The granulocyte orphan receptor CEACAM4 is able to trigger phagocytosis of bacteria

Journal of Leukocyte Biology

Volumn 97, Issue 3, 2015, Pages 521-530

  Tascón, Julia Delgado ^a   Adrian, Jonas ^a   Kopp, Kathrin ^a   Scholz, Philipp ^a   Tschan, Mario P ^a   Kuespert, Katharina ^a,c   Hauck, Christof R ^a,b  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF BERN   (Switzerland)

^c HAIN LIFESCIENCE GMBH   (Germany)

Author keywords

ITAM; Src kinase; Tyrosine phosphorylation

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 3; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 4; NCK PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SH2; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG; CEACAM4 PROTEIN, HUMAN; PHOSPHOTYROSINE; PROTEIN BINDING;

ARTICLE; BACTERIUM; CONTROLLED STUDY; CYTOPLASM; ENZYME INHIBITION; GENE DELETION; GENE SEQUENCE; GRANULOCYTE; HUMAN; HUMAN CELL; INTERNALIZATION; MOLECULE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; AMINO ACID SEQUENCE; BACTERIA; BONE MARROW CELL; CHEMISTRY; GENETICS; HEK293 CELL LINE; HL 60 CELL LINE; METABOLISM; MOLECULAR GENETICS; PHAGOCYTE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

NEGIBACTERIA;

AMINO ACID SEQUENCE; BACTERIA; CARCINOEMBRYONIC ANTIGEN; CYTOPLASM; GRANULOCYTES; HEK293 CELLS; HL-60 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MYELOID CELLS; PHAGOCYTES; PHAGOCYTOSIS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES;

EID: 84928760524     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.2AB0813-449RR     Document Type: Article

References (48)

