flagellar type III secretion system. PLoS One 8: e68384. doi: 10.1371/journal.pone.0068384 PMID: 23874605
35. Minamino T, Kinoshita M, Hara N, Takeuchi S, Hida A, Koya S, et al. (2012) Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol Microbiol 83: 775-788. doi: 10.1111/j.1365-2958.2011.07964.x PMID: 22233518
36. Claret L, Calder SR, Higgins M, Hughes C (2003) Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol Microbiol 48: 1349-1355. PMID: 12787361
37. Kazetani K, Minamino T, Miyata T, Kato T, Namba K (2009) ATP-induced hexamerization facilitates bacterial flagellar protein export. Biochem Biophys Res Comm 388: 323-327. doi: 10.1016/j.bbrc. 2009.08.004 PMID: 19665005
38. Erhardt M, Namba K, Hughes KT (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2: a000299. doi: 10.1101/cshperspect.a000299 PMID: 20926516
39. Bai F, Morimoto YV, Yoshimura SDJ, Hara N, Kami-ike N, Namba K, et al. (2014) Assembly dynamics and the roles of FliI ATPase of the bacterial flagellar export apparatus. Sci Rep 4: 6528. doi: 10.1038/srep06528 PMID: 25284201
40. Auvray F, Ozin AJ, Claret L, Hughes C (2002) Intrinsic membrane targeting of the flagellar export ATPase FliI: Interaction with acidic phospholipids and FliH. J Mol Biol 318: 941-950. PMID: 12054792