Identification of Api88 Binding Partners in Escherichia coli Using a Photoaffinity-Cross-Link Strategy and Label-Free Quantification

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3274-3283

  Volke, Daniela ^a   Krizsan, Andor ^a   Berthold, Nicole ^a   Knappe, Daniel ^a   Hoffmann, Ralf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

70 kDa bacterial heat shock protein DnaK; apidaecin; mass spectrometry; proline rich antimicrobial peptide (PrAMP); protein targets; ribosome

Indexed keywords

API88 PROTEIN; APIDAECIN 1B; DEAD BOX PROTEIN; DNA DIRECTED RNA POLYMERASE; PROTEIN; PROTEIN DNAK; PYRUVATE DEHYDROGENASE; RIBOSOME PROTEIN; STREPTAVIDIN; TRANSKETOLASE; TRANSKETOLASE 1; TRYPSIN; UNCLASSIFIED DRUG; 4-BENZOYLPHENYLALANINE; ANTIMICROBIAL CATIONIC PEPTIDE; APIDAECIN; BENZOPHENONE DERIVATIVE; CROSS LINKING REAGENT; ESCHERICHIA COLI PROTEIN; INSECT PROTEIN; PHENYLALANINE; PROTEIN BINDING; TYROSINE;

AFFINITY CHROMATOGRAPHY; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOTINYLATION; CELL LYSATE; CONTROLLED STUDY; CROSS LINKING; DISSOCIATION CONSTANT; ESCHERICHIA COLI; HONEYBEE; IN VITRO STUDY; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONTENT; PROTEIN INTERACTION; PROTEIN SYNTHESIS; PURINE METABOLISM; TIME OF FLIGHT MASS SPECTROMETRY; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; DRUG EFFECTS; ELECTROSPRAY MASS SPECTROMETRY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR GENETICS; PROCEDURES; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RADIATION RESPONSE; TANDEM MASS SPECTROMETRY; ULTRAVIOLET RADIATION;

APIS MELLIFERA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HEXAPODA; MAMMALIA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BENZOPHENONES; BLOTTING, WESTERN; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROSS-LINKING REAGENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; INSECT PROTEINS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PHENYLALANINE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEOMICS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; TYROSINE; ULTRAVIOLET RAYS;

EID: 84938790594     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00283     Document Type: Article

References (38)

