Studies of dynamic protein-protein interactions in bacteria using renilla luciferase complementation are undermined by nonspecific enzyme inhibition

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Hatzios, Stavroula K ^a,b,c   Ringgaard, Simon ^a,b,c   Davis, Brigid M ^a,b,c   Waldor, Matthew K ^a,b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; CHEY PROTEIN; CHEY3 PROTEIN; COELENTERAZINE; GLUCOSE; LUCIFERASE; LUMINESCENT AGENT; MANNOSE; NICKEL CHLORIDE; PHOSPHATASE; PROTEIN CHEZ; SERINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BIOLUMINESCENCE; CHEMOTAXIS; CHEY3 GENE; CHEZ GENE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; LIMIT OF DETECTION; LUCIFERASE FRAGMENT COMPLEMENTATION ASSAY; NONHUMAN; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUALITATIVE ANALYSIS; RENILLA; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

ANIMALS; BACTERIA; BACTERIAL PROTEINS; CHEMOTAXIS; ENZYME INHIBITORS; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; LUCIFERASES; MEMBRANE PROTEINS; MUTATION; PEPTIDE FRAGMENTS; PLASMIDS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RENILLA; VIBRIO CHOLERAE;

EID: 84865050106     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043175     Document Type: Article

References (36)

1. Bouveret E, Brun C, ((2012)) Bacterial interactomes: from interactions to networks. Methods Mol Biol 804:: 15--33.
2. Stynen B, Tournu H, Tavernier J, Van Dijck P, ((2012)) Diversity in genetic in vivo methods for protein-protein interaction studies: from the yeast two-hybrid system to the Mammalian split-luciferase system. Microbiol Mol Biol Rev 76:: 331--382.
3. Villalobos V, Naik S, Piwnica-Worms D, ((2007)) Current state of imaging protein-protein interactions in vivo with genetically encoded reporters. Annu Rev Biomed Eng 9:: 321--349.
4. Ciruela F, ((2008)) Fluorescence-based methods in the study of protein-protein interactions in living cells. Curr Opin Biotechnol 19:: 338--343.
5. Sourjik V, Vaknin A, Shimizu TS, Berg HC, ((2007)) In vivo measurement by FRET of pathway activity in bacterial chemotaxis. Methods Enzymol 423:: 365--391.
6. Ozawa T, Kaihara A, Sato M, Tachihara K, Umezawa Y, ((2001)) Split luciferase as an optical probe for detecting protein-protein interactions in mammalian cells based on protein splicing. Anal Chem 73:: 2516--2521.
7. Paulmurugan R, Gambhir SS, ((2003)) Monitoring protein-protein interactions using split synthetic Renilla luciferase protein-fragment-assisted complementation. Anal Chem 75:: 1584--1589.
8. Kaihara A, Kawai Y, Sato M, Ozawa T, Umezawa Y, ((2003)) Locating a protein-protein interaction in living cells via split Renilla luciferase complementation. Anal Chem 75:: 4176--4181.
9. Luker KE, Smith MC, Luker GD, Gammon ST, Piwnica-Worms H, et al. ((2004)) Kinetics of regulated protein-protein interactions revealed with firefly luciferase complementation imaging in cells and living animals. Proc Natl Acad Sci U S A 101:: 12288--12293.
10. Remy I, Michnick SW, ((2006)) A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat Methods 3:: 977--979.
11. Stefan E, Aquin S, Berger N, Landry CR, Nyfeler B, et al. ((2007)) Quantification of dynamic protein complexes using Renilla luciferase fragment complementation applied to protein kinase A activities in vivo. Proc Natl Acad Sci U S A 104:: 16916--16921.
12. Villalobos V, Naik S, Bruinsma M, Dothager RS, Pan MH, et al. ((2010)) Dual-color click beetle luciferase heteroprotein fragment complementation assays. Chem Biol 17:: 1018--1029.
13. Wille T, Blank K, Schmidt C, Vogt V, Gerlach RG, ((2012)) Gaussia princeps luciferase as a reporter for transcriptional activity, protein secretion, and protein-protein interactions in Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 78:: 250--257.
14. Shimizu TS, Delalez N, Pichler K, Berg HC, ((2006)) Monitoring bacterial chemotaxis by using bioluminescence resonance energy transfer: absence of feedback from the flagellar motors. Proc Natl Acad Sci U S A 103:: 2093--2097.
15. Wood KV, DeLuca M, ((1987)) Photographic detection of luminescence in Escherichia coli containing the gene for firefly luciferase. Anal Biochem 161:: 501--507.
16. Jawhara S, Mordon S, ((2004)) In vivo imaging of bioluminescent Escherichia coli in a cutaneous wound infection model for evaluation of an antibiotic therapy. Antimicrob Agents Chemother 48:: 3436--3441.
17. Armitage JP, ((1999)) Bacterial tactic responses. Adv Microb Physiol 41:: 229--289.
18. Butler SM, Camilli A, ((2005)) Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3:: 611--620.
19. Boin MA, Austin MJ, Hase CC, ((2004)) Chemotaxis in Vibrio cholerae. FEMS Microbiol Lett 239:: 1--8.
20. Lee SH, Butler SM, Camilli A, ((2001)) Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci U S A 98:: 6889--6894.
21. Adler J, ((1973)) A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol 74:: 77--91.
22. Armstrong JB, Adler J, Dahl MM, ((1967)) Nonchemotactic mutants of Escherichia coli. J Bacteriol 93:: 390--398.
23. Sourjik V, Berg HC, ((2002)) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci U S A 99:: 123--127.
24. Ringgaard S, Schirner K, Davis BM, Waldor MK, ((2011)) A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins. Genes Dev 25:: 1544--1555.
25. Donnenberg MS, Kaper JB, ((1991)) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59:: 4310--4317.
26. Miller VL, Mekalanos JJ, ((1988)) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170:: 2575--2583.
27. Loening AM, Fenn TD, Wu AM, Gambhir SS, ((2006)) Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. Protein Eng Des Sel 19:: 391--400.
28. Barak R, Yan J, Shainskaya A, Eisenbach M, ((2006)) The chemotaxis response regulator CheY can catalyze its own acetylation. J Mol Biol 359:: 251--265.
29. Freter R, O'Brien PC, ((1981)) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: chemotactic responses of Vibrio cholerae and description of motile nonchemotactic mutants. Infect Immun 34:: 215--221.
30. Butler SM, Nelson EJ, Chowdhury N, Faruque SM, Calderwood SB, et al. ((2006)) Cholera stool bacteria repress chemotaxis to increase infectivity. Mol Microbiol 60:: 417--426.
31. Porter SL, Wadhams GH, Armitage JP, ((2011)) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9:: 153--165.
32. Tso WW, Adler J, ((1974)) Negative chemotaxis in Escherichia coli. J Bacteriol 118:: 560--576.
33. Auld DS, Southall NT, Jadhav A, Johnson RL, Diller DJ, et al. ((2008)) Characterization of chemical libraries for luciferase inhibitory activity. J Med Chem 51:: 2372--2386.
34. Thorne N, Auld DS, Inglese J, ((2010)) Apparent activity in high-throughput screening: origins of compound-dependent assay interference. Curr Opin Chem Biol 14:: 315--324.
35. Thorne N, Inglese J, Auld DS, ((2010)) Illuminating insights into firefly luciferase and other bioluminescent reporters used in chemical biology. Chem Biol 17:: 646--657.
36. Herbst KJ, Allen MD, Zhang J, ((2009)) The cAMP-dependent protein kinase inhibitor H-89 attenuates the bioluminescence signal produced by Renilla luciferase. PLoS One 4:: e5642.