Glycosylation changes as important factors for the susceptibility to urinary tract infection

Biochemical Society Transactions

Volumn 39, Issue 1, 2011, Pages 349-354

  Taganna, Joemar ^a   De Boer, Arjen R ^b   Wuhrer, Manfred ^b   Bouckaert, Julie ^c  

^a GHENT UNIVERSITY   (Belgium)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

Adhesion; Apoptosis; Diabetes mellitus; FimH; Paucimannosidic glycan; Urinary tract infection

Indexed keywords

ADHESIN; CELL RECEPTOR; CLATHRIN; GLUCOSE TRANSPORTER; GLYCOPROTEIN; INVASIN; OLIGOMANNOSE 3; OLIGOMANNOSE 5; TAMM HORSFALL GLYCOPROTEIN; UNCLASSIFIED DRUG; UROPLAKIN; VIRULENCE FACTOR;

APOPTOSIS; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING AFFINITY; CONFERENCE PAPER; CONFORMATIONAL TRANSITION; CROHN DISEASE; DISEASE PREDISPOSITION; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; ESCHERICHIA COLI; FIMBRIA; GLYCOSYLATION; HUMAN; MEMBRANE VESICLE; MOLECULAR RECOGNITION; NONHUMAN; PERSISTENT INFECTION; PEYER PATCH; PREVALENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RECURRENT INFECTION; SIGNAL TRANSDUCTION; ULCERATIVE COLITIS; URINARY TRACT INFECTION;

ADHESINS, ESCHERICHIA COLI; ANIMALS; BACTERIAL ADHESION; DISEASE SUSCEPTIBILITY; FEMALE; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GLYCOSYLATION; HUMANS; MALE; MICROARRAY ANALYSIS; POLYSACCHARIDES; PROTEIN BINDING; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI; UROTHELIUM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79551485503     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390349     Document Type: Conference Paper

References (46)

