An iron-containing dodecameric heptosyltransferase family modifies bacterial autotransporters in pathogenesis

Cell Host and Microbe

Volumn 16, Issue 3, 2014, Pages 351-363

  Lu, Qiuhe ^a   Yao, Qing ^a   Xu, Yue ^a,b   Li, Lin ^a   Li, Shan ^a   Liu, Yanhua ^c   Gao, Wenqing ^a   Niu, Miao ^a   Sharon, Michal ^d   Ben Nissan, Gili ^d   Zamyatina, Alla ^e   Liu, Xiaoyun ^c   Chen, She ^a   Shao, Feng ^a,f  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c PEKING UNIVERSITY   (China)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^e UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^f INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CARRIER PROTEIN; HEPTOSE; IRON CONTAINING DODECAMERIC HEPTOSYLTRANSFERASE; PROTEIN AAH2; PROTEIN AIDA I; PROTEIN TIBA; TRANSFERASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; AIDA-I PROTEIN, E COLI; GLYCOSYLTRANSFERASE; HEPTOSYLTRANSFERASE; IRON;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BETA SHEET; CITROBACTER RODENTIUM; CONTROLLED STUDY; CYTOPLASM; ENTEROBACTERIACEAE; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CHEMISTRY; ENTEROBACTERIACEAE INFECTION; ENZYMOLOGY; ESCHERICHIA COLI INFECTION; GENETICS; GLYCOSYLATION; MALE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MOUSE; PATHOGENICITY; PHYSIOLOGY; SEQUENCE ALIGNMENT; VIRULENCE;

BACTERIA (MICROORGANISMS);

ADHESINS, ESCHERICHIA COLI; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; CITROBACTER RODENTIUM; ENTEROBACTERIACEAE INFECTIONS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HUMANS; IRON; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; VIRULENCE;

EID: 84907699044     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.08.008     Document Type: Article

References (39)

