Characterization and functional analysis of AatB, a novel autotransporter adhesin and virulence factor of avian pathogenic Escherichia coli

Infection and Immunity

Volumn 81, Issue 7, 2013, Pages 2437-2447

  ZhuGe, Xiangkai ^a   Wang, Shaohui ^b   Fan, Hongjie ^a   Pan, Zihao ^a   Ren, Jianluan ^a   Yi, Li ^a   Meng, Qingmei ^a   Yang, Xuqiu ^a   Lu, Chengping ^a   Dai, Jianjun ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AUTOTRANSPORTER PROTEIN AATB; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBODY PRODUCTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; DELETION MUTANT; DUCK; ESCHERICHIA COLI; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LUNG INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ADHESINS, ESCHERICHIA COLI; ANIMALS; BACTERIAL ADHESION; BACTERIAL LOAD; BIOFILMS; DUCKS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; LUNG; OPEN READING FRAMES; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE DELETION; VIRULENCE FACTORS;

EID: 84879433340     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00102-13     Document Type: Article

References (58)

1. Krogfelt KA. 1991. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli. Rev. Infect. Dis. 13: 721-735.
2. Kline KA, Falker S, Dahlberg S, Normark S, Henriques-Normark B. 2009. Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5:580-592.
3. Yen YT, Stathopoulos C. 2007. Identification of autotransporter proteins secreted by type V secretion systems in gram-negative bacteria. Methods Mol. Biol. 390:33-46.
4. Henderson IR, Nataro JP. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:1231-1243.
5. Wells TJ, Tree JJ, Ulett GC, Schembri MA. 2007. Autotransporter proteins: novel targets at the bacterial cell surface. FEMS Microbiol. Lett. 274:163-172.
6. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
7. Linke D, Riess T, Autenrieth IB, Lupas A, Kempf VA. 2006. Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 14:264-270.
8. Lyskowski A, Leo JC, Goldman A. 2011. Structure and biology of trimeric autotransporter adhesins. Adv. Exp. Med. Biol. 715:143-158.
9. Cotter SE, Surana NK, St Geme JW, III. 2005. Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol. 13:199-205.
10. Raghunathan D, Wells TJ, Morris FC, Shaw RK, Bobat S, Peters SE, Paterson GK, Jensen KT, Leyton DL, Blair JM, Browning DF, Pravin J, Flores-Langarica A, Hitchcock JR, Moraes CT, Piazza RM, Maskell DJ, Webber MA, May RC, MacLennan CA, Piddock LJ, Cunningham AF, Henderson IR. 2011. SadA, a trimeric autotransporter from Salmonella enterica serovar Typhimurium, can promote biofilm formation and provides limited protection against infection. Infect. Immun. 79:4342-4352.
11. Scarselli M, Serruto D, Montanari P, Capecchi B, Adu-Bobie J, Veggi D, Rappuoli R, Pizza M, Arico B. 2006. Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Mol. Microbiol. 61: 631-644.
12. Leduc I, Olsen B, Elkins C. 2009. Localization of the domains of the Haemophilus ducreyi trimeric autotransporter DsrA involved in serum resistance and binding to the extracellular matrix proteins fibronectin and vitronectin. Infect. Immun. 77:657-666.
13. Sherlock O, Schembri MA, Reisner A, Klemm P. 2004. Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J. Bacteriol. 186:8058-8065.
14. Guyer DM, Henderson IR, Nataro JP, Mobley HL. 2000. Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol. Microbiol. 38:53-66.
15. Felek S, Lawrenz MB, Krukonis ES. 2008. The Yersinia pestis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology 154:1802-1812.
16. Leyton DL, Adams LM, Kelly M, Sloan J, Tauschek M, Robins-Browne RM, Hartland EL. 2007. Contribution of a novel gene, rpeA, encoding a putative autotransporter adhesin to intestinal colonization by rabbitspecific enteropathogenic Escherichia coli. Infect. Immun. 75:4664-4669.
