Home LiteratureArticle Details
PMID: 11080146 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins.

The EMBO journal ·Vol. 19 ·No. 22 ·2000-11-15 ·Pages 5989-99

Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A, Heesemann J

Abstract

The non-fimbrial adhesins, YadA of enteropathogenic Yersinia species, and UspA1 and UspA2 of Moraxella catarrhalis, are established pathogenicity factors. In electron micrographs, both surface proteins appear as distinct 'lollipop'-shaped structures forming a novel type of surface projection on the outer membranes. These structures, amino acid sequence analysis of these molecules and yadA gene manipulation suggest a tripartite organization: an N-terminal oval head domain is followed by a putative coiled-coil rod and terminated by a C-terminal membrane anchor domain. In YadA, the head domain is involved in autoagglutination and binding to host cells and collagen. Analysis of the coiled-coil segment of YadA revealed unusual pentadecad repeats with a periodicity of 3.75, which differs significantly from the 3.5 periodicity found in the Moraxella UspAs and other canonical coiled coils. These findings predict that the surface projections are formed by oligomers containing right- (Yersinia) or left-handed (Moraxella) coiled coils. Strikingly, sequence comparison revealed that related proteins are found in many proteobacteria, both human pathogenic and environmental species, suggesting a common role in adaptation to specific ecological niches.

