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Research

Critical Role of a Sheath Phosphorylation Site On the Assembly and Function of an Atypical Type VI Secretion System

Jason Ziveri, Cerina Chhuon, Anne Jamet, Héloïse Rytter, Guénolé Prigent, Fabiola Tros, Monique Barel, Mathieu Coureuil, Claire Lays, View ORCID ProfileThomas Henry, Nicholas H. Keep, Ida Chiara Guerrera  Correspondence email and View ORCID ProfileAlain Charbit  Correspondence email
Molecular & Cellular Proteomics December 1, 2019, First published on October 2, 2019, 18 (12) 2418-2432; https://doi.org/10.1074/mcp.RA119.001532
Jason Ziveri
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Cerina Chhuon
Plateforme protéomique 3P5-Necker, Universit[c33c]zpi;● Paris Descartes - Structure Fédérative de Recherche Necker, INSERM US24/CNRS UMS3633, Paris 75015, France
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Anne Jamet
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Héloïse Rytter
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Guénolé Prigent
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Fabiola Tros
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Monique Barel
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Mathieu Coureuil
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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Claire Lays
CIRI, Centre International de Recherche en Infectiologie, Université Lyon, Inserm, U1111, University Claude Bernard Lyon 1, CNRS, UMR5308, École Normale Supérieure de Lyon, Labex Ecofect, Eco-evolutionary dynamics of infectious diseases, F-69007, LYON, France
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Thomas Henry
CIRI, Centre International de Recherche en Infectiologie, Université Lyon, Inserm, U1111, University Claude Bernard Lyon 1, CNRS, UMR5308, École Normale Supérieure de Lyon, Labex Ecofect, Eco-evolutionary dynamics of infectious diseases, F-69007, LYON, France
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Nicholas H. Keep
Crystallography, Institute for Structural and Molecular Biology, Department of Biological Sciences Birkbeck, University of London, United Kingdom
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Ida Chiara Guerrera
Plateforme protéomique 3P5-Necker, Universit[c33c]zpi;● Paris Descartes - Structure Fédérative de Recherche Necker, INSERM US24/CNRS UMS3633, Paris 75015, France
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  • For correspondence: chiara.guerrera@inserm.fr
Alain Charbit
Université Paris Descartes, Sorbonne Paris Cité, INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades. Team 7: Pathogenesis of Systemic Infections, Paris 75015, France
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  • For correspondence: alain.charbit@inserm.fr
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Graphical Abstract

Figure1
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Highlights

  • Phosphorylation on Y139 of the sheath protein IglB of Francisella.

  • IglB substitutions Y139A, Y139D or Y139E prevent T6SS formation.

  • Y139F substitution delays but does not abolish phagosomal escape in macrophages.

  • Insight into the role of sheath phosphorylation in T6SS biogenesis.

Abstract

The bacterial pathogen Francisella tularensis possesses a noncanonical type VI secretion system (T6SS) that is required for phagosomal escape in infected macrophages. KCl stimulation has been previously used to trigger assembly and secretion of the T6SS in culture. By differential proteomics, we found here that the amounts of the T6SS proteins remained unchanged upon KCl stimulation, suggesting involvement of post-translational modifications in T6SS assembly. A phosphoproteomic analysis indeed identified a unique phosphorylation site on IglB, a key component of the T6SS sheath. Substitutions of Y139 with alanine or phosphomimetics prevented T6SS formation and abolished phagosomal escape whereas substitution with phenylalanine delayed but did not abolish phagosomal escape in J774–1 macrophages. Altogether our data demonstrated that the Y139 site of IglB plays a critical role in T6SS biogenesis, suggesting that sheath phosphorylation could participate to T6SS dynamics.

Data are available via ProteomeXchange with identifier PXD013619; and on MS-Viewer, key lkaqkllxwx

  • Phosphoproteome
  • Bacteria
  • Phosphorylation
  • Microbiology
  • Pathogens
  • Francisella
  • IglB
  • Type 6 secretion system

Footnotes

  • Author contributions: J.Z., M.B., M.C., T.H., I.C.G., and A.C. designed research; J.Z., C.C., H.R., G.P., F.T., and C.L. performed research; J.Z., A.J., M.C., C.L., N.H.K., I.C.G., and A.C. analyzed data; C.C. and T.H. contributed new reagents/analytic tools; N.H.K., I.C.G., and A.C. wrote the paper.

  • ↵* These studies were supported by INSERM, CNRS and Université Paris Descartes Paris Cité Sorbonne. Jason Ziveri was funded by a fellowship from the “Délégation Générale à l'Armement”. Claire Lays was funded by a fellowship from the LABEX ECOFECT (ANR-11-LABX-0048) of Université de Lyon, within the program “Investissement d'Avenir” (ANR-11-IDEX-0007) operated by the French National Research Agency (ANR). No author has an actual or perceived conflict of interest with the contents of this article.

  • ↵Embedded Image This article contains supplemental material.

  • Received April 29, 2019.
  • Revision received September 3, 2019.
  • © 2019 Ziveri et al.

Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.

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Critical Role of a Sheath Phosphorylation Site On the Assembly and Function of an Atypical Type VI Secretion System
Jason Ziveri, Cerina Chhuon, Anne Jamet, Héloïse Rytter, Guénolé Prigent, Fabiola Tros, Monique Barel, Mathieu Coureuil, Claire Lays, Thomas Henry, Nicholas H. Keep, Ida Chiara Guerrera, Alain Charbit
Molecular & Cellular Proteomics December 1, 2019, First published on October 2, 2019, 18 (12) 2418-2432; DOI: 10.1074/mcp.RA119.001532

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Critical Role of a Sheath Phosphorylation Site On the Assembly and Function of an Atypical Type VI Secretion System
Jason Ziveri, Cerina Chhuon, Anne Jamet, Héloïse Rytter, Guénolé Prigent, Fabiola Tros, Monique Barel, Mathieu Coureuil, Claire Lays, Thomas Henry, Nicholas H. Keep, Ida Chiara Guerrera, Alain Charbit
Molecular & Cellular Proteomics December 1, 2019, First published on October 2, 2019, 18 (12) 2418-2432; DOI: 10.1074/mcp.RA119.001532
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Molecular & Cellular Proteomics: 18 (12)
Molecular & Cellular Proteomics
Vol. 18, Issue 12
1 Dec 2019
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