1. Pinheiro, V. B., Ellar, D. J. (2006) How to kill a mocking bug? Cell. Microbiol. 8, 545–557.
2. Takeda, K., Kaisho, T., Akira, S. (2003) Toll-like receptors. Annu. Rev. Immunol. 21, 335–376.
3. Areschoug, T., Gordon, S. (2008) Pattern recognition receptors and their role in innate immunity: focus on microbial protein ligands. Contrib. Microbiol. 15, 45–60.
4. Areschoug, T., Gordon, S. (2009) Scavenger receptors: role in innate immunity and microbial pathogenesis. jiol. 11, 1160–1169.
5. Kuespert, K., Pils, S., Hauck, C. R. (2006) CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 18, 565–571.
6. Kammerer, R., Popp, T., Härtle, S., Singer, B. B., Zimmermann, W. (2007) Species-specific evolution of immune receptor tyrosine based activation motif-containing CEACAM1-related immune receptors in the dog. BMC Evol. Biol. 7, 196.
7. Kammerer, R., Zimmermann, W. (2010) Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol. 8, 12.
8. Hammarström, S. (1999) The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9, 67–81.
9. Chen, T., Gotschlich, E. C. (1996) CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc. Natl. Acad. Sci. USA 93, 14851–14856.
10. Hauck, C. R., Meyer, T. F., Lang, F., Gulbins, E. (1998) CD66-mediated phagocytosis of Opa52 Neisseria gonorrhoeae requires a Src-like tyrosine kinase- and Rac1-dependent signalling pathway. EMBO J. 17, 443–454.
11. Schmitter, T., Agerer, F., Peterson, L., Munzner, P., Hauck, C. R. (2004) 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.
12. Buntru, A., Roth, A., Nyffenegger-Jann, N. J., Hauck, C. R. (2012) HemITAM signaling by CEACAM3, a human granulocyte receptor recognizing bacterial pathogens. Arch. Biochem. Biophys. 524, 77–83.
13. McCaw, S. E., Schneider, J., Liao, E. H., Zimmermann, W., Gray-Owen, S. D. (2003) Immunoreceptor tyrosine-based activation motif phosphorylation during engulfment of Neisseria gonorrhoeae by the neutrophil-restricted CEACAM3 (CD66d) receptor. Mol. Microbiol. 49, 623–637.
14. Schmitter, T., Pils, S., Weibel, S., Agerer, F., Buntru, A., Kopp, K., Hauck, C. R. (2007) Opa proteins of pathogenic Neisseriae initiate Src kinasedependent or lipid raft-mediated uptake via distinct human carcinoembryonic antigen-related cell adhesion molecule isoforms. Infect. Immun. 75, 4116–4126.
15. Buntru, A., Kopp, K., Voges, M., Frank, R., Bachmann, V., Hauck, C. R. (2011) Phosphatidylinositol 39-kinase activity is critical for initiating the oxidative burst and bacterial destruction during CEACAM3-mediated phagocytosis. J. Biol. Chem. 286, 9555–9566.
16. Kuroki, M., Arakawa, F., Matsuo, Y., Oikawa, S., Misumi, Y., Nakazato, H., Matsuoka, Y. (1991) Molecular cloning of nonspecific cross-reacting antigens in human granulocytes. J. Biol. Chem. 266, 11810–11817.
17. Kuroki, M., Yamanaka, T., Matsuo, Y., Oikawa, S., Nakazato, H., Matsuoka, Y. (1995) Immunochemical analysis of carcinoembryonic antigen (CEA)-related antigens differentially localized in intracellular granules of human neutrophils. Immunol. Invest. 24, 829–843.
18. Beauchemin, N., Draber, P., Dveksler, G., Gold, P., Gray-Owen, S., Grunert, F., Hammarström, S., Holmes, K. V., Karlsson, A., Kuroki, M., Lin, S. H., Lucka, L., Najjar, S. M., Neumaier, M., Obrink, B., Shively, J. E., Skubitz, K. M., Stanners, C. P., Thomas, P., Thompson, J. A., Virji, M., von Kleist, S., Wagener, C., Watt, S., Zimmermann, W. (1999) Redefined nomenclature for members of the carcinoembryonic antigen family. Exp. Cell Res. 252, 243–249.
19. Thompson, J., Mössinger, S., Reichardt, V., Engels, U., Beauchemin, N., Kommoss, F., von Kleist, S., Zimmermann, W. (1993) A polymerasechain- reaction assay for the specific identification of transcripts encoded by individual carcinoembryonic antigen (CEA)-gene-family members. Int. J. Cancer 55, 311–319.
20. Pils, S., Gerrard, D. T., Meyer, A., Hauck, C. R. (2008) CEACAM3: an innate immune receptor directed against human-restricted bacterial pathogens. Int. J. Med. Microbiol. 298, 553–560.
21. Kupsch, E.-M., Knepper, B., Kuroki, T., Heuer, I., Meyer, T. F. (1993) Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12, 641–650.
22. de Vries, F. P., van Der Ende, A., van Putten, J. P., Dankert, J. (1996) Invasion of primary nasopharyngeal epithelial cells by Neisseria meningitidis is controlled by phase variation of multiple surface antigens. Infect. Immun. 64, 2998–3006.
23. Pils, S., Kopp, K., Peterson, L., Delgado Tascón, J., Nyffenegger-Jann, N. J., Hauck, C. R. (2012) The adaptor molecule Nck localizes the WAVE complex to promote actin polymerization during CEACAM3-mediated phagocytosis of bacteria. PLoS ONE 7, e32808.