MeSH Terms
Adhesins, Bacterial/chemistry,genetics,ultrastructure Amino Acid Sequence Bacterial Outer Membrane Proteins/chemistry,genetics,ultrastructure Cell Membrane/chemistry,ultrastructure Genes, Bacterial Humans Microscopy, Electron Molecular Sequence Data Moraxella catarrhalis/chemistry,genetics,ultrastructure Mutation Protein Structure, Tertiary Sequence Homology, Amino Acid Virulence Yersinia enterocolitica/chemistry,genetics,ultrastructure
Chemicals
Adhesins, Bacterial Bacterial Outer Membrane Proteins UspA protein, Moraxella catarrhalis YadA protein, Yersinia
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hoiczyk E
Max von Pettenkofer-Institute for Hygiene and Medical Microbiology, Ludwig Maximilians University Munich, Pettenkoferstrabetae 9a, D-80336 München, Germany.
Roggenkamp A
Reichenbecher M
Lupas A
Heesemann J
References (49)
49 references, click to expand
  1. Envelope structure of four gliding filamentous cyanobacteria.
    J Bacteriol. 1995 May;177(9):2387-95 PMID: 7730269
  2. Deletion of amino acids 29 to 81 in adhesion protein YadA of Yersinia enterocolitica serotype O:8 results in selective abrogation of adherence to neutrophils.
    Infect Immun. 1996 Jul;64(7):2506-14 PMID: 8698473
  3. A workbench for multiple alignment construction and analysis.
    Proteins. 1991;9(3):180-90 PMID: 2006136
  4. Pitch diversity in alpha-helical coiled coils.
    Proteins. 1993 Mar;15(3):223-34 PMID: 8456094
  5. Virulence plasmid-associated autoagglutination in Yersinia spp.
    J Bacteriol. 1984 Jun;158(3):1033-6 PMID: 6725209
  6. Plasmids of human strains of Yersinia enterocolitica: molecular relatedness and possible importance for pathogenesis.
    J Infect Dis. 1983 Jan;147(1):107-15 PMID: 6822745
  7. Substitution of two histidine residues in YadA protein of Yersinia enterocolitica abrogates collagen binding, cell adherence and mouse virulence.
    Mol Microbiol. 1995 Jun;16(6):1207-19 PMID: 8577254
  8. Interaction of enteropathogenic Yersinia enterocolitica with complex basement membranes and the extracellular matrix proteins collagen type IV, laminin-1 and -2, and nidogen/entactin.
    J Biol Chem. 1994 Nov 25;269(47):29732-8 PMID: 7961965
  9. Mechanism of YadA-mediated serum resistance of Yersinia enterocolitica serotype O3.
    Infect Immun. 1992 Jan;60(1):189-95 PMID: 1729182
  10. Model structure of the Omp alpha rod, a parallel four-stranded coiled coil from the hyperthermophilic eubacterium Thermotoga maritima.
    J Mol Biol. 1995 Apr 21;248(1):180-9 PMID: 7731042
  11. The virulence plasmid of Yersinia, an antihost genome.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1315-52 PMID: 9841674
  12. Target recognition failure by the nonspecific defense system: surface constituents of pathogens interfere with the alternative pathway of complement activation.
    Infect Immun. 1992 Mar;60(3):721-7 PMID: 1541544
  13. Characterization of the Moraxella catarrhalis uspA1 and uspA2 genes and their encoded products.
    J Bacteriol. 1999 Jul;181(13):4026-34 PMID: 10383971
  14. A protective epitope of Moraxella catarrhalis is encoded by two different genes.
    Infect Immun. 1997 Nov;65(11):4367-77 PMID: 9353007
  15. The 14-fold periodicity in alpha-tropomyosin and the interaction with actin.
    J Mol Biol. 1976 May 15;103(2):271-98 PMID: 950663
  16. Tetrabrachion: a filamentous archaebacterial surface protein assembly of unusual structure and extreme stability.
    J Mol Biol. 1995 Jan 27;245(4):385-401 PMID: 7837271
  17. Role of YadA in resistance to killing of Yersinia enterocolitica by antimicrobial polypeptides of human granulocytes.
    Infect Immun. 1996 May;64(5):1653-8 PMID: 8613374
  18. Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica.
    Mol Microbiol. 1993 Dec;10(5):995-1011 PMID: 7934875
  19. Heptad breaks in alpha-helical coiled coils: stutters and stammers.
    Proteins. 1996 Oct;26(2):134-45 PMID: 8916221
  20. Structure of the outer membrane protein A transmembrane domain.
    Nat Struct Biol. 1998 Nov;5(11):1013-7 PMID: 9808047
  21. Prediction and analysis of coiled-coil structures.
    Methods Enzymol. 1996;266:513-25 PMID: 8743703
  22. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition.
    Cell. 1993 Jun 4;73(5):887-901 PMID: 8098994
  23. Outer membrane protein YadA of enteropathogenic yersiniae mediates specific binding to cellular but not plasma fibronectin.
    Infect Immun. 1993 Jun;61(6):2513-9 PMID: 8500887
  24. Arthritogenicity of genetically manipulated Yersinia enterocolitica serotype O8 for Lewis rats.
    Infect Immun. 1995 Feb;63(2):714-9 PMID: 7822048
  25. Role of YadA-mediated collagen binding in arthritogenicity of Yersinia enterocolitica serotype O:8: experimental studies with rats.
    Infect Immun. 1995 Aug;63(8):3222-6 PMID: 7622253
  26. Characterization of different oligomeric species of the Yersinia enterocolitica outer membrane protein YadA.
    Med Microbiol Immunol. 1994 Sep;183(4):217-27 PMID: 7845318
  27. Hyperthermostable surface layer protein tetrabrachion from the archaebacterium Staphylothermus marinus: evidence for the presence of a right-handed coiled coil derived from the primary structure.
    J Mol Biol. 1996 Apr 19;257(5):1031-41 PMID: 8632466
  28. Temperature-inducible surface fibrillae associated with the virulence plasmid of Yersinia enterocolitica and Yersinia pseudotuberculosis.
    Infect Immun. 1985 Feb;47(2):561-6 PMID: 3881355
  29. Association of fibril structure formation with cell surface properties of Yersinia enterocolitica.
    Infect Immun. 1984 Oct;46(1):272-5 PMID: 6480110
  30. Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination.
    Infect Immun. 1985 Jun;48(3):782-6 PMID: 2987130
  31. A novel family of channel-forming, autotransporting, bacterial virulence factors.
    Mol Membr Biol. 1997 Jul-Sep;14(3):113-23 PMID: 9394291
  32. High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2875-9 PMID: 8464902
  33. Superficial antigens of Campylobacter (Vibrio) fetus: characterization of antiphagocytic component.
    Infect Immun. 1975 Mar;11(3):517-25 PMID: 46843
  34. Functional mapping of the Yersinia enterocolitica adhesin YadA. Identification Of eight NSVAIG - S motifs in the amino-terminal half of the protein involved in collagen binding.
    Mol Microbiol. 2000 Jul;37(1):192-206 PMID: 10931316
  35. A novel virulence-associated cell surface structure composed of 47-kd protein subunits in Yersinia enterocolitica.
    EMBO J. 1985 Apr;4(4):1013-8 PMID: 4018036
  36. The tranquilizing injection of Yersinia proteins: a pathogen's strategy to resist host defense.
    Biol Chem. 1999 Jul-Aug;380(7-8):795-802 PMID: 10494828
  37. Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp.
    Mol Microbiol. 1989 Apr;3(4):517-29 PMID: 2761389
  38. The regulated outer membrane protein Omp21 from Comamonas acidovorans is identified as a member of a new family of eight-stranded beta-sheet proteins by its sequence and properties.
    J Bacteriol. 1998 Aug;180(15):3741-9 PMID: 9683466
  39. Plasmid-mediated surface fibrillae of Yersinia pseudotuberculosis and Yersinia enterocolitica: relationship to the outer membrane protein YOP1 and possible importance for pathogenesis.
    Infect Immun. 1987 Sep;55(9):2247-54 PMID: 2887516
  40. Crystal structure of invasin: a bacterial integrin-binding protein.
    Science. 1999 Oct 8;286(5438):291-5 PMID: 10514372
  41. Identification of a second family of high-molecular-weight adhesion proteins expressed by non-typable Haemophilus influenzae.
    Mol Microbiol. 1996 Mar;19(6):1215-23 PMID: 8730864
  42. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro.
    J Bacteriol. 2000 Mar;182(5):1364-73 PMID: 10671460
  43. Isolation and cloning of Omp alpha, a coiled-coil protein spanning the periplasmic space of the ancestral eubacterium Thermotoga maritima.
    EMBO J. 1992 Dec;11(12):4369-78 PMID: 1330536
  44. Phenotypic effect of isogenic uspA1 and uspA2 mutations on Moraxella catarrhalis 035E.
    Infect Immun. 1998 Jul;66(7):3113-9 PMID: 9632574
  45. Four different genes responsible for nonimmune immunoglobulin-binding activities within a single strain of Escherichia coli.
    Infect Immun. 2000 Apr;68(4):2205-14 PMID: 10722621
  46. Binding to collagen by Yersinia enterocolitica and Yersinia pseudotuberculosis: evidence for yopA-mediated and chromosomally encoded mechanisms.
    J Bacteriol. 1989 Dec;171(12):6674-9 PMID: 2592347
  47. The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity.
    Mol Microbiol. 1999 Mar;31(5):1443-62 PMID: 10200964
  48. The mechanism of phagocytic uptake promoted by invasin-integrin interaction.
    Trends Cell Biol. 1995 Mar;5(3):120-4 PMID: 14732167
  49. Plasmid-encoded outer membrane protein YadA mediates specific binding of enteropathogenic yersiniae to various types of collagen.
    Infect Immun. 1992 Jun;60(6):2153-9 PMID: 1587583
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-11-15
Pages
5989-99
Language
English
Region
England
NLM ID
8208664
PMCID
PMC305836
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]