Inhibition of CEA release from epithelial cells by lipid A of Gram-negative bacteria
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Fakhraddin Naghibalhossaini
,
Khatere Sayadi
Abstract
A number of bacterial species, both pathogenic and non-pathogenic, use the human CEACAM family members as receptors for internalization into epithelial cells. The GPI-linked CEA and CEACAM6 might play a role in the innate immune defense, protecting the colon from microbial invasion. Previous studies showed that CEA is released from epithelial cells by an endogenous GPI-PLD enzyme. GPI-PLD activity was reported to be inhibited by several synthetic and natural forms of lipid A. We hypothesized that CEA engagement by Gram-negative bacteria might attenuate CEA release from epithelial cells and that this might facilitate bacterial colonization. We tested the hypothesis by examining the effect of Escherichia coli on CEA release from colorectal cancer cells in a co-culture experiment. A subconfluent monolayer culture of colorectal cancer cells (LS-180, Caco-2 and HT29/219) was incubated with E. coli. While there was a significant reduction in CEA secretion from LS-180 and HT29/219 cells, we found only a small reduction of CEA shedding from Caco-2 cells compared to the level from the untreated control cells. Furthermore, lipid A treatment of LS-180 cells inhibited CEA release from the cells in a dosedependent manner. Western blot analysis of total lysates showed that CEA expression levels in cells co-cultured with bacteria did not differ from those in untreated control cells. These results suggest that lipid A of Gram-negative bacteria might play a role in preventing the release of CEA from mucosal surfaces and promote mucosal colonization by bacteria.
References
1. Baranov, V. and Hammarström S. Carcinoembryonic antigen (CEA) and CEA-related cell adhesion molecule 1 (CEACAM1), apically expressed on human colonic M cells, are potential receptors for microbial adhesion. Histochem. Cell Biol. 121 (2004) 83-89.Suche in Google Scholar
2. Bos M.P., Hogan D. and Belland R.J. Homologue scanning mutagenesis reveals CD66 receptor residues required for neisserial Opa protein binding. J. Exp. Med. 190 (1999) 331-340.Suche in Google Scholar
3. Popp, A., Dehio, C., Grunert, F., Meyer, T.F. and Gray-Owen, S.D. 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 (1999) 169-181.Suche in Google Scholar
4. Virji, M., Evans, D., Hadfield, A., Grunert, F., Teixeira, A.M. and Watt, S.M. Critical determinants of host receptor targeting by Neisseria meningitidis and Neisseria gonorrhoeae: identification of Opa adhesiotopes on the N-domain of CD66 molecules. Mol. Microbiol. 34 (1999) 538-551.Suche in Google Scholar
5. Kuespert, K., Pils, S. and Hauck, C.R. CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 18 (2006) 565-571, DOI:10. 1016/j.ceb.2006.08.008.Suche in Google Scholar
6. Kammerer, R. and Zimmermann, W. Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol. 8 (2010) 12, DOI: 10.1186/1741-7007-8-12.10.1186/1741-7007-8-12Suche in Google Scholar PubMed PubMed Central
7. Benchimol S., Fuks, A., Jothy, S., Beauchemin, N., Shirota, K. and Stanners, C.P. Carcinoembryonic antigen, a human tumor marker, functions as an intercellular adhesion molecule. Cell 57 (1989) 327-334.Suche in Google Scholar
8. Jessup, J.M. and Thomas, P. CEA and Metastasis: A Faciliator of Site- Specific Metastasis. in: Cell Adhesion and Communication Mediated by the CEA family. Basic and Clinical Perspectives (Stanners, C.P., Ed.), 1st edition. Harwood Academic Publishers, Amsterdam, 1998, 195-222.Suche in Google Scholar