17. Kjaergaard K, Hasman H, Schembri MA, Klemm P. 2002. Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. J. Bacteriol. 184:4197-4204.
18. Xiao L, Zhou L, Sun C, Feng X, Du C, Gao Y, Ji Q, Yang S, Wang Y, Han W, Langford PR, Lei L. 2011. Apa is a trimeric autotransporter adhesin of Actinobacillus pleuropneumoniae responsible for autoagglutination and host cell adherence. J. Basic Microbiol. 52:598-607.
19. Drago-Serrano ME, Parra SG, Manjarrez-Hernandez HA. 2006. EspC, an autotransporter protein secreted by enteropathogenic Escherichia coli (EPEC), displays protease activity on human hemoglobin. FEMS Microbiol. Lett. 265:35-40.
20. Guignot J, Chaplais C, Coconnier-Polter MH, Servin AL. 2007. The secreted autotransporter toxin, Sat, functions as a virulence factor in Afa/Dr diffusely adhering Escherichia coli by promoting lesions in tight junction of polarized epithelial cells. Cell. Microbiol. 9:204-221.
21. Wells TJ, Sherlock O, Rivas L, Mahajan A, Beatson SA, Torpdahl M, Webb RI, Allsopp LP, Gobius KS, Gally DL, Schembri MA. 2008. EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation. Environ. Microbiol. 10:589-604.
22. Li G, Feng Y, Kariyawasam S, Tivendale KA, Wannemuehler Y, Zhou F, Logue CM, Miller CL, Nolan LK. 2010. AatA is a novel autotransporter and virulence factor of avian pathogenic Escherichia coli. Infect. Immun. 78:898-906.
23. Dai J, Wang S, Guerlebeck D, Laturnus C, Guenther S, Shi Z, Lu C, Ewers C. 2010. Suppression subtractive hybridization identifies an autotransporter adhesin gene of E. coli IMT5155 specifically associated with avian pathogenic Escherichia coli (APEC). BMC Microbiol. 10:236. doi:10.1186/1471-2180-10-236.
24. Dozois CM, Dho-Moulin M, Bree A, Fairbrother JM, Desautels C, Curtiss R, III. 2000. Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the Tsh genetic region. Infect. Immun. 68:4145-4154.
25. Parreira VR, Gyles CL. 2003. A novel pathogenicity island integrated adjacent to the thrW tRNA gene of avian pathogenic Escherichia coli encodes a vacuolating autotransporter toxin. Infect. Immun. 71:5087-5096.
26. Stathopoulos C, Provence DL, Curtiss R, III. 1999. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect. Immun. 67:772-781.
27. Lehr U, Schutz M, Oberhettinger P, Ruiz-Perez F, Donald JW, Palmer T, Linke D, Henderson IR, Autenrieth IB. 2010. 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. 78:932-946.
28. Ackermann N, Tiller M, Anding G, Roggenkamp A, Heesemann J. 2008. Contribution of trimeric autotransporter C-terminal domains of oligomeric coiled-coil adhesin (Oca) family members YadA, UspA1, EibA, and Hia to translocation of the YadA passenger domain and virulence of Yersinia enterocolitica. J. Bacteriol. 190:5031-5043.
29. Cotter SE, Yeo HJ, Juehne T, St Geme JW, III. 2005. Architecture and adhesive activity of the Haemophilus influenzae Hsf adhesin. J. Bacteriol. 187:4656-4664.
30. Meng G, St Geme JW, III, Waksman G. 2008. Repetitive architecture of the Haemophilus influenzae Hia trimeric autotransporter. J. Mol. Biol. 384:824-836.
31. Tavano R, Capecchi B, Montanari P, Franzoso S, Marin O, Sztukowska M, Cecchini P, Segat D, Scarselli M, Arico B, Papini E. 2011. Mapping of the Neisseria meningitidis NadA cell-binding site: relevance of predicted α-helices in the NH2-terminal and dimeric coiled-coil regions. J. Bacteriol. 193:107-115.
32. Paton AW, Srimanote P, Woodrow MC, Paton JC. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69:6999-7009.
33. Valle J, Mabbett AN, Ulett GC, Toledo-Arana A, Wecker K, Totsika M, Schembri MA, Ghigo JM, Beloin C. 2008. UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J. Bacteriol. 190:4147-4161.
