Association of a high-molecular weight arginine-binding protein of Fusobacterium nucleatum ATCC 10953 with adhesion to secretory immunoglobulin A and coaggregation with Streptococcus cristatus

A. M. Edwards, T. J. Grossman, Joel D Rudney

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19 Citations (Scopus)

Abstract

Introduction: Fusobacterium nucleatum coaggregates with a diverse range of bacterial species, and binds to host tissues and proteins such as immunoglobulin. These interactions may support the attachment of a variety of organisms to oral surfaces and can facilitate the invasion of soft tissues. We hypothesized that coaggregation with streptococci and immunoglobulin binding may occur by a common adhesin sensitive to l-arginine. Methods: Repeated mixing of F. nucleatum with non-immune secretory immunoglobulin A (S-IgA) and recovery of non-agglutinating cells isolated a spontaneous mutant (isolate 21) of F. nucleatum that was defective in S-IgA binding. Wild-type and mutant F. nucleatum were compared by coaggregation and adhesion assays. Results: Isolate 21 exhibited significantly reduced S-IgA binding and coaggregation with oral streptococci but not with Porphyromonas gingivalis. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis revealed that the mutant was deficient compared to wild-type for a single protein of approximately 360 kilodaltons. The corresponding protein was isolated from wild-type F. nucleatum protein preparations by coprecipitation with arginine-agarose beads. This protein was able to bind both Streptococcus cristatus and S-IgA. Mass spectrometry analysis indicated that this protein was closely related to putative autotransporter proteins in other F. nucleatum strains and was a 100% match to the deduced amino acid sequence of a 10,638-base-pair open reading frame in the incomplete genome sequence of F. nucleatum ATCC 10953. Peptides identified by MS-MS analysis spanned most of the predicted amino acid sequence, suggesting that the mature protein is not subject to postsecretory cleavage. Conclusion: Coaggregation represents a novel function within the autotransporter class of proteins, which are often associated with virulence.

Original languageEnglish (US)
Pages (from-to)217-224
Number of pages8
JournalOral Microbiology and Immunology
Volume22
Issue number4
DOIs
StatePublished - Aug 1 2007

Fingerprint

Fusobacterium nucleatum
Secretory Immunoglobulin A
Streptococcus
Arginine
Carrier Proteins
Molecular Weight
Proteins
Immunoglobulins
Amino Acid Sequence
Porphyromonas gingivalis
Base Pairing
Sodium Dodecyl Sulfate
Sepharose
Immunoglobulin A
Open Reading Frames
Virulence
Polyacrylamide Gel Electrophoresis
Mass Spectrometry
Genome

Keywords

  • Autotransporter
  • Coaggregation
  • Fusobacterium nucleatum
  • Immunoglobulin binding
  • Streptococcus cristatus

Cite this

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title = "Association of a high-molecular weight arginine-binding protein of Fusobacterium nucleatum ATCC 10953 with adhesion to secretory immunoglobulin A and coaggregation with Streptococcus cristatus",
abstract = "Introduction: Fusobacterium nucleatum coaggregates with a diverse range of bacterial species, and binds to host tissues and proteins such as immunoglobulin. These interactions may support the attachment of a variety of organisms to oral surfaces and can facilitate the invasion of soft tissues. We hypothesized that coaggregation with streptococci and immunoglobulin binding may occur by a common adhesin sensitive to l-arginine. Methods: Repeated mixing of F. nucleatum with non-immune secretory immunoglobulin A (S-IgA) and recovery of non-agglutinating cells isolated a spontaneous mutant (isolate 21) of F. nucleatum that was defective in S-IgA binding. Wild-type and mutant F. nucleatum were compared by coaggregation and adhesion assays. Results: Isolate 21 exhibited significantly reduced S-IgA binding and coaggregation with oral streptococci but not with Porphyromonas gingivalis. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis revealed that the mutant was deficient compared to wild-type for a single protein of approximately 360 kilodaltons. The corresponding protein was isolated from wild-type F. nucleatum protein preparations by coprecipitation with arginine-agarose beads. This protein was able to bind both Streptococcus cristatus and S-IgA. Mass spectrometry analysis indicated that this protein was closely related to putative autotransporter proteins in other F. nucleatum strains and was a 100{\%} match to the deduced amino acid sequence of a 10,638-base-pair open reading frame in the incomplete genome sequence of F. nucleatum ATCC 10953. Peptides identified by MS-MS analysis spanned most of the predicted amino acid sequence, suggesting that the mature protein is not subject to postsecretory cleavage. Conclusion: Coaggregation represents a novel function within the autotransporter class of proteins, which are often associated with virulence.",
keywords = "Autotransporter, Coaggregation, Fusobacterium nucleatum, Immunoglobulin binding, Streptococcus cristatus",
author = "Edwards, {A. M.} and Grossman, {T. J.} and Rudney, {Joel D}",
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T1 - Association of a high-molecular weight arginine-binding protein of Fusobacterium nucleatum ATCC 10953 with adhesion to secretory immunoglobulin A and coaggregation with Streptococcus cristatus

AU - Edwards, A. M.

