Helicobacter pylori exploits human CEACAMs via HopQ for adherence and translocation of CagA

Nature Microbiology

Volumn 2, Issue , 2016, Pages

  Königer, Verena ^a   Holsten, Lea ^a   Harrison, Ute ^a   Busch, Benjamin ^a   Loell, Eva ^a   Zhao, Qing ^a   Bonsor, Daniel A ^b   Roth, Alexandra ^c   Kengmo Tchoupa, Arnaud ^c   Smith, Stella I ^d   Mueller, Susanna ^a   Sundberg, Eric J ^b   Zimmermann, Wolfgang ^a,b   Fischer, Wolfgang ^a   Hauck, Christof R ^c   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d NIGERIAN INSTITUTE OF MEDICAL RESEARCH   (Nigeria)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ADHESIN, HELICOBACTER; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CAGA PROTEIN, HELICOBACTER PYLORI; CELL ADHESION MOLECULE; PROTEIN BINDING;

BACTERIUM ADHERENCE; CELL LINE; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ADHESINS, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL ADHESION MOLECULES; CELL LINE; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84992362187     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.188     Document Type: Article

References (40)

1. Suerbaum, S. & Michetti, P. Helicobacter pylori infection. N. Engl. J. Med. 347, 1175-1186 (2002).
2. Peek, R. M. & Blaser, M. J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2, 28-37 (2002).
3. Kwok, T. et al. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449, 862-866 (2007).
4. Jimenez-Soto, L. F. et al. Helicobacter pylori type IV secretion apparatus exploits beta1 integrin in a novel RGD-independent manner. PLoS Pathog. 5, e1000684 (2009).
5. Odenbreit, S. et al. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287, 1497-1500 (2000).
6. Fischer, W. et al. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42, 1337-1348 (2001).
7. Gorrell, R. J. et al. A novel NOD1- and CagA-independent pathway of interleukin-8 induction mediated by the Helicobacter pylori type IV secretion system. Cell. Microbiol. 15, 554-570 (2013).
8. Selbach, M. et al. Host cell interactome of tyrosine-phosphorylated bacterial proteins. Cell Host. Microbe 5, 397-403 (2009).
9. Higashi, H. et al. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295, 683-686 (2002).
10. Tsutsumi, R., Higashi, H., Higuchi, M., Okada, M. & Hatakeyama, M. Attenuation of Helicobacter pylori CagA-SHP-2 signaling by interaction between CagA and C-terminal Src kinase. J. Biol. Chem. 278, 3664-3670 (2002).
11. Amieva, M. R. et al. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300, 1430-1434 (2003).
12. Saadat, I. et al. Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 447, 330-333 (2007).
13. Ohnishi, N. et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc. Natl Acad. Sci. USA 105, 1003-1008 (2008).
14. Rieder, G., Merchant, J. L. & Haas, R. Helicobacter pylori cag-type IV secretion system facilitates corpus colonization to induce precancerous conditions in Mongolian gerbils. Gastroenterology 128, 1229-1242 (2005).
15. Franco, A. T. et al. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res. 68, 379-387 (2008).
16. Hatakeyama, M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 4, 688-694 (2004).
17. Ishijima, N. et al. BabA-mediated adherence is a potentiator of the Helicobacter pylori Type IV secretion system activity. J. Biol. Chem. 286, 25256-25264 (2011).
18. Belogolova, E. et al. Helicobacter pylori outer membrane protein HopQ identified as a novel T4SS-associated virulence factor. Cell. Microbiol. 15, 1896-1912 (2013).
19. Jimenez-Soto, L. F., Clausen, S., Sprenger, A., Ertl, C. & Haas, R. Dynamics of the Cag-type IV secretion system of Helicobacter pylori as studied by bacterial co-infections. Cell Microbiol. 15, 1924-1937 (2013).
20. Kuespert, K., Pils, S. & Hauck, C. R. CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 18, 565-571 (2006).
21. Gray-Owen, S. D. & Blumberg, R. S. CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 6, 433-446 (2006).
22. Buntru, A., Roth, A., Nyffenegger-Jann, N. J. & Hauck, C. R. HemITAM signaling by CEACAM3, a human granulocyte receptor recognizing bacterial pathogens. Arch. Biochem. Biophys. 524, 77-83 (2012).
23. Hauck, C. R., Agerer, F., Muenzner, P. & Schmitter, T. Cellular adhesion molecules as targets for bacterial infection. Eur. J. Cell Biol. 85, 235-242 (2006).
24. Kuespert, K., Weibel, S. & Hauck, C. R. Profiling of bacterial adhesin-host receptor recognition by soluble immunoglobulin superfamily domains. J. Microbiol. Methods 68, 478-485 (2007).
25. Heuermann, D. & Haas, R. A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol. Gen. Genet. 257, 519-528 (1998).
26. Cao, P. & Cover, T. L. Two different families of hopQ alleles in Helicobacter pylori. J. Clin. Microbiol. 40, 4504-4511 (2002).
27. Korotkova, N. et al. Binding of Dr adhesins of Escherichia coli to carcinoembryonic antigen triggers receptor dissociation. Mol. Microbiol. 67, 420-434 (2008).
28. Garhart, C. A., Redline, R. W., Nedrud, J. G. & Czinn, S. J. Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect. Immun. 70, 3529-3538 (2002).
29. Kammerer, R. & Zimmermann, W. Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol. 8, 12 (2010).
30. Muenzner, P., Bachmann, V., Zimmermann, W., Hentschel, J. & Hauck, C. R. Human-restricted bacterial pathogens block shedding of epithelial cells by stimulating integrin activation. Science 329, 1197-1201 (2010).
31. Barrozo, R. M. et al. Functional plasticity in the type IV secretion system of Helicobacter pylori. PLoS Pathog. 9, e1003189 (2013).
32. Linz, B. et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445, 915-918 (2007).
33. Schmitter, T., Agerer, F., Peterson, L., Munzner, P. & Hauck, C. R. Granulocyte CEACAM3 is a phagocytic receptor of the innate immune system that mediates recognition and elimination of human-specific pathogens. J. Exp. Med. 199, 35-46 (2004).
34. Dailidiene, D., Dailide, G., Kersulyte, D., & Berg, D. E. Contraselectable streptomycin susceptibility determinant for genetic manipulation and analysis of Helicobacter pylori. Appl. Environ. Microbiol. 72, 5908-5914 (2006).
35. Pham, K. T. et al. Cagi is an essential component of the Helicobacter pylori Cag type IV secretion system and forms a complex with CagL. PLoS ONE 7, e35341 (2012).
36. Voges, M., Bachmann, V., Kammerer, R., Gophna, U. & Hauck, C. R. CEACAM1 recognition by bacterial pathogens is species-specific. BMC Microbiol. 10, 117 (2010).
37. Pelegrin, A. et al. Human carcinoembryonic antigen cDNA expressed in rat carcinoma cells can function as target antigen for tumor localization of antibodies in nude rats and as rejection antigen in syngeneic rats. Int. J. Cancer 52, 110-119 (1992).
38. Fischer, W. & Haas, R. The RecA protein of Helicobacter pylori requires a posttranslational modification for full activity. J. Bacteriol. 186 777-784 (2004).
39. Hohlfeld, S. et al. 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 (2006).
40. Odenbreit, S., Faller, G. & Haas, R. Role of the alpAB proteins and lipopolysaccharide in adhesion of Helicobacter pylori to human gastric tissue. Int. J. Med. Microbiol. 292, 247-256 (2002).