The inverse autotransporter family: Intimin, invasin and related proteins

International Journal of Medical Microbiology

Volumn 305, Issue 2, 2015, Pages 276-282

  Leo, Jack C ^a   Oberhettinger, Philipp ^b   Schütz, Monika ^b   Linke, Dirk ^a,c  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Autotransport; Bacterial adhesion; Intimin; Invasin; Type Ve secretion

Indexed keywords

CHAPERONE; DIMER; INTIMIN; INVASIN; SIGNAL PEPTIDE; VIRULENCE FACTOR; ADHESIN; CARRIER PROTEIN; EAEA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; INVASIN, YERSINIA;

AMINO TERMINAL SEQUENCE; BACTERIAL GENOME; BACTERIAL OUTER MEMBRANE; BACTERIUM ADHERENCE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DIMERIZATION; GRAM NEGATIVE BACTERIUM; INVERSE AUTOTRANSPORTER SECRETION SYSTEM; NONHUMAN; PROTEIN DOMAIN; PROTEIN FOLDING; SHORT SURVEY; TYPE V SECRETION SYSTEM; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ADHESINS, BACTERIAL; ESCHERICHIA COLI PROTEINS; GRAM-NEGATIVE BACTERIA; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; VIRULENCE FACTORS;

EID: 84977778125     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.12.011     Document Type: Short Survey

References (71)