1. Thumbikat, P., Berry, R.E., Zhou, G., Billips, B.K., Yaggie, R.E., Zaichuk, T., Sun, T.T., Schaeffer, A.J. and Klumpp, D.J. (2009) Bacteria-induced uroplakin signaling mediates bladder response to infection. PLoS Pathog. 5, e1000415
2. Hannan, T.J., Mysorekar, I.U., Hung, C.S., Isaacson-Schmid, M.L. and Hultgren, S.J. (2010) Early severe inflammatory responses to uropathogenic E. coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog. 6, e1001042
3. Mulvey, M.A., Schilling, J.D. and Hultgren, S.J. (2001) Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect. Immun. 69, 4572-4579
4. Mysorekar, I.U., Mulvey, M.A., Hultgren, S.J. and Gordon, J.I. (2002) Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J. Biol. Chem. 277, 7412-7419
5. Bouckaert, J., Berglund, J., Schembri, M., De Genst, E., Cools, L., Wuhrer, M., Hung, C.S., Pinkner, J., Slattegard, R., Zavialov, A. et al. (2005) Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol. Microbiol. 55, 441-455
6. Zhou, G., Mo, W.J., Sebbel, P., Min, G., Neubert, T.A., Glockshuber, R., Wu, X.R., Sun, T.T. and Kong, X.P. (2001) Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J. Cell Sci. 114, 4095-4103
7. Serafini-Cessi, F., Monti, A. and Cavallone, D. (2005) N-glycans carried by Tamm-Horsfall glycoprotein have a crucial role in the defense against urinary tract diseases. Glycoconjugate J. 22, 383-394
8. 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
9. Wang, H., Min, G., Glockshuber, R., Sun, T.T. and Kong, X.P. (2009) Uropathogenic E. coli adhesin-induced host cell receptor conformational changes: implications in transmembrane signaling transduction. J. Mol. Biol. 392, 352-361
10. Min, G., Stolz, M., Zhou, G., Liang, F., Sebbel, P., Stoffler, D., Glockshuber, R., Sun, T.T., Aebi, U. and Kong, X.P. (2002) Localization of uroplakin Ia, the urothelial receptor for bacterial adhesin FimH, on the six inner domains of the 16 nm urothelial plaque particle. J. Mol. Biol. 317, 697-706
11. Xie, B., Zhou, G., Chan, S.Y., Shapiro, E., Kong, X.P., Wu, X.R., Sun, T.T. and Costello, C.E. (2006) Distinct glycan structures of uroplakins Ia and Ib: structural basis for the selective binding of FimH adhesin to uroplakin Ia4. J. Biol. Chem. 281, 14644-14653
12. Wellens, A., Garofalo, C., Nguyen, H., Van Gerven, N., Slattegard, R., Hernalsteens, J.P., Wyns, L., Oscarson, S., De Greve, H., Hultgren, S. and Bouckaert, J. (2008) Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS ONE 3, e2040
13. + bacteria by M cells initiates mucosal immune response. Nature 462, 226-230
14. Carvalho, F.A., Barnich, N., Sivignon, A., Darcha, C., Chan, C.H., Stanners, C.P. and Darfeuille-Michaud, A. (2009) Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J. Exp. Med. 206, 2179-2189
15. Bouckaert, J., Mackenzie, J., de Paz, J.L., Chipwaza, B., Choudhury, D., Zavialov, A., Mannerstedt, K., Anderson, J., Pierard, D., Wyns, L. et al. (2006) The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol. Microbiol. 61, 1556-1568
16. Chen, S.L., Hung, C.S., Pinkner, J.S., Walker, J.N., Cusumano, C.K., Li, Z., Bouckaert, J., Gordon, J.I. and Hultgren, S.J. (2009) Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. Proc. Natl. Acad. Sci. U.S.A. 106, 22439-22444
17. Hung, C.-S., Bouckaert, J., Hung, D.L., Pinkner, J., Winberg, C., Defusco, A., Auguste, C.G., Strouse, R., Langermann, S., Waksman, G. and Hultgren, S.J. (2002) Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 44, 903-915
18. Geerlings, S.E. (2008) Urinary tract infections in patients with diabetes mellitus: epidemiology, pathogenesis and treatment. Int. J. Antimicrob. Agents 31 (Suppl. 1), S54-S57
19. Geerlings, S.E., Meiland, R., van Lith, E.C., Brouwer, E.C., Gaastra, W. and Hoepelman, A.I. M. (2002) Adherence of type 1-fimbriated Escherichia coli to uroepithelial cells: more in diabetic women than in control subjects. Diabetes Care 25, 1405-1409
20. Knight, S.D. and Bouckaert, J. (2009) Structure, function, and assembly of type 1 fimbriae. Top. Curr. Chem. 288, 67-107
21. Reeves, P.J., Callewaert, N., Contreras, R. and Khorana, H.G. (2002) Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl. Acad. Sci. U.S.A. 99, 13419-13424
22. de Boer, A.R., Hokke, C.H., Deelder, A.M. and Wuhrer, M. (2007) General microarray technique for immobilization and screening of natural glycans. Anal. Chem. 79, 8107-8113
23. Lonardi, E., Balog, C.I., Deelder, A.M. and Wuhrer, M. (2010) Natural glycan microarrays. Expert Rev. Proteomics 7, 761-774
