The stringent response regulator DksA is required for Salmonella enterica serovar typhimurium growth in minimal medium, motility, biofilm formation, and intestinal colonization

Infection and Immunity

Volumn 84, Issue 1, 2015, Pages 375-384

  Azriel, Shalhevet ^a   Goren, Alina ^a,b   Rahav, Galia ^a,b   Gal Mor, Ohad ^a,b  

^a SHEBA MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

DKSA PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CULTURE MEDIUM; DKSA PROTEIN, SALMONELLA TYPHIMURIUM; SPI1 PROTEIN, SALMONELLA; TRANSCRIPTION FACTOR; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; CELL ADHESION; CELL INVASION; COLITIS; CONTROLLED STUDY; ECTOPIC EXPRESSION; EPITHELIUM CELL; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PATHOGENICITY ISLAND; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SINGLE NUCLEOTIDE POLYMORPHISM; VIBRIO CHOLERAE; ANIMAL; ANIMAL SALMONELLOSIS; BACTERIUM ADHERENCE; C57BL MOUSE; CACO-2 CELL LINE; CELL LINE; CHEMISTRY; CHEMOTAXIS; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CACO-2 CELLS; CELL LINE; CHEMOTAXIS; COLITIS; CULTURE MEDIA; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; INTESTINES; MACROPHAGES; MICE; MICE, INBRED C57BL; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; TRANSCRIPTION FACTORS; VIRULENCE FACTORS;

EID: 84957684186     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01135-15     Document Type: Article

References (43)

