Adhesins and invasins of pathogenic bacteria: A structural view

Microbes and Infection

Volumn 6, Issue 1, 2004, Pages 101-112

  Niemann, Hartmut H ^a   Schubert, Wolf Dieter ^a   Heinz, Dirk W ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Adhesins; Crystal structure; Invasins; Pathogenic bacteria; Solution structure; Virulence factors

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; CADHERIN; CELL RECEPTOR; FIBRONECTIN; GLYCOSAMINOGLYCAN; HEPARIN; INTERNALIN A; INTERNALIN B; INTIMIN; INVASIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; PERTACTIN; UNCLASSIFIED DRUG;

BACTERIAL INFECTION; BACTERIUM; BACTERIUM ADHERENCE; BACTERIUM PILUS; BORDETELLA PERTUSSIS; COMPLEX FORMATION; ESCHERICHIA COLI; EUKARYOTE; HOST CELL; LISTERIA MONOCYTOGENES; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 1642493657     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micinf.2003.11.001     Document Type: Short Survey

References (94)

1. Gaillard J.L., Berche P., Frehel C., Gouin E., Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 65:1991;1127-1141.
2. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol. Microbiol. 16:1995;251-261.
3. Parida S.K., Domann E., Rohde M., Muller S., Darji A., Hain T., Wehland J., Chakraborty T. Internalin B is essential for adhesion and mediates the invasion of Listeria monocytogenes into human endothelial cells. Mol. Microbiol. 28:1998;81-93.
4. Pandiripally V.K., Westbrook D.G., Sunki G.R., Bhunia A.K. Surface protein p104 is involved in adhesion of Listeria monocytogenes to human intestinal cell line, Caco-2. J. Med. Microbiol. 48:1999;117-124.
5. Milohanic E., Jonquieres R., Cossart P., Berche P., Gaillard J.L. The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol. Microbiol. 39:2001;1212-1224.
6. Lecuit M., Ohayon H., Braun L., Mengaud J., Cossart P. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect. Immun. 65:1997;5309-5319.
7. Lecuit M., Vandormael-Pournin S., Lefort J., Huerre M., Gounon P., Dupuy C., Babinet C., Cossart P. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science. 292:2001;1722-1725.
8. Mengaud J., Ohayon H., Gounon P., Mege R.M., Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell. 84:1996;923-932.
9. Lingnau A., Domann E., Hudel M., Bock M., Nichterlein T., Wehland J., Chakraborty T. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. Infect. Immun. 63:1995;3896-3903.
10. Garandeau C., Reglier-Poupet H., Dubail I., Beretti J.L., Berche P., Charbit A. The sortase SrtA of Listeria monocytogenes is involved in processing of internalin and in virulence. Infect. Immun. 70:2002;1382-1390.
11. Bierne H., Mazmanian S.K., Trost M., Pucciarelli M.G., Liu G., Dehoux P., Jansch L., Garcia-del Portillo F., Schneewind O., Cossart P. Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence. Mol. Microbiol. 43:2002;869-881.
12. Marino M., Braun L., Cossart P., Ghosh P. Structure of the lnlB leucine-rich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes. Mol. Cell. 4:1999;1063-1072.
13. Schubert W.D., Gobel G., Diepholz M., Darji A., Kloer D., Hain T., Chakraborty T., Wehland J., Domann E., Heinz D.W. Internalins from the human pathogen Listeria monocytogenes combine three distinct folds into a contiguous internalin domain. J. Mol. Biol. 312:2001;783-794.
14. Marino M., Banerjee M., Jonquieres R., Cossart P., Ghosh P. GW domains of the Listeria monocytogenes invasion protein InlB are SH3-like and mediate binding to host ligands. EMBO J. 21:2002;5623-5634.
15. Schubert W.D., Urbanke C., Ziehm T., Beier V., Machner M.P., Domann E., Wehland J., Chakraborty T., Heinz D.W. Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell. 111:2002;825-836.
16. Schubert W.D., Heinz D.W. Structural aspects of adhesion and invasion of host cells by the human pathogen Listeria monocytogenes. Chem. Biochem. 4:2003;1285-1291.
17. Angst B.D., Marcozzi C., Magee A.I. The cadherin superfamily. J. Cell Sci. 114:2001;625-626.
18. Huber A.H., Weis W.I. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell. 105:2001;391-402.
19. Lecuit M., Dramsi S., Gottardi C., Fedor-Chaiken M., Gumbiner B., Cossart P. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18:1999;3956-3963.