1. Adams T.M., Wentzel A., Kolmar H. Intimin-mediated export of passenger proteins requires maintenance of a translocation-competent conformation. J. Bacteriol. 2005, 187:522-533. 10.1128/JB.187.2.522-533.2005.
2. Adu-Bobie J., Frankel G., Bain C., Goncalves A.G., Trabulsi L.R., Douce G., Knutton S., Dougan G. Detection of intimins α, β, γ, and δ, four intimin derivatives expressed by attaching and effacing microbial pathogens. J. Clin. Microbiol. 1998, 36:662-668.
3. Albrecht R., Schütz M., Oberhettinger P., Faulstich M., Bermejo I., Rudel T., Diederichs K., Zeth K. Structure of BamA, an essential factor in outer membrane protein biogenesis. Acta Crystallogr. D Biol. Crystallogr. 2014, 70:1779-1789. 10.1107/S1399004714007482.
4. Bodelón G., Marín E., Fernández L.A. Role of periplasmic chaperones and BamA (YaeT/Omp85) in folding and secretion of intimin from enteropathogenic Escherichia coli strains. J. Bacteriol. 2009, 191:5169-5179. 10.1128/JB 00458-09.
5. Buist G., Steen A., Kok J., Kuipers O. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 2008, 68:838-847. 10.1111/j.1365-2958.2008.06211.x.
6. Chandrapala D., Kim K., Choi Y., Senevirathne A., Kang D., Ryu S., Kim K. Putative Inv is essential for basolateral invasion of Caco-2 cells and acts synergistically with OmpA to affect in vitro and in vivo virulence of Cronobacter sakazakii ATCC 29544. Infect. Immun. 2014, 82:1755-1765. 10.1128/IAI 01397-13.
7. Dersch P., Isberg R.R. A region of the Yersinia pseudotuberculosis invasin protein enhances integrin-mediated uptake into mammalian cells and promotes self-association. EMBO J. 1999, 18:1199-1213. 10.1093/emboj/18.5.1199.
8. Dersch P., Isberg R.R. An immunoglobulin superfamily-like domain unique to the Yersinia pseudotuberculosis invasin protein is required for stimulation of bacterial uptake via integrin receptors. Infect. Immun. 2000, 68:2930-2938.
9. Fairman J.W., Dautin N., Wojtowicz D., Liu W., Noinaj N., Barnard T.J., Udho E., Przytycka T.M., Cherezov V., Buchanan S.K. Crystal structures of the outer membrane domain of intimin and invasin from enterohemorrhagic E. coli and enteropathogenic Y. pseudotuberculosis. Structure 2012, 20:1233-1243. 10.1016/j.str.2012.04.011.
10. Frankel G., Lider O., Hershkoviz R., Mould A.P., Kachalsky S.G., Candy D.C., Cahalon L., Humphries M.J., Dougan G. The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J. Biol. Chem. 1996, 271:20359-20364.
11. Gal-Mor O., Gibson D.L., Baluta D., Vallance B.A., Finlay B.B. A novel secretion pathway of Salmonella enterica acts as an antivirulence modulator during salmonellosis. PLoS Pathog. 2008, 4:e1000036. 10.1371/journal.ppat.1000036.
12. Grosskinsky U., Schütz M., Fritz M., Schmid Y., Lamparter M.C., Szczesny P., Lupas A.N., Autenrieth I.B., Linke D. A conserved glycine residue of trimeric autotransporter domains plays a key role in Yersinia adhesin A autotransport. J. Bacteriol. 2007, 189:9011-9019. 10.1128/JB 00985-07.
13. Gruss F., Zähringer F., Jakob R.P., Burmann B.M., Hiller S., Maier T. The structural basis of autotransporter translocation by TamA. Nat. Struct. Mol. Biol. 2013, 20:1318-1320. 10.1038/nsmb.2689.
14. Guérin J., Baud C., Touati N., Saint Nathalie, Willery E., Locht C., Vezin H., Jacob-Dubuisson F. Conformational dynamics of protein transporter FhaC: large-scale motions of plug helix. Mol. Microbiol. 2014, 92:1164-1176. 10.1111/mmi.12585.
15. Hamburger Z.A., Brown M.S., Isberg R.R., Bjorkman P.J. Crystal structure of invasin: a bacterial integrin-binding protein. Science (New York, NY) 1999, 286:291-295.
16. Henderson I.R., Navarro-Garcia F., Desvaux M., Fernandez R.C., Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 2004, 68:692-744. 10.1128/MMBR.68.4.692-744.2004.
17. Ieva R., Bernstein H.D. Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19120-19125. 10.1073/pnas.0907912106.
18. Ieva R., Skillman K.M., Bernstein H.D. Incorporation of a polypeptide segment into the β-domain pore during the assembly of a bacterial autotransporter. Mol. Microbiol. 2008, 67:188-201. 10.1111/j.1365-2958.2007.06048.x.
19. Ieva R., Tian P., Peterson J., Bernstein H.D. Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:E383-E391. 10.1073/pnas.1103827108.
20. Isberg R.R., Leong J.M. Multiple beta1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 1990, 60:861-871.
21. Isberg R.R., Voorhis D.L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 1987, 50:769-778.
22. Jacob-Dubuisson F., Guérin J., Baelen S., Clantin B. Two-partner secretion: as simple as it sounds?. Res. Microbiol. 2013, 164:583-595. 10.1016/j.resmic.2013.03.009.
23. Jain S., Goldberg M.B. Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J. Bacteriol. 2007, 189:5393-5398. 10.1128/JB.00228-07.
24. 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. U.S.A. 1990, 87:7839-7843.
25. Jose J. Autodisplay: efficient bacterial surface display of recombinant proteins. Appl. Microbiol. Biotechnol. 2006, 69:607-614. 10.1007/s00253-005-0227-z.
