The protein acyltransferase Pat post-transcriptionally controls HilD to repress Salmonella invasion

Molecular Microbiology

Volumn 102, Issue 1, 2016, Pages 121-136

  Hung, Chien Che ^a   Eade, Colleen R ^a   Altier, Craig ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ACYLTRANSFERASE PAT; BACTERIAL PROTEIN; BETA GALACTOSIDASE; COBB PROTEIN; HILD PROTEIN; HISTONE DEACETYLASE; SPI1 PROTEIN; UNCLASSIFIED DRUG;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE MUTATION; HILD GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; RNA TRANSLATION; SALMONELLA; SALMONELLOSIS; SPI1 GENE; TRANSCRIPTION REGULATION;

EID: 84988499127     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13451     Document Type: Article

References (49)

1. AbouElfetouh, A., Kuhn, M.L., Hu, L.I., Scholle, M.D., Sorensen, D.J., Sahu, A.K., et al. (2015) The E. coli sirtuin CobB shows no preference for enzymatic and nonenzymatic lysine acetylation substrate sites. Microbiol Open 4: 66–83.
2. Baxter, M.A., Fahlen, T.F., Wilson, R.L, and Jones, B.D. (2003) HilE interacts with HilD and negatively regulates hilA transcription and expression of the salmonella enterica serovar typhimurium invasive phenotype. Infect Immunity 71: 1295–1305.
3. Boddicker, J.D., Knosp, B.M, and Jones, B.D. (2003) Transcription of the salmonella invasion gene activator, hilA, requires HilD activation in the absence of negative regulators. J Bacteriol 185: 525–533.
4. Chubiz, J.E., Golubeva, Y.A., Lin, D., Miller, L.D, and Slauch, J.M. (2010) FliZ regulates expression of the salmonella pathogenicity island 1 invasion locus by controlling HilD protein activity in Salmonella enterica serovar typhimurium. J Bacteriol 192: 6261–6270.
5. Darwin, K.H and Miller, V.L. (1999) InvF is required for expression of genes encoding proteins secreted by the SPI1 type III secretion apparatus in Salmonella typhimurium. J Bacteriol 181: 4949–4954.
6. Datsenko, K.A and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–6645.
7. Dokmanovic, M., Clarke, C, and Marks, P.A. (2007) Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res: MCR 5: 981–989.
8. Eichelberg, K and Galan, J.E. (1999) Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and hilA. Infect Immunity 67: 4099–4105.
9. Ellermeier, C.D., Ellermeier, J.R, and Slauch, J.M. (2005) HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol 57: 691–705.
10. Ellermeier, C.D and Slauch, J.M. (2003) RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in salmonella enterica serovar Typhimurium. J Bacteriol 185: 5096–5108.
11. Ellermeier, J.R and Slauch, J.M. (2007) Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol 10: 24–29.
12. Frye, R.A. (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 273: 793–798.
13. Fu, Y and Galan, J.E. (1998) Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of salmonella typhimurium. J Bacteriol 180: 3393–3399.
14. Galan, J.E and Curtiss, R. 3rd, (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86: 6383–6387.
15. Garner, C.D., Antonopoulos, D.A., Wagner, B., Duhamel, G.E., Keresztes, I., Ross, D.A., Young, V.B, and Altier, C. (2009) Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a salmonella enterica serovar typhimurium murine model of infection. Infect Immun 77: 2691–2702.
16. Garrity, J., Gardner, J.G., Hawse, W., Wolberger, C, and Escalante-Semerena, J.C. (2007) N-lysine propionylation controls the activity of propionyl-CoA synthetase. J Biol Chem 282: 30239–30245.
17. Glozak, M.A., Sengupta, N., Zhang, X, and Seto, E. (2005) Acetylation and deacetylation of non-histone proteins. Gene 363: 15–23.
18. Golubeva, Y.A., Sadik, A.Y., Ellermeier, J.R, and Slauch, J.M. (2012) Integrating global regulatory input into the salmonella pathogenicity island 1 type III secretion system. Genetics 190: 79–90.
19. Groisman, E.A and Ochman, H. (1993) Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and shigella flexneri. Embo J 12: 3779–3787.
20. Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R, and Galan, J.E. (1998) S. Typhimurium encodes an activator of rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815–826.
21. Hentchel, K.L and Escalante-Semerena, J.C. (2015) In salmonella enterica, the Gcn5-related acetyltransferase MddA (formerly YncA) acetylates methionine sulfoximine and methionine sulfone, blocking their toxic effects. J Bacteriol 197: 314–325.
22. Hung, C.C., Garner, C.D., Slauch, J.M., Dwyer, Z.W., Lawhon, S.D., Frye, J.G., et al. (2013) The intestinal fatty acid propionate inhibits salmonella invasion through the Post-translational control of HilD. Mol Microbiol. 87: 1045–1060.
