The EAL domain containing protein STM2215 (rtn) is needed during Salmonella infection and has cyclic di-GMP phosphodiesterase activity

Molecular Microbiology

Volumn 89, Issue 3, 2013, Pages 403-419

  Zheng, Yi ^a   Sambou, Tounkang ^a   Bogomolnaya, Lydia M ^a   Cirillo, Jeffrey D ^a   Mcclelland, Michael ^b   Andrews Polymenis, Helene ^a  

^a TEXAS A AND M UNIVERSITY SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYCLIC GMP PHOSPHODIESTERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIUM MUTANT; BIOCHEMISTRY; COLON MUCOSA; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE; LIVER; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; SALMONELLA; SALMONELLOSIS; SPLEEN; STM2215 GENE; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CACO-2 CELLS; FEMALE; GENE DELETION; HUMANS; MACROPHAGES; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PHOSPHORIC DIESTER HYDROLASES; PROTEIN STRUCTURE, TERTIARY; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

ENTEROBACTERIACEAE; MURINAE; MUS; SALMONELLA;

EID: 84880779001     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12284     Document Type: Article

References (44)

1. Ahmad, I., Lamprokostopoulou, A., Guyon, S.L., Streck, E., Barthel, M., Peters, V., etal. (2011) Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS ONE 6: e28351.
2. Arthur, T.M., Bosilevac, J.M., Brichta-Harhay, D.M., Kalchayanand, N., King, D.A., Shackelford, S.D., etal. (2008a) Source tracking of Escherichia coli O157:H7 and Salmonella contamination in the lairage environment at commercial U.S. beef processing plants and identification of an effective intervention. J Food Prot 71: 1752-1760.
3. Arthur, T.M., Brichta-Harhay, D.M., Bosilevac, J.M., Guerini, M.N., Kalchayanand, N., Wells, J.E., etal. (2008b) Prevalence and characterization of Salmonella in bovine lymph nodes potentially destined for use in ground beef. J Food Prot 71: 1685-1688.
4. Arthur, T.M., Kalchayanand, N., Bosilevac, J.M., Brichta-Harhay, D.M., Shackelford, S.D., Bono, J.L., etal. (2008c) Comparison of effects of antimicrobial interventions on multidrug-resistant Salmonella, susceptible Salmonella, and Escherichia coli O157:H7. J Food Prot 71: 2177-2181.
5. Bogomolnaya, L.M., Santiviago, C.A., Yang, H.J., Baumler, A.J., and Andrews-Polymenis, H.L. (2008) Form variation' of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine. Mol Microbiol 70: 1105-1119.
6. Brichta-Harhay, D.M., Guerini, M.N., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., etal. (2008) Salmonella and Escherichia coli O157:H7 contamination on hides and carcasses of cull cattle presented for slaughter in the United States: an evaluation of prevalence and bacterial loads by immunomagnetic separation and direct plating methods. Appl Environ Microbiol 74: 6289-6297.
7. Burdette, D.L., Monroe, K.M., Sotelo-Troha, K., Iwig, J.S., Eckert, B., Hyodo, M., etal. (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature 478: 515-518.
8. Callaway, T.R., Keen, J.E., Edrington, T.S., Baumgard, L.H., Spicer, L., Fonda, E.S., etal. (2005) Fecal prevalence and diversity of Salmonella species in lactating dairy cattle in four states. J Dairy Sci 88: 3603-3608.
9. Chang, A.L., Tuckerman, J.R., Gonzalez, G., Mayer, R., Weinhouse, H., Volman, G., etal. (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40: 3420-3426.
10. Christen, M., Christen, B., Folcher, M., Schauerte, A., and Jenal, U. (2005) Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280: 30829-30837.
11. Cotter, P.A., and Stibitz, S. (2007) c-di-GMP-mediated regulation of virulence and biofilm formation. Curr Opin Microbiol 10: 17-23.
12. Elledge, S.J., and Davis, R.W. (1989) Position and density effects on repression by stationary and mobile DNA-binding proteins. Genes Dev 3: 185-197.
13. Fedorka-Cray, P.J., Dargatz, D.A., Thomas, L.A., and Gray, J.T. (1998) Survey of Salmonella serotypes in feedlot cattle. J Food Prot 61: 525-530.
14. Fields, P.I., Swanson, R.V., Haidaris, C.G., and Heffron, F. (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83: 5189-5193.
15. Fontana, M.F., and Vance, R.E. (2011) Two signal models in innate immunity. Immunol Rev 243: 26-39.
