A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar typhimurium

Journal of Bacteriology

Volumn 191, Issue 12, 2009, Pages 3928-3937

  Simm, Roger ^a,b   Remminghorst, Uwe ^a   Ahmad, Irfan ^a   Zakikhany, Katherina ^a   Römling, Ute ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYCLIC DI GUANOSINE PHOSPHATE; CYCLIC GMP DERIVATIVE; NUCLEOTIDE; PHOSPHODIESTERASE; PROTEIN CSGD; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR STM1344; UNCLASSIFIED DRUG; CYCLIC GMP; TRANSACTIVATOR PROTEIN;

ARTICLE; BACTERIAL STRAIN; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSDUCTION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN METABOLISM; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STRAIN DIFFERENCE; TURNOVER TIME; AMINO ACID SEQUENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PHOSPHORIC DIESTER HYDROLASES; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 67549109657     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00290-09     Document Type: Article

References (47)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1994. Current protocols in molecular biology. John Wiley & Sons, New York, NY.
2. Brombacher, E., A. Baratto, C. Dorel, and P. Landini. 2006. Gene expression regulation by the curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J. Bacteriol. 188:2027-2037. (Pubitemid 43376456)
3. Christen, M., B. Christen, M. Folcher, A. Schauerte, and U. Jenal. 2005. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:30829-30837.
4. Cotter, P. A., and S. Stibitz. 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10:17-23.
5. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
6. Duerig, A., S. Abel, M. Folcher, M. Nicollier, T. Schwede, N. Amiot, B. Giese, and U. Jenal. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23:93-104.
7. Galperin, M. Y. 2005. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5:35.
8. Gerstel, U., C. Park, and U. Römling. 2003. Complex regulation of csgD promoter activity by global regulatory proteins. Mol. Microbiol. 49:639-654.
9. Gerstel, U., and U. Römling. 2003. The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res. Microbiol. 154:659-667.
10. Gibson, D. L., A. P. White, S. D. Snyder, S. Martin, C. Heiss, P. Azadi, M. Surette, and W. W. Kay. 2006. Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J. Bacteriol. 188:7722-7730.
11. Guzman, L. M., D. Belin, M. J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
12. Harshey, R. M. 1994. Bees aren't the only ones: swarming in gram-negative bacteria. Mol. Microbiol. 13:389-394.
13. Hisert, K. B., M. MacCoss, M. U. Shiloh, K. H. Darwin, S. Singh, R. A. Jones, S. Ehrt, Z. Zhang, B. L. Gaffney, S. Gandotra, D. W. Holden, D. Murray, and C. Nathan. 2005. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol. Microbiol. 56:1234-1245.
14. Jaroszewski, L., L. Rychlewski, Z. Li, W. Li, and A. Godzik. 2005. FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33(Web server issue):W284-W288. (Pubitemid 44529927)
15. Jonas, K., A. N. Edwards, R. Simm, T. Romeo, U. Römling, and Ö. Melefors. 2008. The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol. Microbiol. 70:236-257.
16. Kader, A., R. Simm, U. Gerstel, M. Morr, and U. Römling. 2006. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60:602-616.
17. Ko, M., and C. Park. 2000. Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J. Mol. Biol. 303:371-382. (Pubitemid 30826090)
18. Kulesekara, H., V. Lee, A. Brencic, N. Liberati, J. Urbach, S. Miyata, D. G. Lee, A. N. Neely, M. Hyodo, Y. Hayakawa, F. M. Ausubel, and S. Lory. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. USA 103:2839-2844.
19. Latasa, C., A. Roux, A. Toledo-Arana, J. M. Ghigo, C. Gamazo, J. R. Penades, and I. Lasa. 2005. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol. Microbiol. 58:1322-1339.
20. -ΔΔCT method. Methods 25:402-408.
21. Merighi, M., V. T. Lee, M. Hyodo, Y. Hayakawa, and S. Lory. 2007. The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 65:876-895. (Pubitemid 47221070)