1. Rabsch W, Tschape H, Baumler AJ. 2001. Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3:237-247. http://dx.doi.org/10.1016/S1286-4579(01)01375-2.
2. Edwards RA, Olsen GJ, Maloy SR. 2002. Comparative genomics of closely related salmonellae. Trends Microbiol 10:94-99. http://dx.doi.org/10.1016/S0966-842X(01)02293-4.
3. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM, International Collaboration on Enteric Disease 'Burden of Illness' Studies. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882-889. http://dx.doi.org/10.1086/650733.
4. Chen PL, Chang CM, Wu CJ, Ko NY, Lee NY, Lee HC, Shih HI, Lee CC, Wang RR, Ko WC. 2007. Extraintestinal focal infections in adults with nontyphoid Salmonella bacteraemia: predisposing factors and clinical outcome. J Intern Med 261:91-100. http://dx.doi.org/10.1111/j.1365-2796.2006.01748.x.
5. Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, van der Giessen J, Kruse H. 2010. Food-borne diseases-the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol 139(Suppl 1):S3-S15. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.01.021.
6. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM. 2011. Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8:887-900. http://dx.doi.org/10.1089/fpd.2010.0787.
7. Humphries AD, Townsend SM, Kingsley RA, Nicholson TL, Tsolis RM, Baumler AJ. 2001. Role of fimbriae as antigens and intestinal colonization factors of Salmonella serovars. FEMS Microbiol Lett 201:121-125. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10744.x.
8. Stevens MP, Humphrey TJ, Maskell DJ. 2009. Molecular insights into farm animal and zoonotic Salmonella infections. Philos Trans R Soc Lond B Biol Sci 364:2709-2723. http://dx.doi.org/10.1098/rstb.2009.0094.
9. Abrahams GL, Hensel M. 2006. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol 8:728-737. http://dx.doi.org/10.1111/j.1462-5822.2006.00706.x.
10. Magnusson LU, Farewell A, Nystrom T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:236-242. http://dx.doi.org/10.1016/j.tim.2005.03.008.
11. Paul BJ, Barker MM, Ross W, Schneider DA, Webb C, Foster JW, Gourse RL. 2004. DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell 118:311-322. http://dx.doi.org/10.1016/j.cell.2004.07.009.
12. Potrykus K, Cashel M. 2008. (p)ppGpp: still magical? Annu Rev Microbiol 62:35-51. http://dx.doi.org/10.1146/annurev.micro.62.081307.162903.
13. Zenkin N, Yuzenkova Y. 2015. New insights into the functions of transcription factors that bind the RNA polymerase secondary channel. Biomolecules 5:1195-1209. http://dx.doi.org/10.3390/biom5031195.
14. Aberg A, Fernandez-Vazquez J, Cabrer-Panes JD, Sanchez A, Balsalobre C. 2009. Similar and divergent effects of ppGpp and DksA deficiencies on transcription in Escherichia coli. J Bacteriol 191:3226-3236. http://dx.doi.org/10.1128/JB.01410-08.
15. Pal RR, Bag S, Dasgupta S, Das B, Bhadra RK. 2012. Functional characterization of the stringent response regulatory gene dksA of Vibrio cholerae and its role in modulation of virulence phenotypes. J Bacteriol 194:5638-5648. http://dx.doi.org/10.1128/JB.00518-12.
16. Jude F, Kohler T, Branny P, Perron K, Mayer MP, Comte R, van Delden C. 2003. Posttranscriptional control of quorum-sensing-dependent virulence genes by DksA in Pseudomonas aeruginosa. J Bacteriol 185:3558-3566 http://dx.doi.org/10.1128/JB.185.12.3558-3566.2003.
17. Mogull SA, Runyen-Janecky LJ, Hong M, Payne SM. 2001. dksA is required for intercellular spread of Shigella flexneri via an RpoSindependent mechanism. Infect Immun 69:5742-5751. http://dx.doi.org/10.1128/IAI.69.9.5742-5751.2001.
18. Sharma AK, Payne SM. 2006. Induction of expression of hfq by DksA is essential for Shigella flexneri virulence. Mol Microbiol 62:469-479. http://dx.doi.org/10.1111/j.1365-2958.2006.05376.x.
19. Nakanishi N, Abe H, Ogura Y, Hayashi T, Tashiro K, Kuhara S, Sugimoto N, Tobe T. 2006. ppGpp with DksA controls gene expression in the locus of enterocyte effacement (LEE) pathogenicity island of enterohaemorrhagic Escherichia coli through activation of two virulence regulatory genes. Mol Microbiol 61:194-205. http://dx.doi.org/10.1111/j.1365-2958.2006.05217.x.
20. Yun J, Jeon B, Barton YW, Plummer P, Zhang Q, Ryu S. 2008. Role of the DksA-like protein in the pathogenesis and diverse metabolic activity of Campylobacter jejuni. J Bacteriol 190:4512-4520. http://dx.doi.org/10.1128/JB.00105-08.
21. Ancona V, Lee JH, Chatnaparat T, Oh J, Hong JI, Zhao Y. 2015. The bacterial alarmone (p) ppGpp activates the type III secretion system in Erwinia amylovora. J Bacteriol 197:1433-1443. http://dx.doi.org/10.1128/JB.02551-14.
