Role of glycosylation/deglycolysation processes in Francisella tularensis pathogenesis

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue MAR, 2017, Pages

  Barel, Monique ^a,b,c   Charbit, Alain ^a,b,c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSERM   (France)

^c CNRS   (France)

Author keywords

Glycosylation; Host pathogen interaction

Indexed keywords

GLYCOSIDASE; GLYCOSYLTRANSFERASE; SOLUTE CARRIER FAMILY 1 MEMBER 5 PROTEIN; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; FRANCISELLA TULARENSIS; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLYCOSYLATION AND DEGLYCOSYLATION; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; HUMAN; MACROPHAGE; NONHUMAN; PATHOGENESIS; PHAGOSOME; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; TULAREMIA; ANIMAL; GENE EXPRESSION REGULATION; GLYCOSYLATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ANIMALS; FRANCISELLA TULARENSIS; GENE EXPRESSION REGULATION; GLYCOSIDE HYDROLASES; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES;

EID: 85027441177     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00071     Document Type: Article

References (38)

1. Abu Kwaik, Y., and Bumann, D. (2013). Microbial quest for food in vivo: “Nutritional virulence” as an emerging paradigm. Cell. Microbiol. 15, 882–890. doi: 10.1111/cmi.12138
2. Arya, S., Sethi, D., Singh, S., Hade, M. D., Singh, V., Raju, P., et al. (2013). Truncated hemoglobin, hbn, is post-translationally modified in Mycobacterium tuberculosis and modulates host-pathogen interactions during intracellular infection. J. Biol. Chem. 288, 29987–29999. doi: 10.1074/jbc.M113.507301
3. Balonova, L., Hernychova, L., Mann, B. F., Link, M., Bilkova, Z., Novotny, M. V., et al. (2010). A multimethodological approach to identification of glycoproteins from the proteome of Francisella tularensis, an intracellular microorganism. J. Proteome Res. 9, 1995–2005. doi: 10.1021/pr9011602
4. Balonova, L., Mann, B. F., Cerveny, L., Alley, W. R., Chovancova, E., Forslund, A.-L., et al. (2012). Characterization of protein glycosylation in Francisella tularensis subsp. holarctica: identification of a novel glycosylated lipoprotein required for virulence. Mol. Cell Proteomics 11:M111.015016. doi: 10.1074/mcp.M111.015016
5. Barel, M., Grall, N., and Charbit, A. (2015). Pathogenesis of Francisella tularensis in Humans. Hoboken, NJ: John Wiley & Sons, Inc.
6. Barel, M., Harduin-Lepers, A., Portier, L., Slomianny, M.-C., and Charbit, A. (2016). Host glycosylation pathways and the unfolded protein response contribute to the infection by Francisella. Cell. Microbiol. 18, 1763–1781. doi: 10.1111/cmi.12614
7. Barel, M., Meibom, K., Dubail, I., Botella, J., and Charbit, A. (2012). Francisella tularensis regulates the expression of the amino acid transporter SLC1A5 in infected THP-1 human monocytes. Cell. Microbiol. 14, 1769–1783. doi: 10.1111/j.1462-5822.2012.01837.x
8. Bastos, P. A. D., da Costa, J. P., and Vitorino, R. (2017). A glimpse into the modulation of post-translational modifications of human-colonizing bacteria. J. Proteomics 152, 254–275. doi: 10.1016/j.jprot.2016.11.005
9. Belyi, Y., Tabakova, I., Stahl, M., and Aktories, K. (2008). Lgt: a family of cytotoxic glucosyltransferases produced by Legionella pneumophila. J. Bacteriol. 190, 3026–3035. doi: 10.1128/JB.01798-07
10. Brotcke, A., Weiss, D. S., Kim, C. C., Chain, P., Malfatti, S., Garcia, E., et al. (2006). Identification of Mgla-regulated genes reveals novel virulence factors in Francisella tularensis. Infect. Immun. 74, 6642–6655. doi: 10.1128/IAI.01250-06
11. Case, E. D. R., Chong, A., Wehrly, T. D., Hansen, B., Child, R., Hwang, S., et al. (2014). The Francisella O-antigen mediates survival in the macrophage cytosol via autophagy avoidance. Cell. Microbiol. 16, 862–877. doi: 10.1111/cmi.12246
12. Chacko, B. K., Scott, D. W., Chandler, R. T., and Patel, R. P. (2011). Endothelial surface N-glycans mediate monocyte adhesion and are targets for antiinflammatory effects of peroxisome proliferator-activated receptor γ ligands. J. Biol. Chem. 286, 38738–38747. doi: 10.1074/jbc.M111.247981
13. Clemens, D. L., Lee, B. Y., and Horwitz, M. A. (2005). Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect. Immun. 73, 5892–5902. doi: 10.1128/IAI.73.9.5892-5902.2005
14. Console, L., Scalise, M., Tarmakova, Z., Coe, I. R., and Indiveri, C. (2015). N-linked glycosylation of human SLC1A5 (ASCT2) transporter is critical for trafficking to membrane. Biochim. Biophys. Acta 1853, 1636–1645. doi: 10.1016/j.bbamcr.2015.03.017
15. Dankova, V., Balonova, L., Link, M., Straskova, A., Sheshko, V., and Stulik, J. (2016). Inactivation of Francisella tularensis gene encoding putative ABC transporter has a pleiotropic effect upon production of various glycoconjugates. J. Proteome Res. 15, 510–524. doi: 10.1021/acs.jproteome.5b00864
