Systematic identification of hypothetical bacteriophage proteins targeting key protein complexes of Pseudomonas aeruginosa

Journal of Proteome Research

Volumn 13, Issue 10, 2014, Pages 4446-4456

  Van Den Bossche, An ^a   Ceyssens, Pieter Jan ^a,d   De Smet, Jeroen ^a   Hendrix, Hanne ^a   Bellon, Hannelore ^a,e   Leimer, Nadja ^a,f   Wagemans, Jeroen ^a   Delattre, Anne Sophie ^a   Cenens, William ^a   Aertsen, Abram ^a   Landuyt, Bart ^a   Minakhin, Leonid ^b   Severinov, Konstantin ^b   Noben, Jean Paul ^c   Lavigne, Rob ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b RUTGERS UNIVERSITY   (United States)

^c HASSELT UNIVERSITY   (Belgium)

^d SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^f UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

affinity purifications; Bacteriophages; functional annotation; interactomics; P. aeruginosa

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN; GLYCOPROTEIN GP 12; RNA; RNA POLYMERASE; UNCLASSIFIED DRUG; AFFINITY LABELING; PROTEIN BINDING; VIRUS PROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIOPHAGE; CELL DIVISION; CONTROLLED STUDY; DNA REPLICATION; ENERGY METABOLISM; FATTY ACID SYNTHESIS; GENETIC TRANSCRIPTION; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; REGULATORY MECHANISM; WESTERN BLOTTING; AFFINITY CHROMATOGRAPHY; AFFINITY LABELING; METABOLISM; TANDEM MASS SPECTROMETRY;

AFFINITY LABELS; BACTERIAL PROTEINS; BACTERIOPHAGES; BLOTTING, WESTERN; CHROMATOGRAPHY, AFFINITY; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; TANDEM MASS SPECTROMETRY; VIRAL PROTEINS;

EID: 84907821771     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500796n     Document Type: Article

References (74)