23. Hung, C.C., Haines, L, and Altier, C. (2012) The flagellar regulator fliT represses salmonella pathogenicity island 1 through flhDC and fliZ. PLoS One 7: e34220.
24. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galan, J.E, and Aizawa, S.I. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602–605.
25. Lawhon, S.D., Maurer, R., Suyemoto, M, and Altier, C. (2002) Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol 46: 1451–1464.
26. Lee, C.A., Jones, B.D, and Falkow, S. (1992) Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants. Proc Natl Acad Sci U S A 89: 1847–1851.
27. Liang, W and Deutscher, M.P. (2012) Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme pka (YfiQ). RNA 18: 37–41.
28. Lima, B.P., Antelmann, H., Gronau, K., Chi, B.K., Becher, D., Brinsmade, S.R, and Wolfe, A.J. (2011) Involvement of protein acetylation in glucose-induced transcription of a stress-responsive promoter. Mol Microbiol 81: 1190–1204.
29. Lima, B.P., Thanh Huyen, T.T., Basell, K., Becher, D., Antelmann, H, and Wolfe, A.J. (2012) Inhibition of acetyl phosphate-dependent transcription by an acetylatable lysine on RNA polymerase. J Biol Chem 287: 32147–32160.
30. Martinez, L.C., Yakhnin, H., Camacho, M.I., Georgellis, D., Babitzke, P., Puente, J.L, and Bustamante, V.H. (2011) Integration of a complex regulatory cascade involving the SirA/BarA and csr global regulatory systems that controls expression of the salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol Microbiol 80: 1637–1656.
31. Miller, J.H. (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, NY.
32. Miller, J.H. (1992) A short course in bacterial genetics: A laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Mills, D.M., Bajaj, V, and Lee, C.A. (1995) A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 15: 749–759.
34. Palacios, S., Starai, V.J, and Escalante-Semerena, J.C. (2003) Propionyl coenzyme a is a common intermediate in the 1,2-propanediol and propionate catabolic pathways needed for expression of the prpBCDE operon during growth of salmonella enterica on 1,2-propanediol. J Bacteriol 185: 2802–2810.
35. Rasband, W.S. (1997–2012) ImageJ. In. Bethesda, Maryland, USA: U. S. National Institutes of Health.
36. Ren, J., Sang, Y., Tan, Y., Tao, J., Ni, J., Liu, S., et al. (2016) Acetylation of lysine 201 inhibits the DNA-binding ability of PhoP to regulate salmonella Virulence. PLoS Pathogens 12: e1005458.
37. Sang, Y., Ren, J., Ni, J., Tao, J., Lu, J, and Yao, Y.F. (2016) Protein acetylation is involved in salmonella enterica serovar typhimurium Virulence. The Journal of Infectious Diseases
38. Schechter, L.M., Damrauer, S.M, and Lee, C.A. (1999) Two AraC/XylS family members can independently counteract the effect of repressing sequences upstream of the hilA promoter. Mol Microbiol 32: 629–642.
39. Starai, V.J., Celic, I., Cole, R.N., Boeke, J.D, and Escalante-Semerena, J.C. (2002) Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298: 2390–2392.
40. Starai, V.J and Escalante-Semerena, J.C. (2004) Identification of the protein acetyltransferase (pat) enzyme that acetylates acetyl-CoA synthetase in salmonella enterica. J Mol Biol 340: 1005–1012.
41. Sternberg, N.L and Maurer, R. (1991) Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol 204: 18–43.
42. Takaya, A., Tomoyasu, T., Tokumitsu, A., Morioka, M, and Yamamoto, T. (2002) The ATP-dependent lon protease of salmonella enterica serovar typhimurium regulates invasion and expression of genes carried on salmonella pathogenicity island 1. J Bacteriol 184: 224–232.
43. Thao, S., Chen, C.S., Zhu, H, and Escalante-Semerena, J.C. (2010) Nepsilon-lysine acetylation of a bacterial transcription factor inhibits its DNA-binding activity. PLoS One 5: e15123.
44. Uzzau, S., Figueroa-Bossi, N., Rubino, S, and Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98: 15264–15269.
45. Verdone, L., Agricola, E., Caserta, M, and Di Mauro, E. (2006) Histone acetylation in gene regulation. Brief Functional Genomics Proteomics 5: 209–221.
46. Villalba, J.M and Alcain, F.J. (2012) Sirtuin activators and inhibitors. BioFactors 38: 349–359.
47. Winson, M.K., Swift, S., Fish, L., Throup, J.P., Jorgensen, F., Chhabra, S.R., et al. (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163: 185–192.
48. Zhou, D., Mooseker, M.S, and Galan, J.E. (1999a) An invasion-associated salmonella protein modulates the actin-bundling activity of plastin. Proc Natl Acad Sci U S A 96: 10176–10181.
49. Zhou, D., Mooseker, M.S, and Galan, J.E. (1999b) Role of the S. Typhimurium actin-binding protein SipA in bacterial internalization. Science 283: 2092–2095.