34. Ewers C, Li G, Wilking H, Kiessling S, Alt K, Antao EM, Laturnus C, Diehl I, Glodde S, Homeier T, Bohnke U, Steinruck H, Philipp HC, Wieler LH. 2007. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int. J. Med. Microbiol. 297:163-176.
35. Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK. 2005. Characterizing the APEC pathotype. Vet. Res. 36:241-256.
36. Alamuri P, Lower M, Hiss JA, Himpsl SD, Schneider G, Mobley HL. 2010. Adhesion, invasion, and agglutination mediated by two trimeric autotransporters in the human uropathogen Proteus mirabilis. Infect. Immun. 78:4882-4894.
37. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:4555-4558.
38. Wang S, Niu C, Shi Z, Xia Y, Yaqoob M, Dai J, Lu C. 2011. Effects of ibeA deletion on virulence and biofilm formation of avian pathogenic Escherichia coli. Infect. Immun. 79:279-287.
39. Wang S, Xia Y, Dai J, Shi Z, Kou Y, Li H, Bao Y, Lu C. 2011. Novel roles for autotransporter adhesin AatA of avian pathogenic Escherichia coli: colonization during infection and cell aggregation. FEMS Immunol. Med. Microbiol. 63:328-338.
40. Wang S, Shi Z, Xia Y, Li H, Kou Y, Bao Y, Dai J, Lu C. 2012. IbeB is involved in the invasion and pathogenicity of avian pathogenic Escherichia coli. Vet. Microbiol. 159:411-419.
41. Davanloo P, Rosenberg AH, Dunn JJ, Studier FW. 1984. Cloning and expression of the gene for bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. U. S. A. 81:2035-2039.
42. Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189: 113-130.
43. Blomfield IC, McClain MS, Eisenstein BI. 1991. Type 1 fimbriae mutants of Escherichia coli K12: characterization of recognized afimbriate strains and construction of new fim deletion mutants. Mol. Microbiol. 5:1439- 1445.
44. Zhang Y. 2009. I-TASSER: fully automated protein structure prediction in CASP8. Proteins 77:100-113.
45. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. doi:10.1186/1471-2105-9-40.
46. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5:725- 738.
47. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
48. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
49. Fung KP, Wong TW. 1989. Estimation of quantal dose response of drugs by the Spearman-Karber method: a computer program written in BASIC. J. Singapore Paediatr. Soc. 31:129-132.
50. Antao EM, Ewers C, Gurlebeck D, Preisinger R, Homeier T, Li G, Wieler LH. 2009. Signature-tagged mutagenesis in a chicken infection model leads to the identification of a novel avian pathogenic Escherichia coli fimbrial adhesin. PLoS One 4:e7796. doi:10.1371/journal.pone.0007796.
51. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
52. Barnard TJ, Dautin N, Lukacik P, Bernstein HD, Buchanan SK. 2007. Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat. Struct. Mol. Biol. 14:1214-1220.
53. Oomen CJ, van Ulsen P, van Gelder P, Feijen M, Tommassen J, Gros P. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:1257-1266.
54. Restieri C, Garriss G, Locas MC, Dozois CM. 2007. Autotransporterencoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl. Environ. Microbiol. 73: 1553-1562.
55. Heimer SR, Rasko DA, Lockatell CV, Johnson DE, Mobley HL. 2004. Autotransporter genes pic and tsh are associated with Escherichia coli strains that cause acute pyelonephritis and are expressed during urinary tract infection. Infect. Immun. 72:593-597.
56. Sandford EE, Orr M, Balfanz E, Bowerman N, Li X, Zhou H, Johnson TJ, Kariyawasam S, Liu P, Nolan LK, Lamont SJ. 2011. Spleen transcriptome response to infection with avian pathogenic Escherichia coli in broiler chickens. BMC Genomics 12:469. doi:10.1186/1471-2164-12-469.
57. Proft T, Baker EN. 2009. Pili in Gram-negative and Gram-positive bacteria- structure, assembly and their role in disease. Cell. Mol. Life Sci. 66:613-635.
58. Costerton JW. 1999. Introduction to biofilm. Int. J. Antimicrob. Agents 11:217-221.