16. Galperin, M.Y. (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6: 552-567.
17. Galperin, M.Y., Nikolskaya, A.N., and Koonin, E.V. (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203: 11-21.
18. Garcia, B., Latasa, C., Solano, C., Garcia-del Portillo, F., Gamazo, C., and Lasa, I. (2004) Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54: 264-277.
19. Hansen-Wester, I., and Hensel, M. (2001) Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect 3: 549-559.
20. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
21. Hisert, K.B., MacCoss, M., Shiloh, M.U., Darwin, K.H., Singh, S., Jones, R.A., etal. (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.
22. Kader, A., Simm, R., Gerstel, U., Morr, M., and Romling, U. (2006) Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 60: 602-616.
23. Karaolis, D.K., Means, T.K., Yang, D., Takahashi, M., Yoshimura, T., Muraille, E., etal. (2007) Bacterial c-di-GMP is an immunostimulatory molecule. J Immunol 178: 2171-2181.
24. Lamprokostopoulou, A., Monteiro, C., Rhen, M., and Romling, U. (2010) Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar Typhimurium at the mucosal lining. Environ Microbiol 12: 40-53.
25. Lawhon, S.D., Frye, J.G., Suyemoto, M., Porwollik, S., McClelland, M., and Altier, C. (2003) Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48: 1633-1645.
26. McWhirter, S.M., Barbalat, R., Monroe, K.M., Fontana, M.F., Hyodo, M., Joncker, N.T., etal. (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206: 1899-1911.
27. Miller, J.H. (1972) Experiments in Molecular Genetics. New York: Cold Spring Harbor Laboratory Press.
28. Oliver, D.B., and Beckwith, J. (1982) Regulation of a membrane component required for protein secretion in Escherichia coli. Cell 30: 311-319.
29. Rao, F., Yang, Y., Qi, Y., and Liang, Z. (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190: 3622-3631.
30. Romling, U. (2009) Rationalizing the evolution of EAL domain-based cyclic di-GMP-specific phosphodiesterases. J Bacteriol 191: 4697-4700.
31. Romling, U. (2012) Cyclic di-GMP, an established secondary messenger still speeding up. Environ Microbiol 14: 1817-1829.
32. Romling, U., and Amikam, D. (2006) Cyclic di-GMP as a second messenger. Curr Opin Microbiol 9: 218-228.
33. Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., etal. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281.
34. Ryan, R.P., Fouhy, Y., Lucey, J.F., Crossman, L.C., Spiro, S., He, Y.W., etal. (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.
35. Santiviago, C., Reynolds, M.M., Porwollik, S., Choi, S.H., Long, F., Andrews-Polymenis, H., and McClelland, M. (2009a) Array-based analysis of pools of Salmonella targeted deletion mutants identifies novel genes under selection during infection. PLoS Pathog 5: e1000477.
36. Santiviago, C.A., Reynolds, M.M., Porwollik, S., Choi, S.H., Long, F., Andrews-Polymenis, H.L., and McClelland, M. (2009b) Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog 5: e1000477.
37. Schmidt, A.J., Ryjenkov, D.A., and Gomelsky, M. (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187: 4774-4781.
38. Simm, R., Lusch, A., Kader, A., Andersson, M., and Romling, U. (2007) Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J Bacteriol 189: 3613-3623.
39. Simm, R., Remminghorst, U., Ahmad, I., Zakikhany, K., and Romling, U. (2009) A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar Typhimurium. J Bacteriol 191: 3928-3937.
40. Sommerfeldt, N., Possling, A., Becker, G., Pesavento, C., Tschowri, N., and Hengge, R. (2009) Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155: 1318-1331.
41. Stewart, M.K., Cummings, L.A., Johnson, M.L., Berezow, A.B., and Cookson, B.T. (2011) Regulation of phenotypic heterogeneity permits Salmonella evasion of the host caspase-1 inflammatory response. Proc Natl Acad Sci USA 108: 20742-20747.
42. Tal, R., Wong, H.C., Calhoon, R., Gelfand, D., Fear, A.L., Volman, G., etal. (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180: 4416-4425.
43. Tamayo, R., Tischler, A.D., and Camilli, A. (2005) The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280: 33324-33330.
44. Wolfe, A.J., and Visick, K.L. (2008) Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190: 463-475.