24. Watts, J.C., Huo, H., Bai, Y., Ehsani, S., Jeon, A.H., Shi, T., Daude, N., Lau, A., Young, R., Xu, L. et al. (2009) Interactome analyses identify ties of PrP and its mammalian paralogs to oligomannosidic N-glycans and endoplasmic reticulum-derived chaperones. PLoS Pathog. 5, e1000608
25. Lau, K.S., Partridge, E.A., Grigorian, A., Silvescu, C.I., Reinhold, V.N., Demetriou, M. and Dennis, J.W. (2007) Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129, 123-134
26. Dam, T.K. and Brewer, F.C. (2010) Maintenance of cell surface glycan density by lectin-glycan interactions: a homeostatic and innate immune regulatory mechanism. Glycobiology 20, 1061-1064
27. Eto, D.S. and Mulvey, M.A. (2007) Flushing bacteria out of the bladder. Nat. Med. 13, 531-532
28. Sharon, N. and Lis, H. (1993) Carbohydrates in cell recognition. Sci. Am. 268, 82-89
29. Mysorekar, I.U. and Hultgren, S.J. (2006) Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc. Natl. Acad. Sci. U.S.A. 103, 14170-14175
30. Eto, D.S., Sundsbak, J.L. and Mulvey, M.A. (2006) Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli. Cell. Microbiol. 8, 704-717
31. Mysorekar, I.U., Isaacson-Schmid, M., Walker, J.N., Mills, J.C. and Hultgren, S.J. (2009) Bone morphogenetic protein 4 signaling regulates epithelial renewal in the urinary tract in response to uropathogenic infection. Cell Host Microbe 5, 463-475
32. Franz, S., Herrmann, K., Furnrohr, B.G., Sheriff, A., Frey, B., Gaipl, U.S., Voll, R.E., Kalden, J.R., Jack, H.M. and Herrmann, M. (2007) After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ. 14, 733-742
33. Bilyy, R., Kit, Y., Hellman, U., Tryndyak, V., Kaminskyy, V. and Stoika, R. (2005) In vivo expression and characteristics of novel α-D-mannose-rich glycoprotein markers of apoptotic cells. Cell Biol. Int. 29, 920-928
34. Bilyy, R. and Stoika, R. (2007) Search for novel cell surface markers of apoptotic cells. Autoimmunity 40, 249-253
35. Meesmann, H.M., Fehr, E.M., Kierschke, S., Herrmann, M., Bilyy, R., Heyder, P., Blank, N., Krienke, S., Lorenz, H.M. and Schiller, M. (2010) Decrease of sialic acid residues as an eat-me signal on the surface of apoptotic lymphocytes. J. Cell Sci. 123, 3347-3356
36. Rosen, D.A., Hooton, T.M., Stamm, W.E., Humphrey, P.A. and Hultgren, S.J. (2007) Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med. 4, e329
37. Muenzner, P., Bachmann, V., Zimmermann, W., Hentschel, J. and Hauck, C.R. (2010) Human-restricted bacterial pathogens block shedding of epithelial cells by stimulating integrin activation. Science 329, 1197-1201
38. Sukumaran, S.K., Fu, N.Y., Tin, C.B., Wan, K.F., Lee, S.S. and Yu, V.C. (2010) A soluble form of the pilus protein FimA targets the VDAC-hexokinase complex at mitochondria to suppress host cell apoptosis. Mol. Cell 37, 768-783
39. Vagin, O., Kraut, J.A. and Sachs, G. (2009) Role of N-glycosylation in trafficking of apical membrane proteins in epithelia. Am. J. Physiol. Renal Physiol. 296, F459-F469
40. Ahmad, N., Gabius, H.J., Andre, S., Kaltner, H., Sabesan, S., Roy, R., Liu, B., Macaluso, F. and Brewer, C.F. (2004) Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J. Biol. Chem. 279, 10841-10847
41. Vassilopoulos, S., Esk, C., Hoshino, S., Funke, B.H., Chen, C.Y., Plocik, A.M., Wright, W.E., Kucherlapati, R. and Brodsky, F.M. (2009) A role for the CHC22 clathrin heavy-chain isoform in human glucose metabolism. Science 324, 1192-1196
42. Tsao, T.S., Burcelin, R., Katz, E.B., Huang, L. and Charron, M.J. (1996) Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 45, 28-36
43. Kolm-Litty, V., Sauer, U., Nerlich, A., Lehmann, R. and Schleicher, E.D. (1998) High glucose-induced transforming growth factor β1 production is mediated by the hexosamine pathway in porcine glomerular mesangial cells. J. Clin. Invest. 101, 160-169
44. Rosen, D.A., Hung, C.S., Kline, K.A. and Hultgren, S.J. (2008) Streptozocin-induced diabetic mouse model of urinary tract infection. Infect. Immun. 76, 4290-4298
45. Carlson, C.M., Turpin, E.A., Moser, L.A., O'Brien, K.B., Cline, T.D., Jones, J.C., Tumpey, T.M., Katz, J.M., Kelley, L.A., Gauldie, J. and Schultz-Cherry, S. (2010) Transforming growth factor-β: activation by neuraminidase and role in highly pathogenic H5N1 influenza pathogenesis. PLoS Pathog. 6, e1001136
46. Chuang, P.Y., Yu, Q., Fang, W., Uribarri, J. and He, J.C. (2007) Advanced glycation endproducts induce podocyte apoptosis by activation of the FOXO4 transcription factor. Kidney Int. 72, 965-976