Home LiteratureArticle Details
PMID: 15271922 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Multiple functions of the leucine-rich repeat protein LrrA of Treponema denticola.

Infection and immunity ·Vol. 72 ·No. 8 ·2004-08-00 ·Pages 4619-27

Ikegami A, Honma K, Sharma A, Kuramitsu HK

Abstract

The gene lrrA, encoding a leucine-rich repeat protein, LrrA, that contains eight consensus tandem repeats of 23 amino acid residues, has been identified in Treponema denticola ATCC 35405. A leucine-rich repeat is a generally useful protein-binding motif, and proteins containing this repeat are typically involved in protein-protein interactions. Southern blot analysis demonstrated that T. denticola ATCC 35405 expresses the lrrA gene, but the gene was not identified in T. denticola ATCC 33520. In order to analyze the functions of LrrA in T. denticola, an lrrA-inactivated mutant of strain ATCC 35405 and an lrrA gene expression transformant of strain ATCC 33520 were constructed. Characterization of the mutant and transformant demonstrated that LrrA is associated with the extracytoplasmic fraction of T. denticola and expresses multifunctional properties. It was demonstrated that the attachment of strain ATCC 35405 to HEp-2 cell cultures and coaggregation with Tannerella forsythensis were attenuated by the lrrA mutation. In addition, an in vitro binding assay demonstrated specific binding of LrrA to a portion of the Tannerella forsythensis leucine-rich repeat protein, BspA, which is mediated by the N-terminal region of LrrA. It was also observed that the lrrA mutation caused a reduction of swarming in T. denticola ATCC 35405 and consequently attenuated tissue penetration. These results suggest that the leucine-rich repeat protein LrrA plays a role in the attachment and penetration of human epithelial cells and coaggregation with Tannerella forsythensis. These properties may play important roles in the virulence of T. denticola.