1. M. Abu-Qarn, J. Eichler, and N. Sharon Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea Curr. Opin. Struct. Biol. 18 2008 544 550
2. I. Benz, and M.A. Schmidt Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli Infect. Immun. 57 1989 1506 1511
3. I. Benz, and M.A. Schmidt Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin Mol. Microbiol. 40 2001 1403 1413
4. I. Benz, and M.A. Schmidt Never say never again: protein glycosylation in pathogenic bacteria Mol. Microbiol. 45 2002 267 276
5. I. Benz, and M.A. Schmidt Structures and functions of autotransporter proteins in microbial pathogens Int. J. Med. Microbiol. 301 2011 461 468
6. M.E. Charbonneau, and M. Mourez Functional organization of the autotransporter adhesin involved in diffuse adherence J. Bacteriol. 189 2007 9020 9029
7. M.E. Charbonneau, J.P. Côté, M.F. Haurat, B. Reiz, S. Crépin, F. Berthiaume, C.M. Dozois, M.F. Feldman, and M. Mourez A structural motif is the recognition site for a new family of bacterial protein O-glycosyltransferases Mol. Microbiol. 83 2012 894 907
8. N. Dautin, and H.D. Bernstein Protein secretion in gram-negative bacteria via the autotransporter pathway Annu. Rev. Microbiol. 61 2007 89 112
9. D.H. Dube, and C.R. Bertozzi Metabolic oligosaccharide engineering as a tool for glycobiology Curr. Opin. Chem. Biol. 7 2003 616 625
10. D.H. Dube, K. Champasa, and B. Wang Chemical tools to discover and target bacterial glycoproteins Chem. Commun. (Camb.) 47 2011 87 101
11. E.A. Elsinghorst, and J.A. Weitz Epithelial cell invasion and adherence directed by the enterotoxigenic Escherichia coli tib locus is associated with a 104-kilodalton outer membrane protein Infect. Immun. 62 1994 3463 3471
12. P. Emsley, I.G. Charles, N.F. Fairweather, and N.W. Isaacs Structure of Bordetella pertussis virulence factor P.69 pertactin Nature 381 1996 90 92
13. W.W. Fish Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples Methods Enzymol. 158 1988 357 364
14. C.M. Fletcher, M.J. Coyne, O.F. Villa, M. Chatzidaki-Livanis, and L.E. Comstock A general O-glycosylation system important to the physiology of a major human intestinal symbiont Cell 137 2009 321 331
15. K.A. Gangwer, D.J. Mushrush, D.L. Stauff, B. Spiller, M.S. McClain, T.L. Cover, and D.B. Lacy Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain Proc. Natl. Acad. Sci. USA 104 2007 16293 16298
16. I.R. Henderson, F. Navarro-Garcia, M. Desvaux, R.C. Fernandez, and D. Ala'Aldeen Type V protein secretion pathway: the autotransporter story Microbiol. Mol. Biol. Rev. 68 2004 692 744
17. J. Jose, and T.F. Meyer The autodisplay story, from discovery to biotechnical and biomedical applications Microbiol. Mol. Biol. Rev. 71 2007 600 619
18. B. Kneidinger, C. Marolda, M. Graninger, A. Zamyatina, F. McArthur, P. Kosma, M.A. Valvano, and P. Messner Biosynthesis pathway of ADP-L-glycero-beta-D-manno-heptose in Escherichia coli J. Bacteriol. 184 2002 363 369
19. N.R. Lazar Adler, J.M. Stevens, M.P. Stevens, and E.E. Galyov Autotransporters and Their Role in the Virulence of Burkholderia pseudomallei and Burkholderia mallei Front. Microbiol. 2 2011 151
20. D.L. Leyton, A.E. Rossiter, and I.R. Henderson From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis Nat. Rev. Microbiol. 10 2012 213 225
21. S. Li, L. Zhang, Q. Yao, L. Li, N. Dong, J. Rong, W. Gao, X. Ding, L. Sun, and X. Chen Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains Nature 501 2013 242 246
22. C. Lindenthal, and E.A. Elsinghorst Identification of a glycoprotein produced by enterotoxigenic Escherichia coli Infect. Immun. 67 1999 4084 4091
23. S.A. Longwell, and D.H. Dube Deciphering the bacterial glycocode: recent advances in bacterial glycoproteomics Curr. Opin. Chem. Biol. 17 2013 41 48
24. J. Maurer, J. Jose, and T.F. Meyer Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli J. Bacteriol. 179 1997 794 804
25. C. Moormann, I. Benz, and M.A. Schmidt Functional substitution of the TibC protein of enterotoxigenic Escherichia coli strains for the autotransporter adhesin heptosyltransferase of the AIDA system Infect. Immun. 70 2002 2264 2270
26. H. Nothaft, and C.M. Szymanski Protein glycosylation in bacteria: sweeter than ever Nat. Rev. Microbiol. 8 2010 765 778
27. B.R. Otto, R. Sijbrandi, J. Luirink, B. Oudega, J.G. Heddle, K. Mizutani, S.Y. Park, and J.R. Tame Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli J. Biol. Chem. 280 2005 17339 17345
28. J. Pohlner, R. Halter, K. Beyreuther, and T.F. Meyer Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease Nature 325 1987 458 462
29. C.R. Raetz, and C. Whitfield Lipopolysaccharide endotoxins Annu. Rev. Biochem. 71 2002 635 700
30. M. Ravi, M. Ngeleka, S.H. Kim, C. Gyles, F. Berthiaume, M. Mourez, D. Middleton, and E. Simko Contribution of AIDA-I to the pathogenicity of a porcine diarrheagenic Escherichia coli and to intestinal colonization through biofilm formation in pigs Vet. Microbiol. 120 2007 308 319
31. O. Sherlock, M.A. Schembri, A. Reisner, and P. Klemm Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation J. Bacteriol. 186 2004 8058 8065
32. O. Sherlock, U. Dobrindt, J.B. Jensen, R. Munk Vejborg, and P. Klemm Glycosylation of the self-recognizing Escherichia coli Ag43 autotransporter protein J. Bacteriol. 188 2006 1798 1807
33. C.M. Szymanski, and B.W. Wren Protein glycosylation in bacterial mucosal pathogens Nat. Rev. Microbiol. 3 2005 225 237
34. M.W. van der Woude, and I.R. Henderson Regulation and function of Ag43 (flu) Annu. Rev. Microbiol. 62 2008 153 169
35. T.J. Wells, J.J. Tree, G.C. Ulett, and M.A. Schembri Autotransporter proteins: novel targets at the bacterial cell surface FEMS Microbiol. Lett. 274 2007 163 172
36. T.J. Wells, M. Totsika, and M.A. Schembri Autotransporters of Escherichia coli: a sequence-based characterization Microbiology 156 2010 2459 2469
37. S.E. Wiley, A.N. Murphy, S.A. Ross, P. van der Geer, and J.E. Dixon MitoNEET is an iron-containing outer mitochondrial membrane protein that regulates oxidative capacity Proc. Natl. Acad. Sci. USA 104 2007 5318 5323
38. A. Zamyatina, S. Gronow, M. Puchberger, A. Graziani, A. Hofinger, and P. Kosma Efficient chemical synthesis of both anomers of ADP L-glycero- and D-glycero-D-manno-heptopyranose Carbohydr. Res. 338 2003 2571 2589
39. L. Zhao, X. Chen, X. Xu, G. Song, and X. Liu Analysis of the AIDA-I gene sequence and prevalence in Escherichia coli isolates from pigs with post-weaning diarrhoea and oedema disease Vet. J. 180 2009 124 129