1. Clatworthy, A. E.; Pierson, E.; Hung, D. T. Targeting virulence: a new paradigm for antimicrobial therapy Nat. Chem. Biol. 2007, 3, 541-8 10.1038/nchembio.2007.24
2. Fox, J. L. Antimicrobial peptides stage a comeback Nat. Biotechnol. 2013, 31 (5) 379-82 10.1038/nbt.2572
3. Casteels, P.; Ampe, C.; Jacobs, F.; Vaeck, M.; Tempst, P. Apidaecins: antibacterial peptides from honeybees EMBO J. 1989, 8, 2387-2391
4. Bulet, P.; Dimarcq, J.-L.; Hetru, C.; Lagueux, M.; Charlet, M.; Hegy, G.; van Dorsselaer, A.; Hoffmann, J. A. A novel inducible antibacterial peptide from Drosophila carries an O-glycosylated substitution J. Biol. Chem. 1993, 268, 14893-14897
5. Cociancich, S.; Dupont, A.; Hegyi, G.; Lanot, R.; Holder, F.; Hetru, C.; Hoffmann, J. A.; Bulet, P. Novel inducible antibacterial peptides from a hernipteran insect, the sap sucking-bug Pyrrhocoris apterus Biochem. J. 1994, 300, 567-575
6. Otvos, L. Antibacterial Peptides Isolated from Insects J. Pept. Sci. 2000, 6, 497-511 10.1002/1099-1387(200010)6:10<497::AID-PSC277>3.3.CO;2-N
7. Gennaro, R.; Skerlavaj, B.; Romeo, D. Purification, composition, and activity of two bactenecins, antibacterial peptides of bovine neutrophils Infect. Immun. 1989, 57, 3142-3146
8. Boman, H. G.; Agerberth, B.; Boman, A. Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine Infect. Immun. 1993, 61, 2978-2984
9. Shamova, O.; Brogden, K. A.; Zhao, C.; Nguyen, T.; Kokryakov, V. N.; Lehrer, R. I. Purification and properties of proline-rich antimicrobial peptides from sheep and goat leukocytes Infect. Immun. 1999, 67, 4106-4111
10. Benincasa, M.; Pelillo, C.; Zorzet, S.; Garrovo, C.; Biffi, S.; Gennaro, R.; Scocchi, M. The proline-rich peptide Bac7(1-35) reduces mortality from Salmonella typhimurium in a mouse model of infection BMC Microbiol. 2010, 10 (1) 178 10.1186/1471-2180-10-178
11. Ostorhazi, E.; Holub, M. C.; Rozgonyi, F.; Harmos, F.; Cassone, M.; Wade, J. D.; Otvos, L. Broad-spectrum antimicrobial efficacy of peptide A3-APO in mouse models of multidrug-resistant wound and lung infections cannot be explained by in vitro activity against the pathogens involved Int. J. Antimicrob. Agents 2011, 37 (5) 480-484 10.1016/j.ijantimicag.2011.01.003
12. Knappe, D.; Fritsche, S.; Alber, G.; Kohler, G.; Hoffmann, R.; Müller, U. Oncocin derivative Onc72 is highly active against Escherichia coli in a systemic septicaemia infection mouse model J. Antimicrob. Chemother. 2012, 67 (10) 2445-2451 10.1093/jac/dks241
13. Czihal, P.; Knappe, D.; Fritsche, S.; Zahn, M.; Berthold, N.; Piantavigna, S.; Müller, U.; van Dorpe, S.; Herth, N.; Binas, A.; Köhler, G.; Spiegeleer, B.; de Martin, L. L.; Nolte, O.; Sträter, N.; Alber, G.; Hoffmann, R. Api88 is a novel antibacterial designer Peptide to treat systemic infections with multidrug-resistant gram-negative pathogens ACS Chem. Biol. 2012, 7, 1281-1291 10.1021/cb300063v
14. Ostorházi, E.; Nemes-Nikodém, é.; Knappe, D.; Hoffmann, R. In vivo activity of optimized apidaecin and oncocin peptides against a multiresistant, KPC-producing Klebsiella pneumoniae strain Prot. Pept. Lett. 2014, 21, 368-73
15. Otvos, L., Jr.; Flick-Smith, H.; Fox, M.; Ostorhazi, E.; Dawson, R. M.; Wade, J. D. The Designer Proline-rich Antibacterial Peptide A3-APO Prevents Bacillus anthracis Mortality by Deactivating Bacterial Toxins Protein Pept Lett. 2014, 21 (4) 374-81
16. Mattiuzzo, M.; Bandiera, A.; Gennaro, R.; Benincasa, M.; Pacor, S.; Antcheva, N.; Scocchi, M. Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides Mol. Microbiol. 2007, 66, 151-163 10.1111/j.1365-2958.2007.05903.x
17. Arnold, MF1; Caro-Hernandez, P.; Tan, K.; Runti, G.; Wehmeier, S.; Scocchi, M.; Doerrler, W. T.; Walker, G. C.; Ferguson, G. P. Enteric YaiW is a surface-exposed outer membrane lipoprotein that affects sensitivity to an antimicrobial peptide J. Bacteriol. 2014, 196 (2) 436-444 10.1128/JB.01179-13
18. Kragol, G.; Lovas, S.; Varadi, G.; Condie, B. A.; Hoffmann, R.; Otvos, L., Jr. The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding Biochemistry 2001, 40 (10) 3016-26 10.1021/bi002656a
19. Zahn, M.; Kieslich, B.; Berthold, N.; Knappe, D.; Hoffmann, R. Structural identification of DnaK binding sites within bovine and sheep bactenecin Bac7 Prot. Pept. Lett. 2014, 21, 407-12