1. Hatfull, G. F.; Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) Program; KwaZulu-Natal Research Institute for Tuberculosis and HIV (K-RITH) Mycobacterial Genetics Course; University of California-Los Angeles Research Immersion Laboratory in Virology; Phage Hunters Integrating Research and Education (PHIRE) Program Complete genome sequences of 63 mycobacteriophages Genome Announce. 2013, 1, 1-3
2. Ceyssens, P.-J.; Lavigne, R. Bacteriophages of Pseudomonas Future Microbiol. 2010, 5, 1-15
3. Altschup, S. F.; Gish, W.; Millers, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool J. Mol. Biol. 1990, 215, 403-410
4. Punta, M.; Coggill, P. C.; Eberhardt, R. Y.; Mistry, J.; Tate, J.; Boursnell, C.; Pang, N.; Forslund, K.; Ceric, G.; Clements, J. The Pfam protein families database Nucleic Acids Res. 2012, 40, D290-301
5. Söding, J.; Biegert, A.; Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 2005, 33, W244-8
6. Kelley, L. A.; Sternberg, M. J. E. Protein structure prediction on the Web: a case study using the Phyre server Nat. Protoc. 2009, 4, 363-371
7. Roucourt, B.; Lavigne, R. The role of interactions between phage and bacterial proteins within the infected cell: a diverse and puzzling interactome Environ. Microbiol. 2009, 11, 2789-2805
8. Koskella, B.; Brockhurst, M. A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities FEMS Microbiol. Rev. 2014, 10.1111/1574-6976.12072
9. Flores, C. O.; Meyer, J. R.; Valverde, S.; Farr, L.; Weitz, J. S. Statistical structure of host-phage interactions Proc. Natl. Acad. Sci. U.S.A. 2011, 108, E288-97
10. Gómez, P.; Buckling, A. Bacteria-phage antagonistic coevolution in soil Science 2011, 332, 106-109
11. Liu, J.; Dehbi, M.; Moeck, G.; Arhin, F.; Bauda, P.; Bergeron, D.; Callejo, M.; Ferretti, V.; Ha, N.; Kwan, T. Antimicrobial drug discovery through bacteriophage genomics Nat. Biotechnol. 2004, 22, 185-191
12. Yano, S. T.; Rothman-Denes, L. B. A phage-encoded inhibitor of Escherichia coli DNA replication targets the DNA polymerase clamp loader Mol. Microbiol. 2011, 79, 1325-1338
13. Wagemans, J.; Lavigne, R. Phages and their hosts, a web of interactions-applications to drug design; Bacteriophages in Health and Disease; Hyman, P.; Abedon, S. T., Eds.; CABI: Cambridge, MA, 2012; pp 119-133.
14. Lu, L. J.; Sboner, A.; Huang, Y. J.; Lu, H. X.; Gianoulis, T. A.; Yip, K. Y.; Kim, P. M.; Montelione, G. T.; Gerstein, M. B. Comparing classical pathways and modern networks: towards the development of an edge ontology Trends Biochem. Sci. 2007, 32, 320-331
15. Gingras, A.-C.; Gstaiger, M.; Raught, B.; Aebersold, R. Analysis of protein complexes using mass spectrometry Nat. Rev. Mol. Cell Biol. 2007, 8, 645-654
16. Butland, G.; Peregrín-Alvarez, J. M.; Li, J.; Yang, W.; Yang, X.; Canadien, V.; Starostine, A.; Richards, D.; Beattie, B.; Krogan, N. Interaction network containing conserved and essential protein complexes in Escherichia coli Nature 2005, 433, 531-537
17. Gavin, A.-C.; Bösche, M.; Krause, R.; Grandi, P.; Marzioch, M.; Bauer, A.; Schultz, J.; Rick, J. M.; Michon, A.-M.; Cruciat, C.-M. Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 2002, 415, 141-147
18. Krogan, N. J.; Cagney, G.; Yu, H.; Zhong, G.; Guo, X.; Ignatchenko, A.; Li, J.; Pu, S.; Datta, N.; Tikuisis, A. P. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae Nature 2006, 440, 637-643
19. Hidron, A. I.; Edwards, J. R.; Patel, J.; Horan, T. C.; Sievert, D. M.; Pollock, D. a; Fridkin, S. K. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007 Infect. Control Hosp. Epidemiol. 2008, 29, 996-1011
20. Gellatly, S. L.; Hancock, R. E. W. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses Pathog. Dis. 2013, 67, 159-173
21. Centers for Disease Control and Prevention National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004 Am. J. Infect. Control 2004, 32, 470-485
22. Zhang, M.; Su, S.; Bhatnagar, R. K.; Hassett, D. J.; Lu, L. J. Prediction and analysis of the protein interactome in Pseudomonas aeruginosa to enable network-based drug target selection PLoS One 2012, 7, e41202
23. Ceyssens, P.-J.; Minakhin, L.; Van den Bossche, A.; Yakunina, M.; Klimuk, E.; Blasdel, B.; De Smet, J.; Noben, J.-P.; Bläsi, U.; Severinov, K.; Lavigne, R. Development of giant bacteriophage φ KZ is independent of the host transcription apparatus J. Virol. 2014, 88, 10501-10510
