Comparative proteomic analysis reveals new components of the PhoP regulon and highlights a role for PhoP in the regulation of genes encoding the F1F0 ATP synthase in Edwardsiella tarda

Microbiology (United Kingdom)

Volumn 159, Issue PART7, 2013, Pages 1340-1351

  Lv, Yuanzhi ^a   Yin, Kaiyu ^a   Shao, Shuai ^a   Wang, Qiyao ^a   Zhang, Yuanxing ^a  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; MESSENGER RNA; PHOP PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AMINO ACID METABOLISM; AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIOGENESIS; CARBOHYDRATE TRANSPORT; DELETION MUTANT; EDWARDSIELLA TARDA; ENERGY YIELD; GEL MOBILITY SHIFT ASSAY; GENE CLUSTER; GENE CONTROL; NONHUMAN; OPERON; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACTERIAL PROTEINS; EDWARDSIELLA TARDA; ENTEROBACTERIACEAE INFECTIONS; FISH DISEASES; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; OPERON; PROTEOMICS; REGULON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ZEBRAFISH;

EDWARDSIELLA TARDA;

EID: 84879828156     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.066803-0     Document Type: Article

References (48)

1. Abbott, S. L. & Janda, J. M. (2006). The genus Edwardsiella. In Proteobacteria: Gamma Class (The Prokaryotes, 3rd edn, vol. 6), pp. 72-89. Edited by M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Sackebrandt. New York: Springer
2. Alkhuder, K., Meibom, K. L., Dubail, I., Dupuis, M. & Charbit, A. (2009). Glutathione provides a source of cysteine essential for intracellular multiplication of Francisella tularensis. PLoS Pathog 5, e1000284.
3. Banbula, A., Potempa, J., Travis, J., Fernandez-Catalén, C., Mann, K., Huber, R., Bode, W. & Medrano, F. J. (1998). Amino-acid sequence and three-dimensional structure of the Staphylococcus aureus metalloproteinase at 1.72 ° resolution. Structure 6, 1185-1193.
4. Bjur, E., Eriksson-Ygberg, S., Aslund, F. & Rhen, M. (2006). Thioredoxin 1 promotes intracellular replication and virulence of Salmonella enterica serovar Typhimurium. Infect Immun 74, 5140- 5151.
5. Calloni, G., Chen, T., Schermann, S. M., Chang, H. C., Genevaux, P., Agostini, F., Tartaglia, G. G., Hayer-Hartl, M. & Hartl, F. U. (2012). DnaK functions as a central hub in the E. coli chaperone network. Cell Rep 1, 251-264.
6. Carmel-Harel, O. & Storz, G. (2000). Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54, 439-461.
7. 2+ sensing by a novel PhoP- PhoQ two-component system for regulation of virulence in Edwardsiella tarda. J Biol Chem 285, 38876-38888.
8. Charles, R. C., Harris, J. B., Chase, M. R., Lebrun, L. M., Sheikh, A., LaRocque, R. C., Logvinenko, T., Rollins, S. M., Tarique, A. & other authors (2009). Comparative proteomic analysis of the PhoP regulon in Salmonella enterica serovar Typhi versus Typhimurium. PLoS ONE 4, e6994.
9. Cordwell, S. J. (2006). Technologies for bacterial surface proteomics. Curr Opin Microbiol 9, 320-329.
10. Di Pasqua, R., Mamone, G., Ferranti, P., Ercolini, D. & Mauriello, G. (2010). Changes in the proteome of Salmonella enterica serovar Thompson as stress adaptation to sublethal concentrations of thymol. Proteomics 10, 1040-1049.
11. Eisenreich, W., Dandekar, T., Heesemann, J. & Goebel, W. (2010). Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8, 401-412.
