Dynamics of the Cag-type IV secretion system of Helicobacter pylori as studied by bacterial co-infections

Cellular Microbiology

Volumn 15, Issue 11, 2013, Pages 1924-1937

  Jiménez Soto, Luisa F ^a   Clausen, Sabine ^a   Sprenger, Annika ^a   Ertl, Claudia ^a   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; INTEGRIN RECEPTOR; OUTER MEMBRANE PROTEIN; VACUOLATING TOXIN;

ADULT; ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; FLAGELLUM; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; LACTOBACILLUS; MIXED INFECTION; NONHUMAN; PATHOGENIC ESCHERICHIA COLI; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; TYPE IV SECRETION SYSTEM;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; HELICOBACTER PYLORI; NEGIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANTIBIOSIS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL LINE; EPITHELIAL CELLS; HELICOBACTER PYLORI; HUMANS; PROTEIN TRANSPORT;

EID: 84885430810     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12166     Document Type: Article

References (40)

1. Agerer, F., Michel, A., Ohlsen, K., and Hauck, C.R. (2003) Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J Biol Chem 278: 42524-42531.
2. Alm, R.A., Bina, J., Andrews, B.M., Doig, P., Hancock, R.E., and Trust, T.J. (2000) Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun 68: 4155-4168.
3. Alvarez-Martinez, C.E., and Christie, P.J. (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
4. Atherton, J.C., Cao, P., Peek, R.M., Tummuru, M.K.R., Blaser, M.J., and Cover, T.L. (1995) Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem 270: 17771-17777.
5. Bik, E.M., Eckburg, P.B., Gill, S.R., Nelson, K.E., Purdom, E.A., Francois, F., etal. (2006) Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 103: 732-737.
6. Blaser, M.J., and Atherton, J.C. (2004) Helicobacter pylori persistence: biology and disease. J Clin Invest 113: 321-333.
7. Brandt, S., Kenny, B., Rohde, M., Martinez-Quiles, N., and Backert, S. (2009) Dual infection system identifies a crucial role for PKA-mediated serine phosphorylation of the EPEC-Tir-injected effector protein in regulating Rac1 function. Cell Microbiol 11: 1254-1271.
8. Cao, P., and Cover, T.L. (2002) Two different families of hopQ alleles in Helicobacter pylori. J Clin Microbiol 40: 4504-4511.
9. Censini, S., Lange, C., Xiang, Z.Y., Crabtree, J.E., Ghiara, P., Borodovsky, M., etal. (1996) Cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93: 14648-14653.
10. Cover, T.L., Tummuru, M.K.R., Cao, P., Thompson, S., and Blaser, M.J. (1994) Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J Biol Chem 269: 10566-10573.
11. Crabill, E., Joe, A., Block, A., van Rooyen, J.M., and Alfano, J.R. (2010) Plant immunity directly or indirectly restricts the injection of type III effectors by the Pseudomonas syringae type III secretion system. Plant Physiol 154: 233-244.
12. Eto, D.S., Jones, T.A., Sundsbak, J.L., and Mulvey, M.A. (2007) Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 3: e100.
13. Fischer, W. (2011) Assembly and molecular mode of action of the Helicobacter pylori Cag type IV secretion apparatus. FEBS J 278: 1203-1212.
14. Fischer, W., Windhager, L., Rohrer, S., Zeiller, M., Karnholz, A., Hoffmann, R., etal. (2010) Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer. Nucleic Acids Res 38: 6089-6101.
15. Gebert, B., Fischer, W., Weiss, E., Hoffmann, R., and Haas, R. (2003) Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301: 1099-1102.
16. Guerrant, R.L., Wanke, C.A., Pennie, R.A., Barrett, L.J., Lima, A.A., and O'Brien, A.D. (1987) Production of a unique cytotoxin by Campylobacter jejuni. Infect Immun 55: 2526-2530.
17. Handt, L.K., Fox, J.G., Stalis, I.H., Rufo, R., Lee, G., Linn, J., etal. (1995) Characterization of feline Helicobacter pylori strains and associated gastritis in a colony of domestic cats. J Clin Microbiol 33: 2280-2289.
18. Higashi, H., Tsutsumi, R., Muto, S., Sugiyama, T., Azuma, T., Asaka, M., etal. (2001) SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295: 683-686.