24. Ceyssens, P.-J.; Lavigne, R.; Mattheus, W.; Chibeu, A.; Hertveldt, K.; Mast, J.; Robben, J.; Volckaert, G. Genomic analysis of Pseudomonas aeruginosa phages LKD16 and LKA1: establishment of the phiKMV subgroup within the T7 supergroup J. Bacteriol. 2006, 188, 6924-6931
25. Ceyssens, P.-J.; Brabban, A.; Rogge, L.; Lewis, M. S.; Pickard, D.; Goulding, D.; Dougan, G.; Noben, J.-P.; Kropinski, A.; Kutter, E. Molecular and physiological analysis of three Pseudomonas aeruginosa phages belonging to the "N4-like viruses" Virology 2010, 405, 26-30
26. Nechaev, S.; Severinov, K. Bacteriophage-induced modifications of host RNA polymerase Annu. Rev. Microbiol. 2003, 57, 301-322
27. Häuser, R.; Blasche, S.; Dokland, T.; Haggård-Ljungquist, E.; von Brunn, A.; Salas, M.; Casjens, S.; Molineux, I.; Uetz, P. Bacteriophage protein-protein interactions Adv. Virus Res. 2012, 83, 219-298
28. Stover, C. K.; Pham, X. Q.; Erwin, a L.; Mizoguchi, S. D.; Warrener, P.; Hickey, M. J.; Brinkman, F. S.; Hufnagle, W. O.; Kowalik, D. J.; Lagrou, M. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen Nature 2000, 406, 959-964
29. Lesic, B.; Rahme, L. G. Use of the lambda Red recombinase system to rapidly generate mutants in Pseudomonas aeruginosa BMC Mol. Biol. 2008, 9, 20
30. Ceyssens, P.-J.; Mesyanzhinov, V.; Sykilinda, N.; Briers, Y.; Roucourt, B.; Lavigne, R.; Robben, J.; Domashin, A.; Miroshnikov, K.; Volckaert, G. The genome and structural proteome of YuA, a new Pseudomonas aeruginosa phage resembling M6 J. Bacteriol. 2008, 190, 1429-1435
31. Klimuk, E.; Akulenko, N.; Makarova, K.; Ceyssens, P.; Volchenkov, I.; Lavigne, R.; Severinov, K. Host RNA polymerase inhibitors encoded by KMV-like phages of Pseudomonas Virology 2013, 436, 67-74
32. Borukhov, S.; Goldfarb, A. Recombinant Escherichia coli RNA polymerase: purification of individually overexpressed subunits and in vitro assembly Protein Expression Purif. 1993, 4, 503-511
33. Polyakov, A.; Severinova, E.; Darst, S. Three-dimensional structure of E. coli core RNA polymerase: promoter binding and elongation conformations of the enzyme Cell 1995, 83, 365-373
34. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 1996, 68, 850-858
35. Dumont, D.; Noben, J.-P.; Raus, J.; Stinissen, P.; Robben, J. Proteomic analysis of cerebrospinal fluid from multiple sclerosis patients Proteomics 2004, 4, 2117-2124
36. Vizcaíno, J. A.; Deutsch, E. W.; Wang, R.; Csordas, A.; Reisinger, F.; Ríos, D.; Dianes, J. A.; Sun, Z.; Farrah, T.; Bandeira, N. ProteomeXchange provides globally coordinated proteomics data submission and dissemination Nat. Biotechnol. 2014, 32, 223-226
37. Wagemans, J.; Blasdel, B. G.; Van den Bossche, A.; Uytterhoeven, B.; De Smet, J.; Paeshuyse, J.; Cenens, W.; Aertsen, A.; Uetz, P.; Savchenko, A. Functional elucidation of antibacterial phage ORFans targeting Pseudomonas aeruginosa Cell. Microbiol. 2014, 10.1111/cmi.12330
38. Choi, K.-H.; Kumar, A.; Schweizer, H. P. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation J. Microbiol. Methods 2006, 64, 391-397
39. Cenens, W.; Mebrhatu, M. T.; Makumi, A.; Ceyssens, P.-J.; Lavigne, R.; Van Houdt, R.; Taddei, F.; Aertsen, A. Expression of a novel P22 ORFan gene reveals the phage carrier state in Salmonella typhimurium PLoS Genet. 2013, 9, e1003269
40. Karimova, G.; Pidoux, J.; Ullmann, A.; Ladant, D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 5752-5756
41. Claessen, D.; Emmins, R.; Hamoen, L. W.; Daniel, R. a; Errington, J.; Edwards, D. H. Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis Mol. Microbiol. 2008, 68, 1029-1046
42. Zhang, X.; Bremer, H. Control of the Escherichia coli rrnB P1 promoter strength by ppGpp J. Biol. Chem. 1995, 270, 11181-11189
43. Kerrien, S.; Aranda, B.; Breuza, L.; Bridge, A.; Broackes-Carter, F.; Chen, C.; Duesbury, M.; Dumousseau, M.; Feuermann, M.; Hinz, U. The IntAct molecular interaction database in 2012 Nucleic Acids Res. 2012, 40, D841-6
44. Szklarczyk, D.; Franceschini, A.; Kuhn, M.; Simonovic, M.; Roth, A.; Minguez, P.; Doerks, T.; Stark, M.; Muller, J.; Bork, P. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Nucleic Acids Res. 2011, 39, D561-8
45. Hu, J. C.; Sherlock, G.; Siegele, D. A.; Aleksander, S. A.; Ball, C. A.; Demeter, J.; Gouni, S.; Holland, T. A.; Karp, P. D.; Lewis, J. E. PortEco: a resource for exploring bacterial biology through high-throughput data and analysis tools Nucleic Acids Res. 2014, 42, D677-84
46. Schmidt, T. G. M.; Skerra, A. The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins Nat. Protoc. 2007, 2, 1528-1535