16. Dey, B., and Bishai, W. R. (2014). Crosstalk between Mycobacterium tuberculosis and the host cell. Semin. Immunol. 26, 486–496. doi: 10.1016/j.smim.2014.09.002
17. Di Gioia, M., and Zanoni, I. (2015). Toll-like receptor co-receptors as master regulators of the immune response. Mol. Immunol. 63, 143–152. doi: 10.1016/j.molimm.2014.05.008
18. Egge-Jacobsen, W., Salomonsson, E. N., Aas, F. E., Forslund, A.-L., Winther-Larsen, H. C., Maier, J., et al. (2011). O-linked glycosylation of the pila pilin protein of Francisella tularensis: identification of the endogenous protein-targeting oligosaccharyltransferase and characterization of the native oligosaccharide. J. Bacteriol. 193, 5487–5497. doi: 10.1128/JB.00383-11
19. Hetz, C., Martinon, F., Rodriguez, D., and Glimcher, L. H. (2011). The unfolded protein response: integrating stress signals through the stress sensor IRE1α. Physiol. Rev. 91, 1219–1243. doi: 10.1152/physrev.00001.2011
20. Lu, Q., Li, S., and Shao, F. (2015). Sweet talk: protein glycosylation in bacterial interaction with the host. Trends Microbiol. 23, 630–641. doi: 10.1016/j.tim.2015.07.003
21. Meibom, K. L., and Charbit, A. (2010). The unraveling panoply of Francisella tularensis virulence attributes. Curr. Opin. Microbiol. 13, 11–17. doi: 10.1016/j.mib.2009.11.007
22. Miller, C., and Celli, J. (2016). Avoidance and subversion of eukaryotic homeostatic autophagy mechanisms by bacterial pathogens. J. Mol. Biol. 428, 3387–3398. doi: 10.1016/j.jmb.2016.07.007
23. Moran, A. P., Gupta, A., and Joshi, L. (2011). Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut 60, 1412–1425. doi: 10.1136/gut.2010.212704
24. Ni, M., Zhou, H., Wey, S., Baumeister, P., and Lee, A. Y. (2009). Regulation of PERK signaling and leukemic cell survival by a novel cytosolic isoform of the UPR regulator GRP78/BiP. PLoS ONE 4:e6868. doi: 10.1371/journal.pone.0006868
25. Nizet, V., and Esko, J. (2009). “Chapter 39: Bacterial and viral infections,” in Essentials of Glycobiology, 2nd Edn., eds R. D. Cummings, A. Varki, J. D. Esko H. H. Freeze, P. Stanley, C. R. Bertozzi, G. W. Hart, and M. E. Etzler (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), 1–16.
26. Opdenakker, G., Proost, P., and Van Damme, J. (2016). Microbiomic and posttranslational modifications as preludes to autoimmune diseases. Trends Mol. Med. 22, 746–757. doi: 10.1016/j.molmed.2016.07.002
27. Pfaffenbach, K. T., and Lee, A. S. (2011). The critical role of of GRP78 in physiologic and pathologic stress. Curr. Opin. Cell Biol. 23, 150–156. doi: 10.1016/j.ceb.2010.09.007
28. Ray, K., Marteyn, B., Sansonetti, P. J., and Tang, C. M. (2009). Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat. Rev. Microbiol. 7, 333–340. doi: 10.1038/nrmicro2112
29. Santic, M., Al Khodor, S., and Abu Kwaik, Y. (2010). Cell biology and molecular ecology of Francisella tularensis. Cell. Microbiol. 12, 129–139. doi: 10.1111/j.1462-5822.2009.01400.x
30. Schäffer, C., and Messner, P. (2016). Emerging facets of prokaryotic glycosylation. FEMS Microbiol. Rev. 41, 49–91. doi: 10.1093/femsre/fuw036
31. Sjöstedt, A. (2011). Special topic on Francisella tularensis and tularemia. Front. Cell. Infect. Microbiol. 2:86. doi: 10.3389/fmicb.2011.00086
32. Tan, F. Y. Y., Tang, C. M., and Exley, R. M. (2015). Sugar coating: bacterial protein glycosylation and host–microbe interactions. Trends Biochem. Sci. 40, 342–350. doi: 10.1016/j.tibs.2015.03.016
33. Thomas, R. M., Twine, S. M., Fulton, K. M., Tessier, L., Kilmury, S. L. N., Ding, W., et al. (2011). Glycosylation of DsbA in francisella tularensis subsp. tularensis. J Bacteriol 193, 5498–5509. doi: 10.1128/JB.00438-11
34. Tytgat, H. L. P., and de Vos, W. M. (2016). Sugar coating the envelope: glycoconjugates for microbe–host crosstalk. Trends Microbiol. 24, 853–861. doi: 10.1016/j.tim.2016.06.004
35. Vaidyanathan, K., Durning, S., and Wells, L. (2014). Functional O-GlcNac modifications: implications in molecular regulation and pathophysiology. Crit. Rev. Biochem. Mol. Biol. 49, 140–163. doi: 10.3109/10409238.2014.884535
36. Varki, A. (1993). Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3, 97–130. doi: 10.1093/glycob/3.2.97
37. Walters, K-A., Olsufka, R., Kuestner, R. E., Cho, J. H., Li, H., Zornetzer,G. A., et al. (2013). Francisella tularensis subsp. tularensis induces a unique pulmonary inflammatory response: role of bacterial gene expression in temporal regulation of host defense responses. PLoS ONE 8:e62412. doi: 10.1371/journal.pone.0062412
38. Zhang, Y. J., andRubin, E. J. (2013). Feast or famine: the host–pathogen battle over amino acids. Cell. Microbiol. 15, 1079–1087. doi: 10.1111/cmi.12140