19. Higashi, H., Nakaya, A., Tsutsumi, R., Yokoyama, K., Fujii, Y., Ishikawa, S., etal. (2004) Helicobacter pylori CagA induces Ras-independent morphogenetic response through SHP-2 recruitment and activation. J Biol Chem 279: 17205-17216.
20. Hohlfeld, S., Pattis, I., Puls, J., Plano, G.V., Haas, R., and Fischer, W. (2006) A C-terminal translocation signal is necessary, but not sufficient for type IV secretion of the Helicobacter pylori CagA protein. Mol Microbiol 59: 1624-1637.
21. Ilver, D., Arnqvist, A., Ogren, J., Frick, I.M., Kersulyte, D., Incecik, E.T., etal. (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279: 373-377.
22. Ishijima, N., Suzuki, M., Ashida, H., Ichikawa, Y., Kanegae, Y., Saito, I., etal. (2011) BabA-mediated adherence is a potentiator of the Helicobacter pylori Type IV secretion system activity. J Biol Chem 286: 25256-25264.
23. Jimenez-Soto, L.F., Kutter, S., Sewald, X., Ertl, C., Weiss, E., Kapp, U., etal. (2009) Helicobacter pylori type IV secretion apparatus exploits beta1 integrin in a novel RGD-independent manner. PLoS Pathog 5: e1000684.
24. Jimenez-Soto, L.F., Rohrer, S., Jain, U., Ertl, C., Sewald, X., and Haas, R. (2012) Effects of cholesterol on Helicobacter pylori growth and virulence properties in vitro. Helicobacter 17: 133-139.
25. Kaplan-Türköz, B., Jimenez-Soto, L.F., Dian, C., Ertl, C., Remaut, H., Louche, A., etal. (2012) Structural insights into Helicobacter pylori oncoprotein CagA interaction with beta1 integrin. Proc Natl Acad Sci USA 109: 14640-14645.
26. Kusters, J.G., van Vliet, A.H., and Kuipers, E.J. (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19: 449-490.
27. Kwok, T., Zabler, D., Urman, S., Rohde, M., Hartig, R., Wessler, S., etal. (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449: 862-866.
28. Loh, J.T., Torres, V.J., Algood, H.M., McClain, M.S., and Cover, T.L. (2008) Helicobacter pylori HopQ outer membrane protein attenuates bacterial adherence to gastric epithelial cells. FEMS Microbiol Lett 289: 53-58.
29. Mahdavi, J., Sonden, B., Hurtig, M., Olfat, F.O., Forsberg, L., Roche, N., etal. (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297: 573-578.
30. Maldonado-Contreras, A., Goldfarb, K.C., Godoy-Vitorino, F., Karaoz, U., Contreras, M., Blaser, M.J., etal. (2011) Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J 5: 574-579.
31. Mould, A.P., Askari, J.A., Barton, S., Kline, A.D., McEwan, P.A., Craig, S.E., etal. (2002) Integrin activation involves a conformational change in the alpha 1 helix of the beta subunit A-domain. J Biol Chem 277: 19800-19805.
32. Mueller, D., Tegtmeyer, N., Brandt, S., Yamaoka, Y., De, P.E., Sgouras, D., etal. (2012) c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J Clin Invest 122: 1553-1566.
33. Odenbreit, S., Till, M., Hofreuter, D., Faller, G., and Haas, R. (1999) Genetic and functional characterisation of the alpAB gene locus essential for adhesion of Helicobacter pylori to human gastric tissue. Mol Microbiol 31: 1537-1548.
34. Odenbreit, S., Püls, J., Sedlmaier, B., Gerland, E., Fischer, W., and Haas, R. (2000) Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287: 1497-1500.
35. Odenbreit, S., Kavermann, H., Puls, J., and Haas, R. (2002) CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from alpAB, HopZ and bab group outer membrane proteins. Int J Med Microbiol 292: 257-266.
36. Saadat, I., Higashi, H., Obuse, C., Umeda, M., Murata-Kamiya, N., Saito, Y., etal. (2007) Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 447: 330-333.
37. Schmitt, W., and Haas, R. (1994) Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol Microbiol 12: 307-319.
38. Secka, O., Antonio, M., Berg, D.E., Tapgun, M., Bottomley, C., Thomas, V., etal. (2011) Mixed infection with cagA-positive and cagA-negative strains of Helicobacter pylori lowers disease burden in The Gambia. PLoS ONE 6: e27954.
39. Taylor, N.S., Fox, J.G., Akopyants, N.S., Berg, D.E., Thompson, N., Shames, B., etal. (1995) Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J Clin Microbiol 33: 918-923.
40. Tomb, J.-F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., etal. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.