Salmonella Modulation of Host Cell Gene Expression Promotes Its Intracellular Growth

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Hannemann, Sebastian ^a   Gao, Beile ^a   Galán, Jorge E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

P21 ACTIVATED KINASE; STAT3 PROTEIN;

APOPTOSIS; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL DIVISION; CONTROLLED STUDY; EPITHELIUM CELL; GENE SILENCING; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOMODULATION; INTERNALIZATION; MICROARRAY ANALYSIS; NONHUMAN; NUCLEAR REPROGRAMMING; POLYACRYLAMIDE GEL ELECTROPHORESIS; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM; WESTERN BLOTTING;

BACTERIAL SECRETION SYSTEMS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HELA CELLS; HEP G2 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; SALMONELLA TYPHIMURIUM; STAT3 TRANSCRIPTION FACTOR;

EID: 84887270879     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003668     Document Type: Article

References (51)

1. Galán J, (2009) Common themes in the design and function of bacterial effectors. Cell Host Microbe 5: 571-579.
2. Mallick P, Schirle M, Chen SS, Flory MR, Lee H, et al. (2007) Computational prediction of proteotypic peptides for quantitative proteomics. Nat Biotechnol 25: 125-131.
3. Lange V, Picotti P, Domon B, Aebersold R, (2008) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4: 222-230.
4. Gallien S, Duriez E, Domon B, (2011) Selected reaction monitoring applied to proteomics. J Mass Spect 46: 298-312.
5. Galan JE, Wolf-Watz H, (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567-573.
6. Galán JE, (2001) Salmonella interaction with host cells: Type III Secretion at Work. Annu Rev Cell Dev Biol 17: 53-86.
7. Waterman SR, Holden DW, (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5: 501-511.
8. Xu G, Paige J, Jaffrey S, (2011) Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat Biotechnol 28: 868-873.
9. Patel JC, Galan JE, (2005) Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr Opin Microbiol 8: 10-15.
10. Patel JC, Galan JE, (2006) Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol 175: 453-463.
11. Hobbie S, Chen LM, Davis R, Galán JE, (1997) Involvement of the mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal cells. J Immunol 159: 5550-5559.
12. Bruno V, Hannemann S, Lara-Tejero M, Flavell RA, Kleinstein SH, et al. (2009) Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog 5: e1000538 doi:1000510.1001371/journal.ppat.1000538.
13. Jenner R, Young R, (2005) Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 3: 281-294.
14. Lee J, Mo J, Shen C, Rucker A, Raz E, (2007) Toll-like receptor signaling in intestinal epithelial cells contributes to colonic homoeostasis. Curr Opin Gastroenterol 23: 27-31.
15. Shibolet O, Podolsky D, (2007) TLRs in the Gut. IV. Negative regulation of Toll-like receptors and intestinal homeostasis: addition by subtraction. Am J Physiol Gastrointest Liver Physiol 292: G1469-1473.
16. Lang T, Mansell A, (2007) The negative regulation of Toll-like receptor and associated pathways. Immunol Cell Biol 85: 425-434.
17. Thiennimitr P, Winter S, Winter M, Xavier M, Tolstikov V, et al. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108: 17480-17485.
18. Stecher B, Robbiani R, Walker A, Westendorf A, Barthel M, et al. (2007) Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5: 2177-2189.
19. Morpeth S, Ramadhani H, Crump J, (2009) Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 49: 606-611.
20. Parry C, Threlfall E, (2008) Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis 21: 531-538.
21. Galán JE, Nakayama K, Curtiss Rd, (1990) Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene 94: 29-35.
22. Yu H, Pardoll D, Jove R, (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9: 798-809.
23. Graham S, (2010) Nontyphoidal salmonellosis in Africa. Curr Opin Infect Dis 23: 409-414.
24. Siddiquee K, Zhang S, Guida W, Blaskovich M, Greedy B, et al. (2007) Selective chemical probe inhibitor of Stat3, identified through structure-based virtual screening, induces antitumor activity. Proc Natl Acad Sci U S A 104: 7391-7396.