20. Kobe B., Kajava A.V. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11:2001;725-732.
21. Braun L., Nato F., Payrastre B., Mazie J.C., Cossart P. The 213-amino-acid leucine-rich repeat region of the Listeria monocytogenes InlB protein is sufficient for entry into mammalian cells, stimulation of PI 3-kinase and membrane ruffling. Mol. Microbiol. 34:1999;10-23.
22. Machner M.P., Frese S., Schubert W.D., Orian-Rousseau V., Gherardi E., Wehland J., Niemann H.H., Heinz D.W. Aromatic amino acids at the surface of InlB are essential for host cell invasion by Listeria monocytogenes. Mol. Microbiol. 48:2003;1525-1536.
23. Ireton K., Payrastre B., Cossart P. The Listeria monocytogenes protein InlB is an agonist of mammalian phosphoinositide 3-kinase. J. Biol. Chem. 274:1999;17025-17032.
24. Fruman D.A., Meyers R.E., Cantley L.C. Phosphoinositide kinases. Annu. Rev. Biochem. 67:1998;481-507.
25. Shen Y., Naujokas M., Park M., Ireton K. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell. 103:2000;501-510.
26. Birchmeier C., Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8:1998;404-410.
27. Braun L., Dramsi S., Dehoux P., Bierne H., Lindahl G., Cossart P. InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol. Microbiol. 25:1997;285-294.
28. Jonquieres R., Bierne H., Fiedler F., Gounon P., Cossart P. Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of gram-positive bacteria. Mol. Microbiol. 34:1999;902-914.
29. Braun L., Ghebrehiwet B., Cossart P. gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J. 19:2000;1458-1466.
30. Jonquieres R., Pizarro-Cerda J., Cossart P. Synergy between the N- and C-terminal domains of InlB for efficient invasion of non-phagocytic cells by Listeria monocytogenes. Mol. Microbiol. 42:2001;955-965.
31. Ghebrehiwet B., Lim B.L., Kumar R., Feng X., Peerschke E.I. gC1q-R/p33, a member of a new class of multifunctional and multicompartmental cellular proteins, is involved in inflammation and infection. Immunol. Rev. 180:2001;65-77.
32. Jiang J., Zhang Y., Krainer A.R., Xu R.M. Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc. Natl. Acad. Sci. USA. 96:1999;3572-3577.
33. Copp J., Marino M., Banerjee M., Ghosh P., van der Geer P. Multiple regions of internalin B contribute to its ability to turn on the Ras-mitogen-activated protein kinase pathway. J. Biol. Chem. 278:2003;7783-7789.
34. Isberg R.R., Voorhis D.L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 50:1987;769-778.
35. Isberg R.R., Leong J.M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 60:1990;861-871.
36. Hamburger Z.A., Brown M.S., Isberg R.R., Bjorkman P.J. Crystal structure of invasin: a bacterial integrin-binding protein. Science. 286:1999;291-295.
37. Kogelberg H., Feizi T. New structural insights into lectin-type proteins of the immune system. Curr. Opin. Struct. Biol. 11:2001;635-643.
38. Leong J.M., Fournier R.S., Isberg R.R. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBO J. 9:1990;1979-1989.
39. Rankin S., Isberg R.R., Leong J.M. The integrin-binding domain of invasin is sufficient to allow bacterial entry into mammalian cells. Infect. Immun. 60:1992;3909-3912.
40. Pierschbacher M.D., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 309:1984;30-33.
41. Aota S., Nomizu M., Yamada K.M. The short amino acid sequence Pro-His-Ser-Arg-Asn in human fibronectin enhances cell-adhesive function. J. Biol. Chem. 269:1994;24756-24761.
42. Bowditch R.D., Hariharan M., Tominna E.F., Smith J.W., Yamada K.M., Getzoff E.D., Ginsberg M.H. Identification of a novel integrin binding site in fibronectin. Differential utilization by beta 3 integrins. J. Biol. Chem. 269:1994;10856-10863.
43. Leong J.M., Morrissey P.E., Marra A., Isberg R.R. An aspartate residue of the Yersinia pseudotuberculosis invasin protein that is critical for integrin binding. EMBO J. 14:1995;422-431.
44. Saltman L.H., Lu Y., Zaharias E.M., Isberg R.R. A region of the Yersinia pseudotuberculosis invasin protein that contributes to high affinity binding to integrin receptors. J. Biol. Chem. 271:1996;23438-23444.
