The Journal of Microbiology

, Volume 46, Issue 3, pp 331–337 | Cite as

The changes of proteomes components of Helicobacter pylori in response to acid stress without urea

  • Chunhong Shao
  • Qunye Zhang
  • Wei Tang
  • Wei Qu
  • Yabin Zhou
  • Yundong Sun
  • Han Yu
  • Jihui Jia
Article

Abstract

Acid stress is the most obvious challenge Helicobacter pylori encounters in human stomach. The urease system is the basic process used to maintain periplasmic and cytoplasmic pH near neutrality when H. pylori is exposed to acidic condition. However, since the urea concentration in gastric juice is approximately 1 mM, considered possibly insufficient to ensure the survival of H. pylori, it is postulated that additional mechanisms of pH homeostasis may contribute to the acid adaptation in H. pylori. In order to identify the acid-related proteins other than the urease system we have compared the proteome profiles of H. pylori strain 26695 exposed to different levels of external pH (7.4, 6.0, 5.0, 4.0, 3.0, and 2.0) for 30 min in the absence of urea using 2-DE. Differentially expressed proteins were identified by MALDI-TOF-TOF-MS analysis, which turned out to be 36 different proteins. The functions of these proteins included ammonia production, molecular chaperones, energy metabolism, cell envelope, response regulator and some proteins with unknown function. SOM analysis indicated that H. pylori responds to acid stress through multi-mechanisms involving many proteins, which depend on the levels of acidity the cells encounter.