20. Zahn, M.; Berthold, N.; Kieslich, B.; Knappe, D.; Hoffmann, R.; Strater, N. Structural studies on the forward and reverse binding modes of peptides to the chaperone DnaK J. Mol. Biol. 2013, 425, 2463-79 10.1016/j.jmb.2013.03.041
21. Knappe, D.; Zahn, M.; Sauer, U.; Schiffer, G.; Sträter, N.; Hoffmann, R. Rational Design of Oncocin derivatives with Superior Protease Stabilities and Antibacterial Activities Based on the High-Resolution Structure of the Oncocin-DnaK-Complex ChemBioChem 2011, 12 (6) 874-6 10.1002/cbic.201000792
22. Zhou, Y.; Chen, W. N. iTRAQ-coupled 2-D LC-MS/MS analysis of cytoplasmic protein profile in Escherichia coli incubated with apidaecin IB J. Proteomics 2011, 75 (2) 511-6 10.1016/j.jprot.2011.08.015
23. Zhou, Y.; Chen, W. N. iTRAQ-coupled 2-D LC-MS/MS analysis of membrane protein profile in Escherichia coli incubated with apidaecin IB PLoS One 2011, 6 (6) e20442 10.1371/journal.pone.0020442
24. Boucard, A. A.; Wilkes, B. C.; Laporte, S. A.; Escher, E.; Guillemette, G.; Leduc, R. Photolabeling identifies position 172 of the human AT(1) receptor as a ligand contact point: receptor-bound angiotensin II adopts an extended structure Biochemistry 2000, 39 (32) 9662-70 10.1021/bi000597v
25. Jossart, C.; Coupal, M.; McNicoll, N.; Fournier, A.; Wilkes, B. C.; De Léan, A. Photolabeling study of the ligand binding domain of natriuretic peptide receptor A: development of a model Biochemistry 2005, 44 (7) 2397-408 10.1021/bi048251y
26. Berthold, N.; Czihal, P.; Fritsche, S.; Sauer, U.; Schiffer, G.; Knappe, D.; Alber, G.; Hoffmann, R. Novel apidaecin 1b analogs with superior serum stabilities for treatment of Gram-negative pathogens Antimicrob. Agents Chemother. 2013, 57, 402-9 10.1128/AAC.01923-12
27. Scocchi, M.; Lüthy, C.; Decarli, P.; Mignogna, G.; Christen, P.; Gennaro, R. The Proline-rich Antibacterial Peptide Bac7 Binds to and Inhibits in vitro the Molecular Chaperone DnaK Int. J. Pept. Res. Ther. 2009, 15, 147-155 10.1007/s10989-009-9182-3
28. Ladner, C. L.; Yang, J.; Turner, R. J.; Edwards, R. A. Visible fluorescent detection of proteins in polyacrylamide gels without staining Anal. Biochem. 2004, 326, 13-20 10.1016/j.ab.2003.10.047
29. Neuhoff, V.; Stamm, R.; Eibel, H. Clear background and highly sensitive protein staining with Coomassie Blue dyes in polyacrylamide gels: A systematic analysis Electrophoresis 1985, 6, 427-448 10.1002/elps.1150060905
30. Lepetit, B.; Volke, D.; Szabó, M.; Hoffmann, R.; Garab, G.; Wilhelm, C.; Goss, R. Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum Biochemistry 2007, 46 (34) 9813-22 10.1021/bi7008344
31. Li, G.-Z.; Vissers, J. P. C.; Silva, J. C.; Golick, D.; Gorenstein, M. V.; Geromanos, S. J. Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures Proteomics 2009, 9, 1696-1719 10.1002/pmic.200800564
32. Berthold, N.; Hoffmann, R. Cellular uptake of apidaecin 1b and related analogs in Gram-negative bacteria reveals novel antibacterial mechanism for proline-rich antimicrobial peptides Protein Pept. Lett. 2014, 21, 391-8
33. Franceschini, A.; Szklarczyk, D.; Frankild, S.; Kuhn, M.; Simonovic, M.; Roth, A.; Lin, J.; Minguez, P.; Bork, P.; von Mering, C.; Jensen, L. J. STRING v9.1: protein-protein interaction networks, with increased coverage and integration Nucleic Acids Res. 2013, 41 (Database issue) D808-D815 10.1093/nar/gks1094
34. Brohée, S.; van Helden, J. Evaluation of clustering algorithms for protein-protein interaction networks BMC Bioinf. 2006, 7, 488 10.1186/1471-2105-7-488
35. Otvos, L., Jr. The short proline-rich antibacterial peptide family Cell. Mol. Life Sci. 2002, 59 (7) 1138-50 10.1007/s00018-002-8493-8
36. Krizsan, A.; Volke, D.; Weinert, S.; Sträter, N.; Knappe, D.; Hoffmann, R. Insect derived proline-rich antimicrobial peptides kill bacteria by inhibiting bacterial protein translation at the 70S ribosome Angew. Chem., Int. Ed. 2014, 53, 12236-9 10.1002/anie.201407145
37. Mardirossian, M.; Grzela, R.; Giglione, C.; Meinnel, T.; Gennaro, R.; Mergaert, P.; Scocchi, M. The Host Antimicrobial Peptide Bac71-35 Binds to Bacterial Ribosomal Proteinsand Inhibits Protein Synthesis Chem. Biol. 2014, 21 (12) 1639-1647 10.1016/j.chembiol.2014.10.009
38. Genevaux, P.; Georgopoulos, C.; Kelley, W. L. The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions Mol. Microbiol. 2007, 66 (4) 840-57 10.1111/j.1365-2958.2007.05961.x