45. Leahy D.J., Aukhil I., Erickson H.P. 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell. 84:1996;155-164.
46. Kenny B. Mechanism of action of EPEC type III effector molecules. Int. J. Med. Microbiol. 291:2002;469-477.
47. Jerse A.E., Yu J., Tall B.D., Kaper J.B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. USA. 87:1990;7839-7843.
48. Donnenberg M.S., Tacket C.O., James S.P., Losonsky G., Nataro J.P., Wasserman S.S., Kaper J.B., Levine M.M. Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J. Clin. Invest. 92:1993;1412-1417.
49. Kenny B., DeVinney R., Stein M., Reinscheid D.J., Frey E.A., Finlay B.B. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 91:1997;511-520.
50. Kelly G., Prasannan S., Daniell S., Fleming K., Frankel G., Dougan G., Connerton I., Matthews S. Structure of the cell-adhesion fragment of intimin from enteropathogenic Escherichia coli. Nat. Struct. Biol. 6:1999;313-318.
51. Luo Y., Frey E.A., Pfuetzner R.A., Creagh A.L., Knoechel D.G., Haynes C.A., Finlay B.B., Strynadka N.C. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature. 405:2000;1073-1077.
52. Batchelor M., Prasannan S., Daniell S., Reece S., Connerton I., Bloomberg G., Dougan G., Frankel G., Matthews S. Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli. EMBO J. 19:2000;2452-2464.
53. Smith A.M., Guzman C.A., Walker M.J. The virulence factors of Bordetella pertussis: a matter of control. FEMS Microbiol. Rev. 25:2001;309-333.
54. Leininger E., Roberts M., Kenimer J.G., Charles I.G., Fairweather N., Novotny P., Brennan M.J. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl. Acad. Sci. USA. 88:1991;345-349.
55. Henderson I.R., Nataro J.P. Virulence functions of autotransporter proteins. Infect. Immun. 69:2001;1231-1243.
56. Charles I., Fairweather N., Pickard D., Beesley J., Anderson R., Dougan G., Roberts M. Expression of the Bordetella pertussis P.69 pertactin adhesin in Escherichia coli: fate of the carboxy-terminal domain. Microbiology. 140:1994;3301-3308.
57. Emsley P., Charles I.G., Fairweather N.F., Isaacs N.W. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature. 381:1996;90-92.
58. Jenkins J., Pickersgill R. The architecture of parallel beta-helices and related folds. Prog. Biophys. Mol. Biol. 77:2001;111-175.
59. Everest P., Li J., Douce G., Charles I., De Azavedo J., Chatfield S., Dougan G., Roberts M. Role of the Bordetella pertussis P.69/pertactin protein and the P.69/pertactin RGD motif in the adherence to and invasion of mammalian cells. Microbiology. 142:1996;3261-3268.
60. van den Berg B.M., Beekhuizen H., Willems R.J., Mooi F.R., van Furth R. Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect. Immun. 67:1999;1056-1062.
61. Bassinet L., Gueirard P., Maitre B., Housset B., Gounon P., Guiso N. Role of adhesins and toxins in invasion of human tracheal epithelial cells by Bordetella pertussis. Infect. Immun. 68:2000;1934-1941.
62. Mulvey M.A. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol. 4:2002;257-271.
63. Soto G.E., Hultgren S.J. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 181:1999;1059-1071.
64. Sauer F.G., Barnhart M., Choudhury D., Knight S.D., Waksman G., Hultgren S.J. Chaperone-assisted pilus assembly and bacterial attachment. Curr. Opin. Struct. Biol. 10:2000;548-556.
65. Abraham S.N., Sun D., Dale J.B., Beachey E.H. Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature. 336:1988;682-684.
66. Krogfelt K.A., Bergmans H., Klemm P. Direct evidence that the FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae. Infect. Immun. 58:1990;1995-1998.
67. Choudhury D., Thompson A., Stojanoff V., Langermann S., Pinkner J., Hultgren S.J., Knight S.D. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science. 285:1999;1061-1066.
68. Hung C.S., Bouckaert J., Hung D., Pinkner J., Widberg C., DeFusco A., Auguste C.G., Strouse R., Langermann S., Waksman G., Hultgren S.J. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 44:2002;903-915.
69. Lund B., Lindberg F., Marklund B.I., Normark S. The PapG protein is the alpha-D-galactopyranosyl-(1-4)-beta-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA. 84:1987;5898-5902.