Keywords

Helicobacter pylori acid stress comparative proteomics 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allan, E., C.L. Clayton, A. McLaren, D.M. Wallace, and B.W. Wren. 2001. Characterization of the low-pH responses of Helicobacter pylori using genomic DNA arrays. Microbiology 147, 2285–2292.PubMedGoogle Scholar
  2. Ang, S., C.Z. Lee, K. Peck, M. Sindici, U. Matrubutham, M.A. Gleeson, and J.T. Wang. 2001. Acid-induced gene expression in Helicobacter pylori: study in genomic scale by microarray. Infect. Immun. 69, 1679–1686.PubMedCrossRefGoogle Scholar
  3. Bijlsma, J.J., M. Lie-A-Ling, I.C. Nootenboom, C.M. Vandenbroucke-Grauls, and J.G. Kusters. 2000. Identification of loci essential for the growth of Helicobacter pylori under acidic conditions. J. Infect. Dis. 182, 1566–1569.PubMedCrossRefGoogle Scholar
  4. Brotz-Oesterhelt, H., J.E. Bandow, and H. Labischinski. 2005. Bacterial proteomics and its role in antibacterial drug discovery. Mass Spectrom. Rev. 24, 549–565.PubMedCrossRefGoogle Scholar
  5. Bury-Mone, S., S. Skouloubris, C. Dauga, J.M. Thiberge, D. Dailidiene, D.E. Berg, A. Labigne, and H. De Reuse. 2003. Presence of active aliphatic amidases in Helicobacter species able to colonize the stomach. Infect. Immun. 71, 5613–5622.PubMedCrossRefGoogle Scholar
  6. Bury-Moné, S., J.M. Thiberge, M. Contreras, A. Maitournam, A. Labigne, and H. De Reuse. 2004. Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 53, 623–638.PubMedCrossRefGoogle Scholar
  7. Comtois, S.L., M.D. Gidley, and D.J. Kelly. 2003. Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology 149, 121–129.PubMedCrossRefGoogle Scholar
  8. Hazard, A.L. and A.E. Senior. 1994. Mutagenesis of subunit delta from Escherichia coli F1F0-ATP synthase. J. Biol. Chem. 269, 418–426.PubMedGoogle Scholar
  9. Hegde, P.S., I.R. White, and C. Debouck. 2003. Interplay of transcriptomics and proteomics. Curr. Opin. Biotechnol. 14, 647–651.PubMedCrossRefGoogle Scholar
  10. Hong, W., K. Sano, S. Morimatsu, D.R. Scott, D.L. Weeks, G. Sachs, T. Goto, S. Mohan, F. Harada, N. Nakajima, and T. Nakano. 2003. Medium pH-dependent redistribution of the urease of Helicobacter pylori. J. Med. Microbiol. 52, 211–216.PubMedCrossRefGoogle Scholar
  11. Huesca, M., A. Goodwin, A. Bhagwansingh, P. Hoffman, and C.A. Lingwood. 1998. Characterization of an acidic-pH-inducible stress protein (hsp70), a putative sulfatide binding adhesin, from Helicobacter pylori. Infect. Immun. 66, 4061–4067.PubMedGoogle Scholar
  12. Iii, J.R. and A.L. Osterman. 2007. Introduction: advances in genomics and proteomics. Chem. Rev. 107, 3363–3366.CrossRefGoogle Scholar
  13. Kurian, D., K. Phadwal, and P. Maenpaa. 2006. Proteomic characterization of acid stress response in Synechocystis sp. PCC 6803. Proteomics 6, 3614–3624.PubMedCrossRefGoogle Scholar
  14. McGee, D.J., C.A. May, R.M. Garner, J.M. Himpsl, and H.L. Mobley. 1999. Isolation of Helicobacter pylori genes that modulate urease activity. J. Bacteriol. 181, 2477–2484.PubMedGoogle Scholar
  15. Merrell, D.S., M.L. Goodrich, G. Otto, L.S. Tompkins, and S. Falkow. 2003. pH-Regulated gene expression of the gastric pathogen Helicobacter pylori. Infect. Immun. 71, 3529–3539.PubMedCrossRefGoogle Scholar
  16. Mizoguchi, H., T. Fujioka, K. Kishi, A. Nishizono, R. Kodama, and M. Nasu. 1998. Diversity in protein synthesis and viability of Helicobacter pylori coccoid forms in response to various stimuli. Infect. Immun. 66, 5555–5560.PubMedGoogle Scholar
  17. Pflock, M., P. Dietz, J. Schar, and D. Beier. 2004. Genetic evidence for histidine kinase HP165 being an acid sensor of Helicobacter pylori. FEMS Microbiol. Lett. 234, 51–61.PubMedCrossRefGoogle Scholar
  18. Scott, D.R., E.A. Marcus, D.L. Weeks, A. Lee, K. Melchers, and G. Sachs. 2000. Expression of the Helicobacter pylori ureI gene is required for acidic pH activation of cytoplasmic urease. Infect. Immun. 68, 470–477.PubMedCrossRefGoogle Scholar
  19. Scott, D.R., E.A. Marcus, Y. Wen, J. Oh, and G. Sachs. 2007. Gene expression in vivo shows that Helicobacter pylori colonizes an acidic niche on the gastric surface. Proc. Natl. Acad. Sci. USA 104, 7235–7240.PubMedCrossRefGoogle Scholar
  20. Slonczewski, J.L., D.J. McGee, J. Phillips, C. Kirkpatrick, and H.L. Mobley. 2000. pH-Dependent protein profiles of Helicobacter pylori analyzed by two-dimensional gels. Helicobacter 5, 240–247.PubMedCrossRefGoogle Scholar
  21. Suerbaum, S., J.M. Thiberge, I. Kansau, R.L. Ferrero, and A. Labigne. 1994. Helicobacter pylori hspA-hspB heat-shock gene cluster: nucleotide sequence, expression, putative function and immunogenicity. Mol. Microbiol. 14, 959–974.PubMedCrossRefGoogle Scholar
  22. Toledo, H., M. Valenzuela, A. Rivas, and C.A. Jerez. 2002. Acid stress response in Helicobacter pylori. FEMS Microbiol. Lett. 213, 67–72.PubMedCrossRefGoogle Scholar
  23. Wen, Y., J. Feng, D.R. Scott, E.A. Marcus, and G. Sachs. 2006. Involvement of the HP0165-HP0166 two-component system in expression of some acidic-pH-upregulated genes of Helicobacter pylori. J. Bacteriol. 188, 1750–1761.PubMedCrossRefGoogle Scholar
  24. Wen, Y., E.A. Marcus, U. Matrubutham, M.A. Gleeson, D.R. Scott, and G. Sachs. 2003. Acid-adaptive genes of Helicobacter pylori. Infect. Immun. 71, 5921–5939.PubMedCrossRefGoogle Scholar
  25. Windle, H.J., A. Fox, D. Ni Eidhin, and D. Kelleher. 2000. The thioredoxin system of Helicobacter pylori. J. Biol. Chem. 275, 5081–5089.PubMedCrossRefGoogle Scholar
  26. Yan, S.P., Q.Y. Zhang, Z.C. Tang, W.A. Su, and W.N. Sun. 2006. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol. Cell. Proteomics 5, 484–496.PubMedGoogle Scholar
  27. Yohannes, E., D.M. Barnhart, and J.L. Slonczewski. 2004. pH-Dependent catabolic protein expression during anaerobic growth of Escherichia coli K-12. J. Bacteriol. 186, 192–199.PubMedCrossRefGoogle Scholar
  28. Young, K.A., Y. Akyon, D.S. Rampton, S.G. Barton, R.P. Allaker, J.M. Hardie, and R.A. Feldman. 2000. Quantitative culture of Helicobacter pylori from gastric juice: the potential for transmission. J. Med. Microbiol. 49, 343–347.PubMedGoogle Scholar
  29. Zheng, P.Z., K.K. Wang, Q.Y. Zhang, Q.H. Huang, Y.Z. Du, Q.H. Zhang, D.K. Xiao, S.H. Shen, S. Imbeaud, E. Eveno, C.J. Zhao, Y.L. Chen, H.Y. Fan, S. Waxman, C. Auffray, G. Jin, S.J. Chen, Z. Chen, and J. Zhang. 2005. Systems analysis of transcriptome and proteome in retinoic acid/arsenic trioxide-induced cell differentiation/apoptosis of promyelocytic leukemia. Proc. Natl. Acad. Sci. USA 24, 7653–7658.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelber GmbH 2008

Authors and Affiliations

  • Chunhong Shao
    • 1
  • Qunye Zhang
    • 2
  • Wei Tang
    • 1
  • Wei Qu
    • 1
  • Yabin Zhou
    • 1
  • Yundong Sun
    • 1
  • Han Yu
    • 1
  • Jihui Jia
    • 1
    • 2
  1. 1.Department of MicrobiologyShandong UniversityJinanP. R. China
  2. 2.Key Lab for Experimental Teratology of Chinese Ministry of Education, School of MedicineShandong UniversityJinanP. R. China

Personalised recommendations