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The rickettsia surface cell antigen 4 applies mimicry to bind to and activate vinculin.

Park H, Lee JH, Gouin E, Cossart P, Izard T
J Biol Chem 286 35096-103 (2011)
Cited: 36 times
EuropePMC logo PMID: 21841197

Abstract

Pathogenic Rickettsia species cause high morbidity and mortality, especially R. prowazekii, the causative agent of typhus. Like many intracellular pathogens, Rickettsia exploit the cytoskeleton to enter and spread within the host cell. Here we report that the cell surface antigen sca4 of Rickettsia co-localizes with vinculin in cells at sites of focal adhesions in sca4-transfected cells and that sca4 binds to and activates vinculin through two vinculin binding sites (VBSs) that are conserved across all Rickettsia. Remarkably, this occurs through molecular mimicry of the vinculin-talin interaction that is also seen with the IpaA invasin of the intracellular pathogen Shigella, where binding of these VBSs to the vinculin seven-helix bundle head domain (Vh1) displaces intramolecular interactions with the vinculin tail domain that normally clamp vinculin in an inactive state. Finally, the vinculin·sca4-VBS crystal structures reveal that vinculin adopts a new conformation when bound to the C-terminal VBS of sca4. Collectively, our data define the mechanism by which sca4 activates vinculin and interacts with the actin cytoskeleton, and they suggest important roles for vinculin in Rickettsia pathogenesis.

Articles - 3tj6 mentioned but not cited (1)

  1. The rickettsia surface cell antigen 4 applies mimicry to bind to and activate vinculin. Park H, Lee JH, Gouin E, Cossart P, Izard T. J Biol Chem 286 35096-35103 (2011)


Reviews citing this publication (12)

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  4. The cytoskeletal protein α-catenin unfurls upon binding to vinculin. Rangarajan ES, Izard T. J Biol Chem 287 18492-18499 (2012)
  5. Asian Citrus Psyllid Expression Profiles Suggest Candidatus Liberibacter Asiaticus-Mediated Alteration of Adult Nutrition and Metabolism, and of Nymphal Development and Immunity. Vyas M, Fisher TW, He R, Nelson W, Yin G, Cicero JM, Willer M, Kim R, Kramer R, May GA, Crow JA, Soderlund CA, Gang DR, Brown JK. PLoS One 10 e0130328 (2015)
  6. Autoimmunity Links Vinculin to the Pathophysiology of Chronic Functional Bowel Changes Following Campylobacter jejuni Infection in a Rat Model. Pimentel M, Morales W, Pokkunuri V, Brikos C, Kim SM, Kim SE, Triantafyllou K, Weitsman S, Marsh Z, Marsh E, Chua KS, Srinivasan S, Barlow GM, Chang C. Dig Dis Sci 60 1195-1205 (2015)
  7. Which Way In? The RalF Arf-GEF Orchestrates Rickettsia Host Cell Invasion. Rennoll-Bankert KE, Rahman MS, Gillespie JJ, Guillotte ML, Kaur SJ, Lehman SS, Beier-Sexton M, Azad AF. PLoS Pathog 11 e1005115 (2015)
  8. Proteome analysis and serological characterization of surface-exposed proteins of Rickettsia heilongjiangensis. Qi Y, Xiong X, Wang X, Duan C, Jia Y, Jiao J, Gong W, Wen B. PLoS One 8 e70440 (2013)
  9. Fibroblast growth factor receptor-1 mediates internalization of pathogenic spotted fever rickettsiae into host endothelium. Sahni A, Patel J, Narra HP, Schroeder CLC, Walker DH, Sahni SK. PLoS One 12 e0183181 (2017)
  10. Vinculin Interacts with the Chlamydia Effector TarP Via a Tripartite Vinculin Binding Domain to Mediate Actin Recruitment and Assembly at the Plasma Membrane. Thwaites TR, Pedrosa AT, Peacock TP, Carabeo RA. Front Cell Infect Microbiol 5 88 (2015)
  11. Identification of novel surface-exposed proteins of Rickettsia rickettsii by affinity purification and proteomics. Gong W, Xiong X, Qi Y, Jiao J, Duan C, Wen B. PLoS One 9 e100253 (2014)
  12. Rickettsia rickettsii outer membrane protein YbgF induces protective immunity in C3H/HeN mice. Gong W, Qi Y, Xiong X, Jiao J, Duan C, Wen B. Hum Vaccin Immunother 11 642-649 (2015)
  13. Proteolytic Cleavage of the Immunodominant Outer Membrane Protein rOmpA in Rickettsia rickettsii. Noriea NF, Clark TR, Mead D, Hackstadt T. J Bacteriol 199 e00826-16 (2017)
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  15. Molecular characterization and tissue-specific gene expression of Dermacentor variabilis α-catenin in response to rickettsial infection. Sunyakumthorn P, Petchampai N, Kearney MT, Sonenshine DE, Macaluso KR. Insect Mol Biol 21 197-204 (2012)
  16. Chlamydial virulence factor TarP mimics talin to disrupt the talin-vinculin complex. Whitewood AJ, Singh AK, Brown DG, Goult BT. FEBS Lett 592 1751-1760 (2018)
  17. Crystal structure of vinculin in complex with vinculin binding site 50 (VBS50), the integrin binding site 2 (IBS2) of talin. Yogesha SD, Rangarajan ES, Vonrhein C, Bricogne G, Izard T. Protein Sci 21 583-588 (2012)
  18. The metavinculin tail domain directs constitutive interactions with raver1 and vinculin RNA. Lee JH, Rangarajan ES, Vonrhein C, Bricogne G, Izard T. J Mol Biol 422 697-704 (2012)
  19. Crystal structure of the N-terminal domains of the surface cell antigen 4 of Rickettsia. Lee JH, Vonrhein C, Bricogne G, Izard T. Protein Sci 22 1425-1431 (2013)
  20. GroEL is an immunodominant surface-exposed antigen of Rickettsia typhi. Rauch J, Barton J, Kwiatkowski M, Wunderlich M, Steffen P, Moderzynski K, Papp S, Höhn K, Schwanke H, Witt S, Richardt U, Mehlhoop U, Schlüter H, Pianka V, Fleischer B, Tappe D, Osterloh A. PLoS One 16 e0253084 (2021)
  21. The Cryogenic Electron Microscopy Structure of the Cell Adhesion Regulator Metavinculin Reveals an Isoform-Specific Kinked Helix in Its Cytoskeleton Binding Domain. Rangarajan ES, Izard T. Int J Mol Sci 22 E645 (2021)
  22. New insights into the impact of microbiome on horizontal and vertical transmission of a tick-borne pathogen. Du LF, Zhang MZ, Yuan TT, Ni XB, Wei W, Cui XM, Wang N, Xiong T, Zhang J, Pan YS, Zhu DY, Li LJ, Xia LY, Wang TH, Wei R, Liu HB, Sun Y, Zhao L, Lam TT, Cao WC, Jia N. Microbiome 11 50 (2023)
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