12. Faucher, S. P., Porwollik, S., Dozois, C. M., McClelland, M. & Daigle, F. (2006). Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci U S A 103, 1906-1911.
13. Grcia-del Portillo, F., Foster, J. W. & Finlay, B. B. (1993). Role of acid tolerance response genes in Salmonella typhimurium virulence. Infect Immun 61, 4489-4492.
14. Groisman, E. A. (2001). The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183, 1835-1842.
15. Hansen, A. M., Qiu, Y., Yeh, N., Blattner, F. R., Durfee, T. & Jin, D. J. (2005). SspA is required for acid resistance in stationary phase by downregulation of H-NS in Escherichia coli. Mol Microbiol 56, 719- 734.
16. Herrero, M., de Lorenzo, V. & Timmis, K. N. (1990). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram- negative bacteria. J Bacteriol 172, 6557-6567.
17. Hohmann, E. L., Oletta, C. A., Killeen, K. P. & Miller, S. I. (1996). phoP/ phoQ-deleted Salmonella typhi (Ty800) is a safe and immunogenic single- dose typhoid fever vaccine in volunteers. J Infect Dis 173, 1408-1414.
18. Horzempa, J., Carlson, P. E., Jr, O'Dee, D. M., Shanks, R. M. Q. & Nau, G. J. (2008). Global transcriptional response to mammalian temperature provides new insight into Francisella tularensis patho- genesis. BMC Microbiol 8, 172.
19. Jones, H. M., Brajkovich, C. M. & Gunsalus, R. P. (1983). In vivo 59 terminus and length of the mRNA for the proton-translocating ATPase (unc) operon of Escherichia coli. J Bacteriol 155, 1279-1287.
20. Kato, A., Groisman, E. A. & Howard Hughes Medical Institute., (2008). The PhoQ/PhoP regulatory network of Salmonella enterica. Adv Exp Med Biol 631, 7-21.
21. Koháryová, M. & Kolárová, M. (2008). Oxidative stress and thioredoxin system. Gen Physiol Biophys 27, 71-84.
22. Laarman, A. J., Ruyken, M., Malone, C. L., van Strijp, J. A. G., Horswill, A. R. & Rooijakkers, S. H. M. (2011). Staphylococcus aureus metalloprotease aureolysin cleaves complement C3 to mediate immune evasion. J Immunol 186, 6445-6453.
23. -DDCT Method. Methods 25, 402-408.
24. Lv, Y., Xiao, J., Liu, Q., Wu, H., Zhang, Y. & Wang, Q. (2012a). Systematic mutation analysis of two-component signal transduction systems reveals EsrA-EsrB and PhoP-PhoQ as the major virulence regulators in Edwardsiella tarda. Vet Microbiol 157, 190-199.
25. Lv, Y., Zheng, J., Yang, M., Wang, Q. & Zhang, Y. (2012b). An Edwardsiella tarda mutant lacking UDP-glucose dehydrogenase shows pleiotropic phenotypes, attenuated virulence, and potential as a vaccine candidate. Vet Microbiol 160, 506-512.
26. McEntire, J. C., Carman, G. M. & Montville, T. J. (2004). Increased ATPase activity is responsible for acid sensitivity of nisin-resistant Listeria monocytogenes ATCC 700302. Appl Environ Microbiol 70, 2717-2721.
27. Mohanty, B. R. & Sahoo, P. K. (2007). Edwardsiellosis in fish: a brief review. J Biosci 32 (S3), 1331-1344.
28. Muñ oz-Elías, E. J. & McKinney, J. D., (2006). Carbon metabolism of intracellular bacteria. Cell Microbiol 8, 10-22.
29. Northen, H., Paterson, G. K., Constantino-Casas, F., Bryant, C. E., Clare, S., Mastroeni, P., Peters, S. E. & Maskell, D. J. (2010). Salmonella enterica serovar Typhimurium mutants completely lacking the F0F1 ATPase are novel live attenuated vaccine strains. Vaccine 28, 940-949.