24. Kopp, K., Buntru, A., Pils, S., Zimmermann, T., Frank, R., Zumbusch, A., Hauck, C. R. (2012) Grb14 is a negative regulator of CEACAM3-mediated phagocytosis of pathogenic bacteria. J. Biol. Chem. 287, 39158–39170.
25. Schmitter, T., Pils, S., Sakk, V., Frank, R., Fischer, K. D., Hauck, C. R. (2007) The granulocyte receptor carcinoembryonic antigen-related cell adhesion molecule 3 (CEACAM3) directly associates with Vav to promote phagocytosis of human pathogens. J. Immunol. 178, 3797–3805.
26. Zhang, D. E., Hetherington, C. J., Chen, H. M., Tenen, D. G. (1994) The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol. Cell. Biol. 14, 373–381.
27. Tschan, M. P., Reddy, V. A., Ress, A., Arvidsson, G., Fey, M. F., Torbett, B. E. (2008) PU.1 binding to the p53 family of tumor suppressors impairs their transcriptional activity. Oncogene 27, 3489–3493.
28. Osoegawa, K., Mammoser, A. G., Wu, C., Frengen, E., Zeng, C., Catanese, J. J., de Jong, P. J. (2001) A bacterial artificial chromosome library for sequencing the complete human genome. Genome Res. 11, 483–496.
29. Muenzner, P., Bachmann, V., Zimmermann, W., Hentschel, J., Hauck, C. R. (2010) Human-restricted bacterial pathogens block shedding of epithelial cells by stimulating integrin activation. Science 329, 1197–1201.
30. Schmittgen, T. D., Livak, K. J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
31. Agerer, F., Michel, A., Ohlsen, K., 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.
32. Kuespert, K., Hauck, C. R. (2009) Characterizing host receptor recognition by individual bacterial pathogens. In Methods in Molecular Biology (S. Rupp, K. Sohn, N. Hauser, eds.), Humana, Totowa, NJ, USA, 57–65.
33. Kuespert, K., Weibel, S., Hauck, C. R. (2007) Profiling of bacterial adhesin—host receptor recognition by soluble immunoglobulin superfamily domains. J. Microbiol. Methods 68, 478–485.
34. Kuespert, K., Roth, A., Hauck, C. R. (2011) Neisseria meningitidis has two independent modes of recognizing its human receptor CEACAM1. PLoS ONE 6, e14609.
35. DeKoter, R. P., Walsh, J. C., Singh, H. (1998) PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/ macrophage progenitors. EMBO J. 17, 4456–4468.
36. Wang, K., Wang, P., Shi, J., Zhu, X., He, M., Jia, X., Yang, X., Qiu, F., Jin, W., Qian, M., Fang, H., Mi, J., Yang, X., Xiao, H., Minden, M., Du, Y., Chen, Z., Zhang, J. (2010) PML/RARalpha targets promoter regions containing PU.1 consensus and RARE half sites in acute promyelocytic leukemia. Cancer Cell 17, 186–197.
37. Chen, T., Grunert, F., Medina-Marino, A., Gotschlich, E. C. (1997) Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J. Exp. Med. 185, 1557–1564.
38. Virji, M., Evans, D., Griffith, J., Hill, D., Serino, L., Hadfield, A., Watt, S. M. (2000) Carcinoembryonic antigens are targeted by diverse strains of typable and non-typable Haemophilus influenzae. Mol. Microbiol. 36, 784–795.
39. Hill, D. J., Virji, M. (2003) A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the Ndomain of carcinoembryonic antigen-related cell adhesion molecules by UspA 1. Mol. Microbiol. 48, 117–129.
40. Brooks, M. J., Sedillo, J. L., Wagner, N., Wang, W., Attia, A. S., Wong, H., Laurence, C. A., Hansen, E. J., Gray-Owen, S. D. (2008) Moraxella catarrhalis binding to host cellular receptors is mediated by sequencespecific determinants not conserved among all UspA1 protein variants. Infect. Immun. 76, 5322–5329.
41. Popp, A., Dehio, C., Grunert, F., Meyer, T. F., Gray-Owen, S. D. (1999) Molecular analysis of neisserial Opa protein interactions with the CEA family of receptors: identification of determinants contributing to the differential specificities of binding. Cell. Microbiol. 1, 169–181.
42. Frank, R. (1992) SPOT synthesis: an easy technique for the positionally addressable, parallel chemical synthesis on a membrane support. Tetrahedron 48, 9217–9232.
43. Reth, M. (1989) Antigen receptor tail clue. Nature 338, 383–384.
44. Underhill, D. M., Rossnagle, E., Lowell, C. A., Simmons, R. M. (2005) Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 106, 2543–2550.
45. Rogers, N. C., Slack, E. C., Edwards, A. D., Nolte, M. A., Schulz, O., Schweighoffer, E., Williams, D. L., Gordon, S., Tybulewicz, V. L., Brown, G. D., Reis e Sousa, C. (2005) Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22, 507–517.
46. Indik, Z. K., Park, J. G., Hunter, S., Schreiber, A. D. (1995) The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood 86, 4389–4399.
47. Araki, N., Johnson, M. T., Swanson, J. A. (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135, 1249–1260.
48. McCaw, S. E., Liao, E. H., Gray-Owen, S. D. (2004) Engulfment of Neisseria gonorrhoeae: revealing distinct processes of bacterial entry by individual carcinoembryonic antigen-related cellular adhesion molecule family receptors. Infect. Immun. 72, 2742–2752.