25. Yu Y, Zeng H, Vijay-Kumar M, Neish A, Merlin D, Sitaraman SV, et al. (2004) STAT signaling underlies difference between flagellin-induced and tumor necrosis factor-alpha-induced epithelial gene expression. J Biol Chem 279: 35210-35218.
26. Galán JE, Ginocchio C, Costeas P, (1992) Molecular and functional characterization of the Salmonella typhimurium invasion gene invA: Homology of InvA to members of a new protein family. J Bacteriol 17: 4338-4349.
27. Hardt W-D, Chen L-M, Schuebel KE, Bustelo XR, Galán JE, (1998) Salmonella typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826.
28. Zhou D, Chen LM, Hernandez L, Shears SB, Galán JE, (2001) A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 39: 248-259.
29. Isberg RR, Falkow S, (1985) A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli. Nature 317: 262-264.
30. Srikanth C, Mercado-Lubo R, Hallstrom K, McCormick B, (2011) Salmonella effector proteins and host-cell responses. Cell Mol Life Sci 68: 3687-3697.
31. Lin T, Bost K, (2004) STAT3 activation in macrophages following infection with Salmonella. Biochem Biophys Res Commun 321: 828-834.
32. Xue L, Wang WH, Iliuk A, Hu L, Galan JA, et al. (2012) Sensitive kinase assay linked with phosphoproteomics for identifying direct kinase substrates. Proc Natl Acad Sci U S A 109: 5615-5620.
33. Van Etten R, (1999) Cycling, stressed-out and nervous: cellular functions of c-Abl. Trends Cell Biol 9: 179-186.
34. Ly K, Casanova J, (2009) Abelson tyrosine kinase facilitates Salmonella enterica serovar Typhimurium entry into epithelial cells. Infect Immun 77: 60-69.
35. Coppo P, Dusanter-Fourt I, Millot G, Nogueira M, Dugray A, et al. (2003) Constitutive and specific activation of STAT3 by BCR-ABL in embryonic stem cells. Oncogene 22: 4102-4110.
36. Ilaria RJ, Van Etten R, (1996) P210 and P190(BCR/ABL) induce the tyrosine phosphorylation and DNA binding activity of multiple specific STAT family members. J Biol Chem 271: 31704-31710.
37. Buchdunge E, Zimmermann J, Mett H, Meyer T, Müller M, et al. (1996) Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res 56: 100-104.
38. Martin-Carrasco M, Gonzalez-Pinto A, Galan JL, Ballesteros J, Maurino J, et al. (2012) Number of prior episodes and the presence of depressive symptoms are associated with longer length of stay for patients with acute manic episodes. Ann Gen Psychiatry 11: 7.
39. Roig J, Tuazon P, Zipfel P, Pendergast A, Traugh J, (2000) Functional interaction between c-Abl and the p21-activated protein kinase gamma-PAK. Proc Natl Acad Sci U S A 97: 14346-14351.
40. Chen LM, Bagrodia S, Cerione RAa, Galán JE, (1999) Requirement of p21-activated kinase (PAk) for Salmonella typhimurium-induced nuclear responses. J Exp Med 189: 1479-1488.
41. D'Auria G, Galan JC, Rodriguez-Alcayna M, Moya A, Baquero F, et al. (2011) Complete genome sequence of Acidaminococcus intestini RYC-MR95, a Gram-negative bacterium from the phylum Firmicutes. J Bacteriol 193: 7008-7009.
42. Yebra G, de Mulder M, Perez-Elias MJ, Perez-Molina JA, Galan JC, et al. (2011) Increase of transmitted drug resistance among HIV-infected sub-Saharan Africans residing in Spain in contrast to the native population. PLoS One 6: e26757.
43. Chen LM, Hobbie S, Galan JE, (1996) Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274: 2115-2118.
44. Sandler H, Stoecklin G, (2008) Control of mRNA decay by phosphorylation of tristetraprolin. Biochem Soc Trans 36: 491-496.
45. Sansone P, Bromberg J, (2012) Targeting the interleukin-6/Jak/stat pathway in human malignancies. J Clin Oncol 30: 1005-1014.
46. Nelson E, Sharma S, Settleman J, Frank D, (2011) A chemical biology approach to developing STAT inhibitors: molecular strategies for accelerating clinical translation. Oncotarget 2: 518-524.
47. Kichina J, Goc A, Al-Husein B, Somanath P, Kandel E, (2010) PAK1 as a therapeutic target. Expert Opin Ther Targets 14: 703-725.
48. Eichelberg K, Galan JE, (1999) Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and hilA. Infect Immun 67: 4099-4105.
49. Galán JE, Curtiss III R, (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sc USA 86: 6383-6387.
50. Teng T, Lin B, Manser E, Ng D, Cao X, (2009) Stat3 promotes directional cell migration by regulating Rac1 activity via its activator betaPIX. J Cell Sci 122: 4150-4159.
51. Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.