9. Kinugasa, T., Kuroki, M., Yamanaka, T., Matsuo, Y., Oikawa, S., Nakazato, H. and Matsuoka, Y. Non-proteolytic release of carcinoembryonic antigen from normal human colonic epithelial cells cultured in collagen gel. Int. J. Cancer 58 (1994) 102-107.Suche in Google Scholar
10. Matsuoka, Y., Matsuo, Y., Okamoto, N., Kuroki, M., Kuroki, M. and Ikehara, Y. Highly effective extraction of carcinoembryonic antigen with phosphatidylinositol-specific phospholipase C. Tumour Biol. 12 (1991) 91-98.Suche in Google Scholar
11. Baranov, V., Yeung, M.M. and Hammarström, S. Expression of carcinoembryonic antigen and nonspecific cross-reacting 50-kDa antigen in human normal and cancerous colon mucosa: comparative ultrastructural study with monoclonal antibodies. Cancer Res. 54 (1994) 3305-3314.Suche in Google Scholar
12. Frängsmyr, L., Baranov, V., Prall, F., Yeung, M.M., Wagener, C. and Hammarström, S. Cell- and region-specific expression of biliary glycoprotein and its messenger RNA in normal human colonic mucosa. Cancer Res. 55 (1995) 2963-2867.Suche in Google Scholar
13. Hammarström, S. and Baranov, V. Is there a role for CEA in innate immunity in the colon? Trends Microbiol. 9 (2001) 119-125.Suche in Google Scholar
14. Hammarström, S. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9 (1999) 67-81.Suche in Google Scholar
15. Naghibalhossaini, F. and Ebadi, P. Evidence for CEA release from human colon cancer cells by an endogenous GPI-PLD enzyme. Cancer Lett. 234 (2006) 158-167. DOI:10.1016/j.canlet.2005.03.028.10.1016/j.canlet.2005.03.028Suche in Google Scholar PubMed
16. Yamamoto, Y., Hirakawa, E., Mori, S., Hamada, Y., Kawaguchi, N. and Matsuura, N. Cleavage of carcinoembryonic antigen induces metastatic potential in colorectal carcinoma. Biochem. Biophys. Res. Commun. 333 (2005) 223-229. DOI:10.1016/j.bbrc.2005.05.084. 10.1016/j.bbrc.2005.05.084Suche in Google Scholar PubMed
17. Low, M.G. and Huang, K-S. Phosphatidic acid, lysophosphatidic acid, and lipid A are inhibitors of glycosylphosphatidylinositolspecific phospholipase D. Specific inhibition of a phospholipase by product analogues? J. Biol. Chem. 268 (1993) 8480-8490.Suche in Google Scholar
18. Low, M.G. and Stütz, P. Inhibition of the plasma glycosylphosphatidylinositolspecific phospholipase D by synthetic analogs of lipid A and phosphatidic acid. Arch. Biochem. Biophys. 371(1999) 332-339. DOI:10.1006/abbi. 1999.1436.Suche in Google Scholar
19. Pakdel, A., Naghibalhossaini, F., Mokarram, P., Jaberipour, M. and Hosseini, A. Regulation of carcinoembryonic antigen release from colorectal cancer cells. Mol. Biol. Rep. 39 (2012) 3695-3704.Suche in Google Scholar
20. Chen, T., Grunert, F., Medina-Marinom, A. and Gotschlich, E.C. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J. Exp. Med. 185 (1997) 1557-1564. DOI: 10.1084/jem. 185.9.1557.10.1084/jemSuche in Google Scholar
21. Hill, D.J. and Virji, M.A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol. Microbiol. 48 (2003) 117-129. DOI: 10.1046/j.1365-2958. 2003.03433.x.Suche in Google Scholar
22. Berger, C.N., Billker, O., Meyer, T.F., Servin, A.L. and Kansau, I. Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol. Microbiol. 52 (2004) 963-983. DOI: 10.1111/j.1365-2958.2004. 04033.x.Suche in Google Scholar