MeSH Terms
Amino Acid Sequence Bacterial Adhesion Bacterial Proteins/chemistry,genetics,metabolism Base Sequence Cell Line Cloning, Molecular Humans Leucine-Rich Repeat Proteins Molecular Sequence Data Movement Proteins/chemistry,genetics,metabolism Recombinant Proteins/genetics,metabolism Repetitive Sequences, Amino Acid Sequence Analysis, DNA Treponema/genetics,metabolism,pathogenicity,physiology
Chemicals
Bacterial Proteins Leucine-Rich Repeat Proteins Proteins Recombinant Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ikegami Akihiko
Department of Oral Biology, School of Dental Medicine, State University of New York, Buffalo, 14214, USA.
Honma Kiyonobu
Sharma Ashu
Kuramitsu Howard K
References (49)
49 references, click to expand
  1. The effect of SRP on the clinical and microbiological parameters of periodontal diseases.
    J Clin Periodontol. 1997 May;24(5):324-34 PMID: 9178112
  2. Molecular characterization and cellular localization of TpLRR, a processed leucine-rich repeat protein of Treponema pallidum, the syphilis spirochete.
    J Bacteriol. 1997 May;179(10):3188-95 PMID: 9150213
  3. Differential attachment of oral treponemes to monolayers of epithelial cells.
    J Periodontol. 1997 Oct;68(10):1010-8 PMID: 9358369
  4. Adherence of human oral spirochetes by collagen-binding proteins.
    Microbiol Immunol. 1997;41(12):917-23 PMID: 9492176
  5. Structural diversity of leucine-rich repeat proteins.
    J Mol Biol. 1998 Apr 3;277(3):519-27 PMID: 9533877
  6. Cytopathic effects of the major surface protein and the chymotrypsinlike protease of Treponema denticola.
    Infect Immun. 1998 May;66(5):1869-77 PMID: 9573063
  7. Molecular characterization of PcpA: a novel choline-binding protein of Streptococcus pneumoniae.
    FEMS Microbiol Lett. 1998 Jul 1;164(1):207-14 PMID: 9675866
  8. Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037.
    Infect Immun. 1998 Dec;66(12):5703-10 PMID: 9826345
  9. Development of a system for expressing heterologous genes in the oral spirochete Treponema denticola and its use in expression of the Treponema pallidum flaA gene.
    Infect Immun. 1999 Jul;67(7):3653-6 PMID: 10377154
  10. A capping domain for LRR protein interaction modules.
    FEBS Lett. 1999 Aug 13;456(3):349-51 PMID: 10462041
  11. Studies on the binding of Treponema pectinovorum to HEp-2 epithelial cells.
    Oral Microbiol Immunol. 1999 Jun;14(3):165-71 PMID: 10495710
  12. Adherence to and penetration through endothelial cells by oral treponemes.
    Oral Microbiol Immunol. 1999 Dec;14(6):379-83 PMID: 10895695
  13. Molecular pathogenesis of the cell surface proteins and lipids from Treponema denticola.
    FEMS Microbiol Lett. 1999 Dec 15;181(2):199-204 PMID: 10585538
  14. Structure of the lnlB leucine-rich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes.
    Mol Cell. 1999 Dec;4(6):1063-72 PMID: 10635330
  15. Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment.
    Infect Immun. 2000 Apr;68(4):1884-92 PMID: 10722578
  16. Spirochaetal lipoproteins and pathogenesis.
    Microbiology. 2000 Jul;146 ( Pt 7):1491-504 PMID: 10878114
  17. Oral microbial communities: biofilms, interactions, and genetic systems.
    Annu Rev Microbiol. 2000;54:413-37 PMID: 11018133
  18. Taxonomy and virulence of oral spirochetes.
    Oral Microbiol Immunol. 2000 Feb;15(1):1-9 PMID: 11155157
  19. Cloning and expression of two novel hemin binding protein genes from Treponema denticola.
    Infect Immun. 2001 Jul;69(7):4465-72 PMID: 11401987
  20. Development of a gene inactivation system for Bacteroides forsythus: construction and characterization of a BspA mutant.
    Infect Immun. 2001 Jul;69(7):4686-90 PMID: 11402017
  21. Review: proteins with repeated sequence--structural prediction and modeling.
    J Struct Biol. 2001 May-Jun;134(2-3):132-44 PMID: 11551175
  22. Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola.
    Infect Immun. 2001 Oct;69(10):6276-83 PMID: 11553571
  23. Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit.
    J Mol Biol. 2001 Sep 28;312(4):807-21 PMID: 11575934
  24. The leucine-rich repeat as a protein recognition motif.
    Curr Opin Struct Biol. 2001 Dec;11(6):725-32 PMID: 11751054
  25. Assessment of the ability to model proteins with leucine-rich repeats in light of the latest structural information.
    Protein Sci. 2002 May;11(5):1082-90 PMID: 11967365
  26. Construction and characterization of a cheA mutant of Treponema denticola.
    J Bacteriol. 2002 Jun;184(11):3130-4 PMID: 12003957
  27. Communication among oral bacteria.
    Microbiol Mol Biol Rev. 2002 Sep;66(3):486-505, table of contents PMID: 12209001
  28. Bacterial coaggregation: an integral process in the development of multi-species biofilms.
    Trends Microbiol. 2003 Feb;11(2):94-100 PMID: 12598132
  29. Attachment of Treponema denticola to cultured human epithelial cells.
    Scand J Dent Res. 1984 Feb;92(1):55-63 PMID: 6585912
  30. Purification and characterization of an enzyme produced by Treponema denticola capable of hydrolyzing synthetic trypsin substrates.
    Infect Immun. 1986 Jul;53(1):213-20 PMID: 3013780
  31. Quantitative relationship of Treponema denticola to severity of periodontal disease.
    Infect Immun. 1988 Apr;56(4):726-8 PMID: 3346072
  32. Tip-oriented adherence of Treponema denticola to fibronectin.
    Infect Immun. 1990 Dec;58(12):3924-8 PMID: 2254019
  33. Sulfhydryl-dependent attachment of Treponema denticola to laminin and other proteins.
    Infect Immun. 1991 Nov;59(11):4230-7 PMID: 1937780
  34. Relative proportions of pathogen-related oral spirochetes (PROS) and Treponema denticola in supragingival and subgingival plaque from patients with periodontitis.
    J Periodontol. 1992 Feb;63(2):131-6 PMID: 1372653
  35. Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola.
    Oral Microbiol Immunol. 1992 Oct;7(5):280-4 PMID: 1337373
  36. Fibronectin-binding proteins of a human oral spirochete Treponema denticola.
    Microbiol Immunol. 1993;37(1):75-8 PMID: 8474361
  37. Bacterial mediators in periodontal disease.
    Clin Infect Dis. 1993 Jun;16 Suppl 4:S203-10 PMID: 8324120
  38. Attachment of T. denticola strains ATCC 33520, ATCC 35405, B11 and Ny541 to a morphologically distinct population of rat palatal epithelial cells.
    J Periodontal Res. 1993 Jul;28(4):274-80 PMID: 8101566
  39. Attachment of Treponema denticola strains to monolayers of epithelial cells of different origin.
    Oral Microbiol Immunol. 1993 Apr;8(2):84-8 PMID: 8355990
  40. Spirochaetes in oral infections.
    Endod Dent Traumatol. 1993 Jun;9(3):87-94 PMID: 8243346
  41. Involvement of treponemal surface-located protein and carbohydrate moieties in the attachment of Treponema denticola ATCC 33520 to cultured rat palatal epithelial cells.
    Oral Microbiol Immunol. 1993 Aug;8(4):236-41 PMID: 8247611
  42. The leucine-rich repeat: a versatile binding motif.
    Trends Biochem Sci. 1994 Oct;19(10):415-21 PMID: 7817399
  43. Intergeneric coaggregation of oral Treponema spp. with Fusobacterium spp. and intrageneric coaggregation among Fusobacterium spp.
    Infect Immun. 1995 Dec;63(12):4584-8 PMID: 7591109
  44. Sequence analysis, expression, and binding activity of recombinant major outer sheath protein (Msp) of Treponema denticola.
    J Bacteriol. 1996 May;178(9):2489-97 PMID: 8626313
  45. Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant.
    J Bacteriol. 1996 Jun;178(12):3664-7 PMID: 8655571
  46. The major surface protein complex of Treponema denticola depolarizes and induces ion channels in HeLa cell membranes.
    Infect Immun. 1996 Aug;64(8):2904-10 PMID: 8757811
  47. Characterization of the Treponema denticola prtP gene encoding a prolyl-phenylalanine-specific protease (dentilisin).
    Infect Immun. 1996 Dec;64(12):5178-86 PMID: 8945563
  48. Conservation of msp, the gene encoding the major outer membrane protein of oral Treponema spp.
    J Bacteriol. 1997 Feb;179(4):1082-9 PMID: 9023187
  49. Clinical and microbiological features of subjects with adult periodontitis who responded poorly to scaling and root planing.
    J Clin Periodontol. 1997 Oct;24(10):767-76 PMID: 9350562
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2004-08-00
Pages
4619-27
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC470683
Subset
IM
Grants
NIDCR NIH HHS · R01 DE009821 · United States
NIDCR NIH HHS · R01 DE014749 · United States
NIDCR NIH HHS · DE09821 · United States
NIDCR NIH HHS · DE14749 · United States
Databases
GENBANK
AY545217
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: product@genelibs.com