22. Holley CL, Zhang X, Fortney KR, Ellinger S, Johnson P, Baker B, Liu Y, Janowicz DM, Katz BP, Munson RS, Jr, Spinola SM. 2015. DksA and (p)ppGpp have unique and overlapping contributions to Haemophilus ducreyi pathogenesis in humans. Infect Immun 83:3281-3292. http://dx.doi.org/10.1128/IAI.00692-15.
23. Henard CA, Bourret TJ, Song M, Vazquez-Torres A. 2010. Control of redox balance by the stringent response regulatory protein promotes antioxidant defenses of Salmonella. J Biol Chem 285:36785-36793. http://dx.doi.org/10.1074/jbc.M110.160960.
24. Henard CA, Vazquez-Torres A. 2012. DksA-dependent resistance of Salmonella enterica serovar Typhimurium against the antimicrobial activity of inducible nitric oxide synthase. Infect Immun 80:1373-1380. http://dx.doi.org/10.1128/IAI.06316-11.
25. Webb C, Moreno M, Wilmes-Riesenberg M, Curtiss R, III, Foster JW. 1999 Effects of DksA and ClpP protease on sigma S production and virulence in Salmonella typhimurium. Mol Microbiol 34:112-123. http://dx.doi.org/10.1046/j.1365-2958.1999.01581.x.
26. Datsenko KA, Wanner BL. 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. http://dx.doi.org/10.1073/pnas.120163297.
27. Elhadad D, Desai P, Rahav G, McClelland M, Gal-Mor O. 2015. Flagellin is required for host cell invasion and normal Salmonella pathogenicity island 1 expression by Salmonella enterica serovar Paratyphi A. Infect Immun 83:3355-3368. http://dx.doi.org/10.1128/IAI.00468-15.
28. Duan Q, Zhou M, Zhu L, Zhu G. 2013. Flagella and bacterial pathogenicity. J Basic Microbiol 53:1-8. http://dx.doi.org/10.1002/jobm.201100335.
29. Crawford RW, Reeve KE, Gunn JS. 2010. Flagellated but not hyperfimbriated Salmonella enterica serovar Typhimurium attaches to and forms biofilms on cholesterol-coated surfaces. J Bacteriol 192:2981-2990. http://dx.doi.org/10.1128/JB.01620-09.
30. Galan JE, Ginocchio C, Costeas P. 1992. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol 174:4338-4349.
31. Rice CJ, Ramachandran VK, Shearer N, Thompson A. 2015. Transcriptional and post-transcriptional modulation of SPI1 and SPI2 expression by ppGpp, RpoS and DksA in Salmonella enterica sv Typhimurium. PLoS One 10:e0127523. http://dx.doi.org/10.1371/journal.pone.0127523.
32. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71:2839-2858. http://dx.doi.org/10.1128/IAI.71.5.2839-2858.2003.
33. +/+ mice. Infect Immun 74:5047-5057. http://dx.doi.org/10.1128/IAI.00072-06.
34. Paul BJ, Berkmen MB, Gourse RL. 2005. DksA potentiates direct activation of amino acid promoters by ppGpp. Proc Natl Acad Sci U S A 102:7823-7828. http://dx.doi.org/10.1073/pnas.0501170102.
35. Lemke JJ, Durfee T, Gourse RL. 2009. DksA and ppGpp directly regulate transcription of the Escherichia coli flagellar cascade. Mol Microbiol 74: 1368-1379. http://dx.doi.org/10.1111/j.1365-2958.2009.06939.x.
36. Magnusson LU, Gummesson B, Joksimovic P, Farewell A, Nystrom T. 2007 Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J Bacteriol 189:5193-5202. http://dx.doi.org/10.1128/JB.00330-07.
37. Osterberg S, Skarfstad E, Shingler V. 2010. The sigma-factor FliA, ppGpp and DksA coordinate transcriptional control of the aer2 gene of Pseudomonas putida. Environ Microbiol 12:1439-1451. http://dx.doi.org/10.1111/j.1462-2920.2009.02139.x.
38. Dalebroux ZD, Yagi BF, Sahr T, Buchrieser C, Swanson MS. 2010. Distinct roles of ppGpp and DksA in Legionella pneumophila differentiation. Mol Microbiol 76:200-219. http://dx.doi.org/10.1111/j.1365-2958.2010.07094.x.
39. Turner AK, Lovell MA, Hulme SD, Zhang-Barber L, Barrow PA. 1998. Identification of Salmonella typhimurium genes required for colonization of the chicken alimentary tract and for virulence in newly hatched chicks. Infect Immun 66:2099-2106.
40. Baumler AJ. 1997. The record of horizontal gene transfer in Salmonella. Trends Microbiol 5:318-322. http://dx.doi.org/10.1016/S0966-842X(97)01082-2.
41. Gal-Mor O, Elhadad D, Deng W, Rahav G, Finlay BB. 2011. The Salmonella enterica PhoP directly activates the horizontally acquired SPI-2 gene sseL and is functionally different from a S. bongori ortholog. PLoS One 6:e20024. http://dx.doi.org/10.1371/journal.pone.0020024.
42. Kato A, Groisman EA, Howard Hughes Medical Institute. 2008. The PhoQ/PhoP regulatory network of Salmonella enterica. Adv Exp Med Biol 631:7-21. http://dx.doi.org/10.1007/978-0-387-78885-2_2.
43. Bjarnason J, Southward CM, Surette MG. 2003. Genomic profiling of iron-responsive genes in Salmonella enterica serovar Typhimurium by high-throughput screening of a random promoter library. J Bacteriol 185: 4973-4982. http://dx.doi.org/10.1128/JB.185.16.4973-4982.2003.