A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana

Peng Zhang, Bruno B Chomel, Maureen K. Schau, Jeanna S. Goo, Sara Droz, Karen L. Kelminson, Smitha S. George, Nicholas W. Lerche, Jane E. Koehler

Research output: Contribution to journalArticle

114 Citations (Scopus)

Abstract

Bartonella species are fastidious, Gram-negative human pathogens that can persist in the host bloodstream for years and bind to and invade several types of host cells. For many pathogens, adhesion to host cells and extracellular matrix (ECM) components is a critical virulence determinant. Bacteria often vary expression of surface adhesins by phase or antigenic variation to subvert the host immune response and permit adaptive interaction with different host structures. We developed a macaque animal model for Bartonella quintana infection to detect changes in bacterial outer-membrane proteins (OMP) during prolonged bloodstream infection. We identified a gene family encoding four highly conserved, 100-kDa, variably expressed OMP (Vomp), two of which function as adhesins. The variable expression of Vomp family members appears to be mediated by deletion of one or more vomp genes during chronic bloodstream infection. vomp deletion was observed also in isolates from humans with chronic B. quintana infection. The Vomp are closely related to the afimbrial adhesin, YadA, a virulence factor of Yersinia enterocolitica, The surface-expressed Vomp contain conserved structural features of YadA, including collagen-binding motifs. We demonstrate that the B. quintana Vomp are multifunctional OMP involved in binding to collagen and autoaggregation: VompC confers the ability to bind collagen IV, and VompA is necessary and sufficient for autoaggregation. The B. quintana Vomp are members of the newly recognized family of YadA-like trimeric autotransporters; the Vomp constitute a multigene family, they are variably expressed, and different virulence properties are attributable to individual Vomp family members.

Original languageEnglish (US)
Pages (from-to)13630-13635
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume101
Issue number37
DOIs
StatePublished - Sep 14 2004

Fingerprint

Bartonella quintana
Membrane Proteins
Bartonella Infections
Collagen
Virulence
Bacterial Outer Membrane Proteins
Bartonella
Antigenic Variation
Yersinia enterocolitica
Aptitude
Macaca
Adaptive Immunity
Virulence Factors
Multigene Family
Infection
Genes
Extracellular Matrix
Animal Models

Keywords

  • Bloodstream infection
  • Collagen binding
  • Multifunctional adhesin
  • Phase variation
  • YadA homolog

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana. / Zhang, Peng; Chomel, Bruno B; Schau, Maureen K.; Goo, Jeanna S.; Droz, Sara; Kelminson, Karen L.; George, Smitha S.; Lerche, Nicholas W.; Koehler, Jane E.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 101, No. 37, 14.09.2004, p. 13630-13635.

Research output: Contribution to journalArticle

Zhang, Peng ; Chomel, Bruno B ; Schau, Maureen K. ; Goo, Jeanna S. ; Droz, Sara ; Kelminson, Karen L. ; George, Smitha S. ; Lerche, Nicholas W. ; Koehler, Jane E. / A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana. In: Proceedings of the National Academy of Sciences of the United States of America. 2004 ; Vol. 101, No. 37. pp. 13630-13635.
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T1 - A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana

AU - Zhang, Peng

AU - Chomel, Bruno B

AU - Schau, Maureen K.

AU - Goo, Jeanna S.

AU - Droz, Sara

AU - Kelminson, Karen L.

AU - George, Smitha S.

AU - Lerche, Nicholas W.

AU - Koehler, Jane E.

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N2 - Bartonella species are fastidious, Gram-negative human pathogens that can persist in the host bloodstream for years and bind to and invade several types of host cells. For many pathogens, adhesion to host cells and extracellular matrix (ECM) components is a critical virulence determinant. Bacteria often vary expression of surface adhesins by phase or antigenic variation to subvert the host immune response and permit adaptive interaction with different host structures. We developed a macaque animal model for Bartonella quintana infection to detect changes in bacterial outer-membrane proteins (OMP) during prolonged bloodstream infection. We identified a gene family encoding four highly conserved, 100-kDa, variably expressed OMP (Vomp), two of which function as adhesins. The variable expression of Vomp family members appears to be mediated by deletion of one or more vomp genes during chronic bloodstream infection. vomp deletion was observed also in isolates from humans with chronic B. quintana infection. The Vomp are closely related to the afimbrial adhesin, YadA, a virulence factor of Yersinia enterocolitica, The surface-expressed Vomp contain conserved structural features of YadA, including collagen-binding motifs. We demonstrate that the B. quintana Vomp are multifunctional OMP involved in binding to collagen and autoaggregation: VompC confers the ability to bind collagen IV, and VompA is necessary and sufficient for autoaggregation. The B. quintana Vomp are members of the newly recognized family of YadA-like trimeric autotransporters; the Vomp constitute a multigene family, they are variably expressed, and different virulence properties are attributable to individual Vomp family members.

AB - Bartonella species are fastidious, Gram-negative human pathogens that can persist in the host bloodstream for years and bind to and invade several types of host cells. For many pathogens, adhesion to host cells and extracellular matrix (ECM) components is a critical virulence determinant. Bacteria often vary expression of surface adhesins by phase or antigenic variation to subvert the host immune response and permit adaptive interaction with different host structures. We developed a macaque animal model for Bartonella quintana infection to detect changes in bacterial outer-membrane proteins (OMP) during prolonged bloodstream infection. We identified a gene family encoding four highly conserved, 100-kDa, variably expressed OMP (Vomp), two of which function as adhesins. The variable expression of Vomp family members appears to be mediated by deletion of one or more vomp genes during chronic bloodstream infection. vomp deletion was observed also in isolates from humans with chronic B. quintana infection. The Vomp are closely related to the afimbrial adhesin, YadA, a virulence factor of Yersinia enterocolitica, The surface-expressed Vomp contain conserved structural features of YadA, including collagen-binding motifs. We demonstrate that the B. quintana Vomp are multifunctional OMP involved in binding to collagen and autoaggregation: VompC confers the ability to bind collagen IV, and VompA is necessary and sufficient for autoaggregation. The B. quintana Vomp are members of the newly recognized family of YadA-like trimeric autotransporters; the Vomp constitute a multigene family, they are variably expressed, and different virulence properties are attributable to individual Vomp family members.

KW - Bloodstream infection

KW - Collagen binding

KW - Multifunctional adhesin

KW - Phase variation

KW - YadA homolog

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