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Virulence Increasing of Salmonella typhimurium in Balb/c Mice After Heat-Stress Induction of Phage Shock Protein A

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Abstract

Salmonella typhimurium is a potentially intracellular pathogen and is responsible for thousands of reported cases of acute gastroenteritis and diarrhea each year. Although many successful physiological and genetic approaches have been taken to conclude the key virulence determinants encoded by this organism, the total number of uncharacterized reading frames observed within the S. typhimurium genome suggests that many virulence factors remain to be discovered. This study was conducted to evaluate the role of heat induced phage shock protein A (PspA), in the pathogenicity of S. typhimurium. The stress proteins detected on sodium dodecyl sulfate-polyacrylamide gel electrophoresis were identified specifically by immunoblotting with polyclonal antibody against PspA. PspA was produced in response to heat stress at 45°C and it was over-expressed at 65°C. At this temperature, the stressed bacterial cells producing PspA were more virulent (16 folds greater) to female 6–8 week-old Balb/c mice. Correspondency between decrease in LD50 and increase in PspA production during heat stress and lower pathogenicity in non-producing cells that emerged during stress at 55°C represents PspA as an important virulence factor in heat stressed S. typhimurium.

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References

  1. Adams H, Teertstra W, Koster M, Tommassen J (2002) PspE (phage-shock protein E) of Escherichia coli is a rhodanese. FEBS Lett 518:173–176

    Article  PubMed  CAS  Google Scholar 

  2. Ausable FM (ed) (1989) Current protocols in molecular biology. Wiley Press, New York

    Google Scholar 

  3. Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen J, Molin S, Prensier G, Arbeille B, Ghigo JM (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674

    Article  PubMed  CAS  Google Scholar 

  4. Brissette JL, Russel M, Weiner L, Model P (1990) Phage shock protein, a stress protein of Escherichia coli. Proc Natl Acad Sci USA 87:862–866

    Article  PubMed  CAS  Google Scholar 

  5. Brissette JL, Weiner L, Ripmaster TL, Model P (1991) Characterization and sequence of the Escherichia coli stress induced psp operon. J Mol Biol 220:35–48

    Article  PubMed  CAS  Google Scholar 

  6. Cassens RG (1994) Meat preservation: preventing losses and assuring safety. Food and Nutrition Press, Inc, Trumbull

    Google Scholar 

  7. Cossart P, Sansonetti PJ (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242–248

    Article  PubMed  CAS  Google Scholar 

  8. Darwin AJ, Miller VL (1999) Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature tagged transposon mutagenesis. Mol Microbiol 32:51–62

    Article  PubMed  CAS  Google Scholar 

  9. Darwin AJ, Miller VL (2001) The psp locus of Yersinia enterocolitica is required for virulence and for growth in vitro when the Ysc type III secretion system is produced. Mol Microbiol 39:429–445

    Article  PubMed  CAS  Google Scholar 

  10. DeLisa MP, Lee P, Palmer T, Georgiou G (2004) Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J Bacteriol 186:366–373

    Article  PubMed  CAS  Google Scholar 

  11. DelVecchio VG, Wagner MA, Eschenbrenner M, Horn TA, Kraycer JA, Estock F, Elzer P, Mujer CV (2002) Brucella proteomes a review. J Vet Microbiol 90:593–603

    Article  CAS  Google Scholar 

  12. Dworkin J, Jovanovic G, Model P (2000) The PspA protein of Escherichia coli is a negative regulator of s54-dependent transcription. J Bacteriol 182:311–319

    Article  PubMed  CAS  Google Scholar 

  13. Elderkin S, Jones S, Schumacher J, Studholme D, Buck M (2002) Mechanism of action of the Escherichia coli phage shock protein PspA in repression of the AAA family transcription factor PspF. J Mol Biol 320:23–37

    Article  PubMed  CAS  Google Scholar 

  14. Elderkin S, Bordes P, Jones S, Rappas M, Buck M (2005) Molecular determinants for PspA mediated repression of the transcriptional activator PspF. J Bacteriol 187:3238–3248

    Article  PubMed  CAS  Google Scholar 

  15. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47:103–118

    Article  PubMed  CAS  Google Scholar 

  16. Gomez TM, Motarjemi Y, Miyagawa S, Kaferstein FK, Stohr K (1997) Foodborne salmonellosis. World Health Stat 50:81–89

    CAS  Google Scholar 

  17. Hecker M, Volker U (2004) Towards a comprehensive understanding of Bacillus subtilis cell physiology by physiological proteomics. Proteomics 4:3727–3750

    Article  PubMed  CAS  Google Scholar 

  18. Jovanovic G, Model P (1999) In vivo and in vitro activities of the Escherichia coli σ54 transcription activator, PspF, and its DNA binding mutant, PspF HTH. J Mol Biol 285:469–483

    Article  PubMed  CAS  Google Scholar 

  19. Jovanovic G, Weiner L, Model P (1996) Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress induced psp operon. J Bacteriol 178:1936–1945

    PubMed  CAS  Google Scholar 

  20. Jovanovic G, Lloyd LJ, Stumpf MP, Mayhew AJ, Buck M (2006) Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli. J Biol Chem 281:21147–21161