AU - Grossman, T. J.

AU - Rudney, Joel D

PY - 2007/8/1

Y1 - 2007/8/1

N2 - Introduction: Fusobacterium nucleatum coaggregates with a diverse range of bacterial species, and binds to host tissues and proteins such as immunoglobulin. These interactions may support the attachment of a variety of organisms to oral surfaces and can facilitate the invasion of soft tissues. We hypothesized that coaggregation with streptococci and immunoglobulin binding may occur by a common adhesin sensitive to l-arginine. Methods: Repeated mixing of F. nucleatum with non-immune secretory immunoglobulin A (S-IgA) and recovery of non-agglutinating cells isolated a spontaneous mutant (isolate 21) of F. nucleatum that was defective in S-IgA binding. Wild-type and mutant F. nucleatum were compared by coaggregation and adhesion assays. Results: Isolate 21 exhibited significantly reduced S-IgA binding and coaggregation with oral streptococci but not with Porphyromonas gingivalis. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis revealed that the mutant was deficient compared to wild-type for a single protein of approximately 360 kilodaltons. The corresponding protein was isolated from wild-type F. nucleatum protein preparations by coprecipitation with arginine-agarose beads. This protein was able to bind both Streptococcus cristatus and S-IgA. Mass spectrometry analysis indicated that this protein was closely related to putative autotransporter proteins in other F. nucleatum strains and was a 100% match to the deduced amino acid sequence of a 10,638-base-pair open reading frame in the incomplete genome sequence of F. nucleatum ATCC 10953. Peptides identified by MS-MS analysis spanned most of the predicted amino acid sequence, suggesting that the mature protein is not subject to postsecretory cleavage. Conclusion: Coaggregation represents a novel function within the autotransporter class of proteins, which are often associated with virulence.

AB - Introduction: Fusobacterium nucleatum coaggregates with a diverse range of bacterial species, and binds to host tissues and proteins such as immunoglobulin. These interactions may support the attachment of a variety of organisms to oral surfaces and can facilitate the invasion of soft tissues. We hypothesized that coaggregation with streptococci and immunoglobulin binding may occur by a common adhesin sensitive to l-arginine. Methods: Repeated mixing of F. nucleatum with non-immune secretory immunoglobulin A (S-IgA) and recovery of non-agglutinating cells isolated a spontaneous mutant (isolate 21) of F. nucleatum that was defective in S-IgA binding. Wild-type and mutant F. nucleatum were compared by coaggregation and adhesion assays. Results: Isolate 21 exhibited significantly reduced S-IgA binding and coaggregation with oral streptococci but not with Porphyromonas gingivalis. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis revealed that the mutant was deficient compared to wild-type for a single protein of approximately 360 kilodaltons. The corresponding protein was isolated from wild-type F. nucleatum protein preparations by coprecipitation with arginine-agarose beads. This protein was able to bind both Streptococcus cristatus and S-IgA. Mass spectrometry analysis indicated that this protein was closely related to putative autotransporter proteins in other F. nucleatum strains and was a 100% match to the deduced amino acid sequence of a 10,638-base-pair open reading frame in the incomplete genome sequence of F. nucleatum ATCC 10953. Peptides identified by MS-MS analysis spanned most of the predicted amino acid sequence, suggesting that the mature protein is not subject to postsecretory cleavage. Conclusion: Coaggregation represents a novel function within the autotransporter class of proteins, which are often associated with virulence.

KW - Autotransporter

KW - Coaggregation

KW - Fusobacterium nucleatum

KW - Immunoglobulin binding

KW - Streptococcus cristatus

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U2 - 10.1111/j.1399-302X.2006.00343.x

DO - 10.1111/j.1399-302X.2006.00343.x

M3 - Article

VL - 22

SP - 217

EP - 224

JO - Molecular Oral Microbiology

JF - Molecular Oral Microbiology

SN - 2041-1006

IS - 4

ER -