23. Voges, M., Bachmann, V., Kammerer, R., Gophna, U. and Hauck, C.R. CEACAM1 recognition by bacterial pathogens is species-specific. BMC Microbiology 10 (2010) 117. DOI: 10.1186/1471-2180-10-117.10.1186/1471-2180-10-117Suche in Google Scholar PubMed PubMed Central
24. Kuespert, K., Pils, S. and Hauck, C.R. CEACAMs - their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 18 (2006) 565-571. DOI:10. 1016/j.ceb.2006.08.008.Suche in Google Scholar
25. Muenzner, P., Rohde, M., Kneitz, S. and Hauck, C.R. CEACAM engagement by human pathogens enhances cell adhesion and counteracts bacteria-induced detachment of epithelial cells. J. Cell Biol. 17 (2005) 825-836.Suche in Google Scholar
26. Kim, M., Ogawa, M., Fujita, Y., Yoshikawa, Y., Nagai, T., Koyama, T., Nagai, S., Lange, A. Fässler, R. and Sasakawa, C. Bacteria hijack integrinlinked kinase to stabilize focal adhesions and block cell detachment. Nature 459 (2009) 578-582. DOI: 10.1038/nature07952.10.1038/nature07952Suche in Google Scholar PubMed
27. Turner, A., Chen, S.N., Joike, M.K., Pendland, S.L., Pauli, G.F. and Farnsworth, N.R. Inhibition of uropathogenic Escherichia coli by cranberry juice: A new antiadherence assay. J. Agric. Food Chem. 53 (2005) 8940-8947.Suche in Google Scholar
28. Leusch, H.G., Drzeniek, Z., Markos-Pusztai, Z. and Wagener, C. Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose. Infect. Immun. 59 (1991) 2051-2057.Suche in Google Scholar
29. Sauter, S.L., Rutherfurd, S.M., Wagener, C., Shively, J.E. and Hefta, S.A. Identification of the specific oligosaccharide sites recognized by type 1 fimbriae from Escherichia coli on nonspecific cross-reacting antigen, a CD66 cluster granulocyte glycoprotein. J. Biol. Chem. 25 (1993) 15510-15516.Suche in Google Scholar
30. Korotkova, N., Yarova-Yarovaya, Y., Tchesnokova, V., Yazvenko, N., Carl, M.A., Stapleton, A.E. and Moseley, S.L. Escherichia coli DraE adhesin-associated bacterial internalization by epithelial cells is promoted independently by decay-accelerating factor and carcinoembryonic antigenrelated cell adhesion molecule binding and does not require the DraD invasin. Infect. Immun. 76 (2008) 3869-3880. DOI: 10.1128/IAI.00427-08. 10.1128/IAI.00427-08Suche in Google Scholar PubMed PubMed Central
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Artikel in diesem Heft
- Transcriptional profiling of bovine muscle-derived satellite cells during differentiation in vitro by high throughput RNA sequencing
- Inhibition of CEA release from epithelial cells by lipid A of Gram-negative bacteria
- Neurotrophine-3 may contribute to neuronal differentiation of mesenchymal stem cells through the activation of the bone morphogenetic protein pathway
- In vitro and in vivo analysis of human fibroblast reprogramming and multipotency
- The pharmacological features of bilirubin: the question of the century
- Evaluation of the expressions pattern of miR-10b, 21, 200c, 373 and 520c to find the correlation between epithelial-to-mesenchymal transition and melanoma stem cell potential in isolated cancer stem cells
- Effects of neuritin on the migration, senescence and proliferation of human bone marrow mesenchymal stem cells
- Lipoxin A4 methyl ester alleviates vascular cognition impairment by regulating the expression of proteins related to autophagy and ER stress in the rat hippocampus
- Biomedical and agricultural applications of energy dispersive X-ray spectroscopy in electron microscopy
- The effect of the bioactive sphingolipids S1P and C1P on multipotent stromal cells – new opportunities in regenerative medicine