26. Jose J., Meyer T. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol. Mol. Biol. Rev. 2007, 71:600-619. 10.1128/MMBR 00011-07.
27. Junker M., Schuster C.C., McDonnell A.V., Sorg K.A., Finn M.C., Berger B., Clark P.L. Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4918-4923. 10.1073/pnas.0507923103.
28. Junker M., Besingi R.N., Clark P.L. Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol. Microbiol. 2009, 71:1323-1332. 10.1111/j.1365-2958.2009.06607.x.
29. 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. 1999, 6:313-318. 10.1038/7545.
30. Kingsley R., Humphries A., Weening E., Zoete M., Winter S., Papaconstantinopoulou A., Dougan G., Bäumler A. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect. Immun. 2003, 71:629-640.
31. Klauser T., Pohlner J., Meyer T.F. The secretion pathway of IgA protease-type proteins in gram-negative bacteria. BioEssays 1993, 15:799-805. 10.1002/bies.950151205.
32. Lehr U., Schütz M., Oberhettinger P., Ruiz-Perez F., Donald J.W., Palmer T., Linke D., Henderson I.R., Autenrieth I.B. C-terminal amino acid residues of the trimeric autotransporter adhesin YadA of Yersinia enterocolitica are decisive for its recognition and assembly by BamA. Mol. Microbiol. 2010, 78:932-946. 10.1111/j.1365-2958.2010.07377.x.
33. Leo J.C., Grin I., Linke D. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2012, 367:1088-1101. 10.1098/rstb.2011.0208.
34. Leo J.C., Skurnik M. Adhesins of human pathogens from the genus Yersinia. Adv. Exp. Med. Biol. 2011, 715:1-15. 10.1007/978-94-007-0940-9_1.
35. Leyton D., Sevastsyanovich Y., Browning D., Rossiter A., Wells T., Fitzpatrick R., Overduin M., Cunningham A., Henderson I. Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins. J. Biol. Chem. 2011, 286:42283-42291. 10.1074/jbc.M111.306118.
36. Leyton D., de Luna M., Sevastsyanovich Y., Jensen K., Browning D., Scott-Tucker A., Henderson I. The unusual extended signal peptide region is not required for secretion and function of an Escherichia coli autotransporter. FEMS Microbiol. Lett. 2010, 311:133-139. 10.1111/j.1574-6968.2010.02081.x.
37. Li M., Hu Y., Zheng W., Sun B., Wang C., Sun L. Inv1: an Edwardsiella tarda invasin and a protective immunogen that is required for host infection. Fish Shellfish Immunol. 2012, 32:586-592. 10.1016/j.fsi.2012.01.016.
38. Linke D., Riess T., Autenrieth I.B., Lupas A., Kempf V.A. Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 2006, 14:264-270. 10.1016/j.tim.2006.04.005.
39. Liu H., Magoun L., Leong J.M. beta1-chain integrins are not essential for intimin-mediated host cell attachment and enteropathogenic Escherichia coli-induced actin condensation. Infect. Immun. 1999, 67:2045-2049.
40. 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 2000, 405:1073-1077. 10.1038/35016618.
41. Mallick E.M., Brady M.J., Luperchio S.A., Vanguri V.K., Magoun L., Liu H., Sheppard B.J., Mukherjee J., Donohue-Rolfe A., Tzipori S., Leong J.M., Schauer D.B. Allele- and Tir-independent functions of intimin in diverse animal infection models. Front. Microbiol. 2012, 3:11. 10.3389/fmicb.2012.00011.
42. Marchès O., Nougayrède J.P., Boullier S., Mainil J., Charlier G., Raymond I., Pohl P., Boury M., de Rycke J., Milon A., Oswald E. Role of tir and intimin in the virulence of rabbit enteropathogenic Escherichia coli serotype O103:H2. Infect. Immun. 2000, 68:2171-2182.
43. McKee M.L., Melton-Celsa A.R., Moxley R.A., Francis D.H., O'Brien A.D. Enterohemorrhagic Escherichia coli O157:H7 requires intimin to colonize the gnotobiotic pig intestine and to adhere to HEp-2 cells. Infect. Immun. 1995, 63:3739-3744.
44. Nesta B., Spraggon G., Alteri C., Moriel D.G., Rosini R., Veggi D., Smith S., Bertoldi I., Pastorello I., Ferlenghi I., Fontana M.R., Frankel G., Mobley H.L., Rappuoli R., Pizza M., Serino L., Soriani M. FdeC, a novel broadly conserved Escherichia coli adhesin eliciting protection against urinary tract infections. mBio 2012, 3:1-10. 10.1128/mBio.00010-12.
45. Newman C., Stathopoulos C. Autotransporter and two-partner secretion: delivery of large-size virulence factors by gram-negative bacterial pathogens. Crit. Rev. Microbiol. 2004, 30:275-286. 10.1080/10408410490499872.
46. Noinaj N., Kuszak A.J., Balusek C., Gumbart J.C., Buchanan S.K. Lateral opening and exit pore formation are required for BamA function. Structure 2014, 22:1055-1062. 10.1016/j.str.2014.05.008.
47. Noinaj N., Kuszak A.J., Gumbart J.C., Lukacik P., Chang H., Easley N.C., Lithgow T., Buchanan S.K. Structural insight into the biogenesis of β-barrel membrane proteins. Nature 2013, 501:385-390. 10.1038/nature12521.
48. Oberhettinger P., Schütz M., Leo J.C., Heinz N., Berger J., Autenrieth I.B., Linke D. Intimin and invasin export their C-terminus to the bacterial cell surface using an inverse mechanism compared to classical autotransport. PLoS ONE 2012, 7:e47069. 10.1371/journal.pone.0047069.
49. Oswald E., Schmidt H., Morabito S., Karch H., Marchès O., Caprioli A. Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect. Immun. 2000, 68:64-71.