47. Renuse, S.; Chaerkady, R.; Pandey, A. Proteogenomics Proteomics 2011, 11, 620-630
48. Venter, E.; Smith, R. D.; Payne, S. H. Proteogenomic analysis of bacteria and archaea: a 46 organism case study PLoS One 2011, 6, e27587
49. Armengaud, J.; Trapp, J.; Pible, O. Non-model organisms, a species endangered by proteogenomics J. Proteomics 2014, 105, 5-18
50. Berggård, T.; Linse, S.; James, P. Methods for the detection and analysis of protein-protein interactions Proteomics 2007, 7, 2833-2842
51. Morita, T.; Maki, K.; Aiba, H. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs Genes Dev. 2005, 19, 2176-2186
52. Ikeda, Y.; Yagi, M.; Morita, T.; Aiba, H. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli Mol. Microbiol. 2011, 79, 419-432
53. De Lay, N.; Gottesman, S. Role of polynucleotide phosphorylase in sRNA function in Escherichia coli RNA 2011, 17, 1172-1189
54. Vogel, J.; Luisi, B. F. Hfq and its constellation of RNA Nat. Rev. Microbiol. 2011, 9, 578-589
55. Milojevic, T.; Grishkovskaya, I.; Sonnleitner, E.; Djinovic-Carugo, K.; Bläsi, U. The Pseudomonas aeruginosa catabolite repression control protein Crc is devoid of RNA binding activity PLoS One 2013, 8, e64609
56. Majorek, K. A.; Dunin-Horkawicz, S.; Steczkiewicz, K.; Muszewska, A.; Nowotny, M.; Ginalski, K.; Bujnicki, J. M. The RNase H-like superfamily: new members, comparative structural analysis and evolutionary classification Nucleic Acids Res. 2014, 42, 4160-4179
57. Rothfield, L.; Justice, S.; Garcia-Lara, J. Bacterial cell division Annu. Rev. Genet. 1999, 33, 423-448
58. Adams, D. W.; Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring Nat. Rev. Microbiol. 2009, 7, 642-653
59. Errington, J.; Daniel, R. A.; Scheffers, D. Cytokinesis in bacteria Micrbiology Mol. Biol. Rev. 2003, 67, 52-65
60. Kraemer, J. A.; Erb, M. L.; Waddling, C. A.; Montabana, E. A.; Zehr, E. A.; Wang, H.; Nguyen, K.; Pham, D. S. L.; Agard, D. A.; Pogliano, J. A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell Cell 2012, 149, 1488-1499
61. Belley, A.; Callejo, M.; Arhin, F.; Dehbi, M.; Fadhil, I.; Liu, J.; McKay, G.; Srikumar, R.; Bauda, P.; Bergeron, D. Competition of bacteriophage polypeptides with native replicase proteins for binding to the DNA sliding clamp reveals a novel mechanism for DNA replication arrest in Staphylococcus aureus Mol. Microbiol. 2006, 62, 1132-1143
62. Court, R.; Cook, N.; Saikrishnan, K.; Wigley, D. The crystal structure of lambda-Gam protein suggests a model for RecBCD inhibition J. Mol. Biol. 2007, 371, 25-33
63. Johnson, A.; O'Donnell, M. Cellular DNA replicases: components and dynamics at the replication fork Annu. Rev. Biochem. 2005, 74, 283-315
64. Kelch, B. A.; Makino, D. L.; O'Donnell, M.; Kuriyan, J. How a DNA polymerase clamp loader opens a sliding clamp Science 2011, 334, 1675-1680
65. Hedglin, M.; Kumar, R.; Benkovic, S. J. Replication clamps and clamp loaders Cold Spring Harbor Perspect. Biol. 2013, 5, a010165
66. Hayner, J. N.; Bloom, L. B. The β sliding clamp closes around DNA prior to release by the Escherichia coli clamp loader γ complex J. Biol. Chem. 2013, 288, 1162-1170
67. White, S. W.; Zheng, J.; Zhang, Y.-M.; Rock, C. O. The structural biology of type II fatty acid biosynthesis Annu. Rev. Biochem. 2005, 74, 791-831
68. Zhang, Y.-M.; White, S. W.; Rock, C. O. Inhibiting bacterial fatty acid synthesis J. Biol. Chem. 2006, 281, 17541-17544
69. Lavigne, R.; Lecoutere, E.; Wagemans, J.; Cenens, W.; Aertsen, A.; Schoofs, L.; Landuyt, B.; Paeshuyse, J.; Scheer, M.; Schobert, M. A multifaceted study of Pseudomonas aeruginosa shutdown by virulent podovirus LUZ19 mBio 2013, 4, 1-8
70. Ladant, D.; Ullman, A. Bordetella pertussis adenylate cyclase: a toxin with multiple talents Trends Microbiol. 1999, 7, 172-176
71. Blatter, E. E.; Ross, W.; Tang, H.; Gourse, R. L.; Ebright, R. H. Domain organization of RNA polymerase alpha subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding Cell 1994, 78, 889-896
72. Gourse, R. L.; Ross, W.; Gaal, T. UPs and downs in bacterial transcription initiation: the role of the alpha subunit of RNA polymerase in promoter recognition Mol. Microbiol. 2000, 37, 687-695
73. Wilkens, K.; Tiemann, B.; Bazan, F.; Rüger, W. ADP-ribosylation and early transcription regulation by bacteriophage T4 Adv. Exp. Med. Biol. 1997, 419, 71-82
74. Osmundson, J.; Montero-Diez, C.; Westblade, L. F.; Hochschild, A.; Darst, S. A. Promoter-specific transcription inhibition in Staphylococcus aureus by a phage protein Cell 2012, 151, 1005-1016