30. Park, S. B., Aoki, T. & Jung, T. S. (2012). Pathogenesis of and strategies for preventing Edwardsiella tarda infection in fish. Vet Res 43, 67.
31. 2+ homeostasis. PLoS Genet 5, e1000428.
32. Powell, J. T. & Morrison, J. F. (1978). The purification and properties of the aspartate aminotransferase and aromatic-amino-acid amino- transferase from Escherichia coli. Eur J Biochem 87, 391-400.
33. Pressley, M. E., Phelan, P. E., III, Witten, P. E., Mellon, M. T. & Kim, C. H. (2005). Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev Comp Immunol 29, 501-513.
34. Reed, L. J. & Muench, H. (1938). A simple method of estimating fifty percent endpoints. Am J Epidemiol 27, 493-497.
35. Sem, X. H. & Rhen, M. (2012). Pathogenicity of Salmonella enterica in Caenorhabditis elegans relies on disseminated oxidative stress in the infected host. PLoS ONE 7, e45417.
36. Sieprawska-Lupa, M., Mydel, P., Krawczyk, K., Wójcik, K., Puklo, M., Lupa, B., Suder, P., Silberring, J., Reed, M. & other authors (2004). Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob Agents Chemother 48, 4673-4679.
37. Srinivasa Rao, P. S., Yamada, Y. & Leung, K. Y. (2003). A major catalase (KatB) that is required for resistance to H2O2 and phagocyte- mediated killing in Edwardsiella tarda. Microbiology 149, 2635-2644.
38. Tozzi, M. G., Camici, M., Mascia, L., Sgarrella, F. & Ipata, P. L. (2006). Pentose phosphates in nucleoside interconversion and catabolism. FEBS J 273, 1089-1101.
39. Tran, S. L. & Cook, G. M. (2005). The F1F0-ATP synthase of Mycobacterium smegmatis is essential for growth. J Bacteriol 187, 5023-5028.
40. Turnbull, A. L. & Surette, M. G. (2010). Cysteine biosynthesis, oxidative stress and antibiotic resistance in Salmonella typhimurium. Res Microbiol 161, 643-650.
41. von Ballmoos, C., Wiedenmann, A. & Dimroth, P. (2009). Essentials for ATP synthesis by F1F0 ATP synthases. Annu Rev Biochem 78, 649- 672.
42. Wang, Q., Yang, M., Xiao, J., Wu, H., Wang, X., Lv, Y., Xu, L., Zheng, H., Wang, S. & other authors (2009a). Genome sequence of the versatile fish pathogen Edwardsiella tarda provides insights into its adaptation to broad host ranges and intracellular niches. PLoS ONE 4, e7646.
43. Wang, S., Deng, K., Zaremba, S., Deng, X., Lin, C., Wang, Q., Tortorello, M. L. & Zhang, W. (2009b). Transcriptomic response of Escherichia coli O157: H7 to oxidative stress. Appl Environ Microbiol 75, 6110-6123.
44. Xiao, J., Wang, Q., Liu, Q., Wang, X., Liu, H. & Zhang, Y. (2008). Isolation and identification of fish pathogen Edwardsiella tarda from mariculture in China. Aquac Res 40, 13-17.
45. Xiao, J., Wang, Q., Liu, Q., Xu, L., Wang, X., Wu, H. & Zhang, Y. (2009). Characterization of Edwardsiella tarda rpoS: effect on serum resistance, chondroitinase activity, biofilm formation, and autoindu- cer synthetases expression. Appl Microbiol Biotechnol 83, 151-160.
46. Yu, J. L. & Guo, L. (2011). Quantitative proteomic analysis of Salmonella enterica serovar Typhimurium under PhoP/PhoQ activa- tion conditions. J Proteome Res 10, 2992-3002.
47. Zhao, G., Weatherspoon, N., Kong, W., Curtiss, R., III & Shi, Y. (2008). A dual-signal regulatory circuit activates transcription of a set of divergent operons in Salmonella typhimurium. Proc Natl Acad Sci U S A105,20924-20929.
48. 2+- responsive PhoP regulator in Yersinia pestis. FEMS Microbiol Lett 250, 85-95.