50. Pepe J., Badger J., Miller V. Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene. Mol. Microbiol. 1994, 11:123-135.
51. Peterson J., Tian P., Ieva R., Dautin N., Bernstein H.D. Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17739-17744. 10.1073/pnas.1009491107.
52. Pisano F., Kochut A., Uliczka F., Geyer R., Stolz T., Thiermann T., Rohde M., Dersch P. In vivo-induced InvA-like autotransporters Ifp and InvC of Yersinia pseudotuberculosis promote interactions with intestinal epithelial cells and contribute to virulence. Infect. Immun. 2012, 80:1050-1064. 10.1128/IAI 05715-11.
53. Pohlner J., Halter R., Beyreuther K., Meyer T.F., Beyreuther T.F.K. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 1987, 325:458-462. 10.1038/325458a0.
54. Prehna G., Li Y., Stoynov N., Okon M., Vuckovic M., McIntosh L.P., Foster L.J., Finlay B.B., Strynadka N.C. The zinc regulated antivirulence pathway of Salmonella is a multiprotein immunoglobulin adhesion system. J. Biol. Chem. 2012, 287:32324-32337. 10.1074/jbc.M112.357210.
55. Remmert M., Biegert A., Linke D., Lupas A.N., Söding J. Evolution of outer membrane β-barrels from an ancestral ββ hairpin. Mol. Biol. Evol. 2010, 27:1348-1358. 10.1093/molbev/msq017.
56. Roman-Hernandez G., Peterson J.H., Bernstein H.D. Reconstitution of bacterial autotransporter assembly using purified components. eLife 2014, e04234. 10.7554/eLife.04234.
57. Ruiz-Perez F., Henderson I.R., Leyton D.L., Rossiter A.E., Zhang Y., Nataro J.P. Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J. Bacteriol. 2009, 191:6571-6583. 10.1128/JB 00754-09.
58. Ruiz-Perez Fernando, Henderson Ian R., Nataro James P. Interaction of FkpA, a peptidyl-prolyl cis/trans isomerase with EspP autotransporter protein. Gut Microbes 2010, 1:339-344. 10.4161/gmic.1.5.13436.
59. Salacha R., Kovacić F., Brochier-Armanet C., Wilhelm S., Tommassen J., Filloux A., Voulhoux R., Bleves S. The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel Type V secretion system. Environ. Microbiol. 2010, 12:1498-1512. 10.1111/j.1462-2920.2010.02174.x.
60. Salema V., Marín E., Martínez-Arteaga R., Ruano-Gallego D., Fraile S., Margolles Y., Teira X., Gutierrez C., Bodelón G., Fernández L.Á. Selection of single domain antibodies from immune libraries displayed on the surface of E. coli cells with two β-domains of opposite topologies. PLoS ONE 2013, 8:e75126. 10.1371/journal.pone.0075126.
61. Sauri A., Soprova Z., Wickström D., de Gier J., van der Schors R.C., Smit A.B., Jong W.S.P., Luirink J. The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology (Reading, England) 2009, 155:3982-3991. 10.1099/mic.0.034991-0.
62. Schmidt M.A. LEEways: tales of EPEC ATEC and EHEC. Cell. Microbiol. 2010, 12:1544-1552. 10.1111/j.1462-5822.2010.01518.x.
63. Selkrig J., Mosbahi K., Webb C.T., Belousoff M.J., Perry A.J., Wells T.J., Morris F., Leyton D.L., Totsika M., Phan M., Celik N., Kelly M., Oates C., Hartland E.L., Robins-Browne R.M., Ramarathinam S.H., Purcell A.W., Schembri M.A., Strugnell R.A., Henderson I.R., Walker D., Lithgow T. Discovery of an archetypal protein transport system in bacterial outer membranes. Nat. Struct. Mol. Biol. 2012, 19(S1):506-510. 10.1038/nsmb.2261.
64. Seo K.S., Kim J.W., Park J.Y., Viall A.K., Minnich S.S., Rohde H.N., Schnider D.R., Lim S.Y., Hong J.B., Hinnebusch B.J., O'Loughlin J.L., Deobald C.F., Bohach G.A., Hovde C.J., Minnich S.A. Role of a new intimin/invasin-like protein in Yersinia pestis virulence. Infect. Immun. 2012, 80:3559-3569. 10.1128/IAI 00294-12.
65. Shahid S.A., Bardiaux B., Franks W.T., Krabben L., Habeck M., van Rossum B., Linke D. Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nat. Methods 2012, 9:1212-1217. 10.1038/nmeth.2248.
66. Sinclair J.F., O'Brien A.D. Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-γ of enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem. 2002, 277:2876-2885. 10.1074/jbc.M110230200.
67. Strong P., Hinchliffe S., Patrick H., Atkinson S., Champion O., Wren B. Identification and characterisation of a novel adhesin Ifp in Yersinia pseudotuberculosis. BMC Microbiol. 2011, 11:85. 10.1186/1471-2180-11-85.
68. Szabady R.L., Peterson J.H., Skillman K.M., Bernstein H.D. An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:221-226. 10.1073/pnas.0406055102.
69. Touzé T., Hayward R.D., Eswaran J., Leong J.M., Koronakis V. Self-association of EPEC intimin mediated by the β-barrel-containing anchor domain: a role in clustering of the Tir receptor. Mol. Microbiol. 2004, 51:73-87.
70. Tsai J.C., Yen M., Castillo R., Leyton D.L., Henderson I.R., Saier M.H. The bacterial intimins and invasins: a large and novel family of secreted proteins. PLoS ONE 2010, 5:e14403-e14414. 10.1371/journal.pone.0014403.
71. Wentzel A., Christmann A., Adams T., Kolmar H. Display of passenger proteins on the surface of Escherichia coli K-12 by the enterohemorrhagic E. coli intimin EaeA. J. Bacteriol. 2001, 183:7273-7284. 10.1128/JB.183.24.7273-7284.2001.