    Article  PubMed  CAS  Google Scholar 

  21. Kleerebezem M, Crielaard W, Tommassen J (1996) Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the proton motive force under stress conditions. EMBO J 15:162–171

    PubMed  CAS  Google Scholar 

  22. Kwan LY, Isaccson RE (1998) Identification and characterization of a phase nonfimbrial Salmonella typhimurium gene that alters O-antigen production. Infect Immun 66(12):5725–5730. doi: 0019-9567

    Google Scholar 

  23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  24. Lipton MS, Pasa-Tolic L, Anderson GA, Anderson DJ, Auberry DL, Battista JR, Daly MJ, Fredrickson J, Hixson K, Kostandarithes H, Masselon C, Markillie L, Moore R, Romine MF, Shen Y, Stritmatter E, Tolic N, Udseth H, Venkateswaran A, Wong KK, Zhao R, Smith RD (2002) Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc Natl Acad Sci USA 99:11049–11054

    Article  PubMed  CAS  Google Scholar 

  25. Lloyd LJ, Jones SE, Jovanovic G, Gyaneshwar P, Rolfe MD, Thompson A, Hinton JC, Buck M (2004) Identification of a new member of the phage shock protein response in Escherichia coli, the phage shock protein G (PspG). J Biol Chem 279:55707–55714

    Article  PubMed  CAS  Google Scholar 

  26. Maxson ME, Darwin AJ (2004) Identification of inducers of the Yersinia enterocolitica phage shock protein system and comparison to the regulation of the RpoE and Cpx extracytoplasmic stress responses. J Bacteriol 186:4199–4208

    Article  PubMed  CAS  Google Scholar 

  27. Maxson ME, Darwin AJ (2005) Improved system for construction and analysis of single copy beta-galactosidase operon fusions in Yersinia enterocolitica. Appl Environ Microbiol 71:5614–5618

    Article  PubMed  CAS  Google Scholar 

  28. Maxson ME, Darwin AJ (2006) PspB and PspC of Yersinia enterocolitica are dual function proteins: regulators and effectors of the phage shock protein response. Mol Microbiol 59:1610–1623

    Article  PubMed  CAS  Google Scholar 

  29. National Institutes of Health (1985) Guide for the care and use of laboratory animals. National Institutes of Health publication no 85±23. National Institutes of Health, Bethesda, MD

    Google Scholar 

  30. Pang TZ, Bhutta A, Finlay BB, Altwegg M (1995) Typhoid fever and other salmonellosis: a continuing challenge. Trends Microbiol 3:253–255

    Article  PubMed  CAS  Google Scholar 

  31. Reed LJ, Muench H (1938) A simple method of estimating fifty percent end point. Am J Hyg 27:493–499

    Google Scholar 

  32. Shoae Hassani A, Malekzadeh F, Amirmozafari N, Hamdi K, Ordouzadeh N, Ghaemi A (2009) Phage shock protein G, a novel ethanol induced stress protein in Salmonella typhimurium. Curr Microbiol 58(3):239–244

    Article  PubMed  CAS  Google Scholar 

  33. Suutari M, Laakso S (1994) Microbial fatty acids and thermal adaptation. Crit Rev Microbiol 20:285–328

    Article  PubMed  CAS  Google Scholar 

  34. Vrancken K, Mellaert LV, Anné J (2008) Characterization of the Streptomyces lividans PspA Response. J Bacteriol 190:3475–3481

    Article  PubMed  CAS  Google Scholar 

  35. Wallis TS, Galyov EE (2000) Molecular basis of Salmonella induced enteritis. Mol Microbiol 36:997–1005

    Article  PubMed  CAS  Google Scholar 

  36. Wang Q, Frye JG, McClelland M, Harshey RM (2004) Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol Microbiol 52:169–187

    Article  PubMed  CAS  Google Scholar 

  37. Weiner L, Brissette JL, Model P (1991) Stress induced expression of the Escherichia coli phage shock protein operon is dependent on sigma 54 and modulated by positive and negative feedback mechanisms. Genes Dev 5:1912–1923

    Article  PubMed  CAS  Google Scholar 

  38. Yousef AE, Juneja VK (2002) Microbial stress adaptation and food safety. CRC Press, Boca Raton, pp 178–183

    Google Scholar 

  39. Yuk HG, Marshall DL (2003) Heat adaptation alters Escherichia coli O157:H7 membrane lipid composition and verotoxin production. Appl Environ Microbiol 69:5115–5119

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Young Researchers Club (YRC) in Tehran Sciences and Research Branch of IAU. We thank Ahmadreza Shoa Hassani for the helpful comments and benefit information.

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Correspondence to Amir Ghaemi.

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Hassani, A.S., Amirmozafari, N. & Ghaemi, A. Virulence Increasing of Salmonella typhimurium in Balb/c Mice After Heat-Stress Induction of Phage Shock Protein A. Curr Microbiol 59, 446–450 (2009). https://doi.org/10.1007/s00284-009-9458-z

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  • DOI: https://doi.org/10.1007/s00284-009-9458-z

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