22. Newell, P. D., R. D. Monds, and G. A. O'Toole. 2009. LapD is a bis-(3′-5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl. Acad. Sci. USA 106:3461-3466.
23. Paul, R., S. Weiser, N. C. Amiot, C. Chan, T. Schirmer, B. Giese, and U. Jenal. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-727. (Pubitemid 38489938)
24. Pei, J., and N. V. Grishin. 2001. GGDEF domain is homologous to adenylyl cyclase. Proteins 42:210-216. (Pubitemid 32047329)
25. Rao, F., Y. Yang, Y. Qi, and Z. X. Liang. 2008. Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J. Bacteriol. 190:3622-3631.
26. Römling, U. 2005. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci. 62:1234-1246.
27. Römling, U., and D. Amikam. 2006. Cyclic di-GMP as a second messenger. Curr. Opin. Microbiol. 9:218-228.
28. Römling, U., Z. Bian, M. Hammar, W. D. Sierralta, and S. Normark. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180:722-731.
29. Römling, U., W. Bokranz, W. Rabsch, X. Zogaj, M. Nimtz, and H. Tschäpe. 2003. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int. J. Med. Microbiol. 293:273-285.
30. Römling, U., M. Rohde, A. Olsen, S. Normark, and J. Reinköster. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36:10-23.
31. Römling, U., W. D. Sierralta, K. Eriksson, and S. Normark. 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249-264. (Pubitemid 28182249)
32. Ryan, R. P., Y. Fouhy, J. F. Lucey, L. C. Crossman, S. Spiro, Y. W. He, L. H. Zhang, S. Heeb, M. Camara, P. Williams, and J. M. Dow. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. USA 103:6712-6717.
33. Ryan, R. P., Y. Fouhy, J. F. Lucey, and J. M. Dow. 2006. Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J. Bacteriol. 188:8327-8334. (Pubitemid 44894031)
34. Ryjenkov, D. A., R. Simm, U. Römling, and M. Gomelsky. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP. The PilZ domain protein YcgR controls motility in Enterobacteria. J. Biol. Chem. 281:30310-30314. (Pubitemid 44582083)
35. Ryjenkov, D. A., M. Tarutina, O. V. Moskvin, and M. Gomelsky. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187:1792-1798. (Pubitemid 40289381)
36. Schmidt, A. J., D. A. Ryjenkov, and M. Gomelsky. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187:4774-4781. (Pubitemid 40962195)
37. Simm, R., A. Lusch, A. Kader, M. Andersson, and U. Römling. 2007. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:3613-3623.
38. Simm, R., M. Morr, A. Kader, M. Nimtz, and U. Römling. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53:1123-1134.
39. Simm, R., M. Morr, U. Remminghorst, M. Andersson, and U. Römling. 2009. Quantitative determination of cyclic diguanosine monophosphate con-centrations in nucleotide extracts of bacteria by matrix-assisted laser desorption/ ionization-time-of-flight mass spectrometry. Anal. Biochem. 386:53-58.
40. Suzuki, K., P. Babitzke, S. R. Kushner, and T. Romeo. 2006. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev. 20:2605-2617. (Pubitemid 44396844)
41. Tamayo, R., J. T. Pratt, and A. Camilli. 2007. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu. Rev. Microbiol. 61:131-148.
42. Tischler, A. D., and A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
43. Tschowri, N., S. Busse, and R. Hengge. 2009. The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. Genes Dev. 23:522-534.
44. Wei, B. L., A. M. Brun-Zinkernagel, J. W. Simecka, B. M. Pruss, P. Babitzke, and T. Romeo. 2001. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol. Microbiol. 40:245-256. (Pubitemid 32322877)
45. Wozniak, C. E., C. Lee, and K. T. Hughes. 2008. T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J. Bacteriol. 191:1498-1508.
46. Zeghouf, M., J. Li, G. Butland, A. Borkowska, V. Canadien, D. Richards, B. Beattie, A. Emili, and J. F. Greenblatt. 2004. Sequential peptide affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J. Proteome Res. 3:463-468. (Pubitemid 39207350)
47. Zogaj, X., M. Nimtz, M. Rohde, W. Bokranz, and U. Römling. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:1452-1463.