70. Dodson K.W., Pinkner J.S., Rose T., Magnusson G., Hultgren S.J., Waksman G. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell. 105:2001;733-743.
71. Sung M.A., Fleming K., Chen H.A., Matthews S. The solution structure of PapGII from uropathogenic Escherichia coli and its recognition of glycolipid receptors. EMBO Rep. 2:2001;621-627.
72. Flock J.I., Froman G., Jonsson K., Guss B., Signas C., Nilsson B., Raucci G., Hook M., Wadstrom T., Lindberg M. Cloning and expression of the gene for a fibronectin-binding protein from Staphylococcus aureus. EMBO J. 6:1987;2351-2357.
73. Dziewanowska K., Patti J.M., Deobald C.F., Bayles K.W., Trumble W.R., Bohach G.A. Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect. Immun. 67:1999;4673-4678.
74. Talay S.R., Valentin-Weigand P., Jerlstrom P.G., Timmis K.N., Chhatwal G.S. Fibronectin-binding protein of Streptococcus pyogenes: sequence of the binding domain involved in adherence of streptococci to epithelial cells. Infect. Immun. 60:1992;3837-3844.
75. Molinari G., Talay S.R., Valentin-Weigand P., Rohde M., Chhatwal G.S. The fibronectin-binding protein of Streptococcus pyogenes, SfbI, is involved in the internalization of group A streptococci by epithelial cells. Infect. Immun. 65:1997;1357-1363.
76. Schwarz-Linek U., Werner J.M., Pickford A.R., Gurusiddappa S., Kim J.H., Pilka E.S., Briggs J.A., Gough T.S., Hook M., Campbell I.D., Potts J.R. Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature. 423:2003;177-181.
77. Kim K.S. E. coli invasion of brain microvascular endothelial cells as a pathogenetic basis of meningitis. Subcell Biochem. 33:2000;47-59.
78. Prasadarao N.V., Wass C.A., Weiser J.N., Stins M.F., Huang S.H., Kim K.S. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect. Immun. 64:1996;146-153.
79. Prasadarao N.V., Wass C.A., Stins M.F., Shimada H., Kim K.S. Outer membrane protein A-promoted actin condensation of brain microvascular endothelial cells is required for Escherichia coli invasion. Infect. Immun. 67:1999;5775-5783.
80. Prasadarao N.V. Identification of Escherichia coli outer membrane protein A receptor on human brain microvascular endothelial cells. Infect. Immun. 70:2002;4556-4563.
81. Prasadarao N.V., Srivastava P.K., Rudrabhatla R.S., Kim K.S., Huang S.H., Sukumaran S.K. Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infect. Immun. 71:2003;1680-1688.
82. Mecsas J., Welch R., Erickson J.W., Gross C.A. Identification and characterization of an outer membrane protein, OmpX, in Escherichia coli that is homologous to a family of outer membrane proteins including Ail of Yersinia enterocolitica. J. Bacteriol. 177:1995;799-804.
83. de Kort G., Bolton A., Martin G., Stephen J., van de Klundert J.A. Invasion of rabbit ileal tissue by Enterobacter cloacae varies with the concentration of OmpX in the outer membrane. Infect. Immun. 62:1994;4722-4726.
84. Miller V.L., Falkow S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect. Immun. 56:1988;1242-1248.
85. Pautsch A., Schulz G.E. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5:1998;1013-1017.
86. Vogt J., Schulz G.E. The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Struct. Fold. Des. 7:1999;1301-1309.
87. Virji M., Makepeace K., Ferguson D.J., Achtman M., Sarkari J., Moxon E.R. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol. Microbiol. 6:1992;2785-2795.
88. Virji M., Makepeace K., Ferguson D.J., Achtman M., Moxon E.R. Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 10:1993;499-510.
89. de Vries F.P., Cole R., Dankert J., Frosch M., van Putten J.P. Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 27:1998;1203-1212.
90. Prince S.M., Achtman M., Derrick J.P. Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA. 99:2002;3417-3421.
91. Teichmann S.A., Chothia C. Immunoglobulin superfamily proteins in Caenorhabditis elegans. J. Mol. Biol. 296:2000;1367-1383.
92. Kobe B., Deisenhofer J. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature. 374:1995;183-186.
93. Schulz G.E. The structure of bacterial outer membrane proteins. Biochim. Biophys. Acta. 1565:2002;308-317.
94. DeLano W.L. The PyMOL Molecular Graphics System, on World Wide Web. :2002