The modular structure of the inner-membrane ring component PrgK facilitates assembly of the type III secretion system basal body

Julien R C Bergeron; Liam J Worrall; Soumya De; Nikolaos G Sgourakis; Adrienne H Cheung; Emilie Lameignere; Mark Okon; Gregory A Wasney; David Baker; Lawrence P McIntosh; Natalie C J Strynadka

doi:10.1016/j.str.2014.10.021

The modular structure of the inner-membrane ring component PrgK facilitates assembly of the type III secretion system basal body

Julien R C Bergeron, Liam J Worrall, Soumya De, Nikolaos G Sgourakis, Adrienne H Cheung, Emilie Lameignere, Mark Okon, Gregory A Wasney, David Baker, Lawrence P McIntosh, Natalie C J Strynadka

Randall Centre of Cell & Molecular Biophysics

Department of Biochemistry and Molecular Biology, Life Sciences Centre, The University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada; Centre for Blood Research, Life Sciences Centre, The University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada.
National Institute of Diabetes & Digestive & Kidney Diseases, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892, USA. Electronic address: [email protected].
University of Washington
Department of Biochemistry and Molecular Biology, The University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC, V6T 1Z3, Canada; Department of Chemistry, University of British Columbia, 2350 Health Sciences Mall, Vancouver BC, V6T 1Z3, Canada.
Department of Biochemistry and Molecular Biology, Life Sciences Centre, The University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada; Centre for Blood Research, Life Sciences Centre, The University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada. Electronic address: [email protected].

Research output: Contribution to journal › Article › peer-review

39 Citations (Scopus)

Abstract

The type III secretion system (T3SS) is a large macromolecular assembly found at the surface of many pathogenic Gram-negative bacteria. Its role is to inject toxic "effector" proteins into the cells of infected organisms. The molecular details of the assembly of this large, multimembrane-spanning complex remain poorly understood. Here, we report structural, biochemical, and functional analyses of PrgK, an inner-membrane component of the prototypical Salmonella typhimurium T3SS. We have obtained the atomic structures of the two ring building globular domains and show that the C-terminal transmembrane helix is not essential for assembly and secretion. We also demonstrate that structural rearrangement of the two PrgK globular domains, driven by an interconnecting linker region, may promote oligomerization into ring structures. Finally, we used electron microscopy-guided symmetry modeling to propose a structural model for the intimately associated PrgH-PrgK ring interaction within the assembled basal body.

Original language	English
Pages (from-to)	161-172
Number of pages	12
Journal	Structure
Volume	23
Issue number	1
DOIs	https://doi.org/10.1016/j.str.2014.10.021
Publication status	Published - 6 Jan 2015

Keywords

Bacterial Proteins/chemistry
Basal Bodies/chemistry
Membrane Microdomains/chemistry
Membrane Proteins/chemistry
Models, Molecular
Protein Multimerization
Protein Structure, Secondary
Salmonella typhimurium
Secretory Pathway
Secretory Vesicles/chemistry

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10.1016/j.str.2014.10.021

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Bergeron, J. R. C., Worrall, L. J., De, S., Sgourakis, N. G., Cheung, A. H., Lameignere, E., Okon, M., Wasney, G. A., Baker, D., McIntosh, L. P., & Strynadka, N. C. J. (2015). The modular structure of the inner-membrane ring component PrgK facilitates assembly of the type III secretion system basal body. Structure, 23(1), 161-172. https://doi.org/10.1016/j.str.2014.10.021

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title = "The modular structure of the inner-membrane ring component PrgK facilitates assembly of the type III secretion system basal body",

abstract = "The type III secretion system (T3SS) is a large macromolecular assembly found at the surface of many pathogenic Gram-negative bacteria. Its role is to inject toxic {"}effector{"} proteins into the cells of infected organisms. The molecular details of the assembly of this large, multimembrane-spanning complex remain poorly understood. Here, we report structural, biochemical, and functional analyses of PrgK, an inner-membrane component of the prototypical Salmonella typhimurium T3SS. We have obtained the atomic structures of the two ring building globular domains and show that the C-terminal transmembrane helix is not essential for assembly and secretion. We also demonstrate that structural rearrangement of the two PrgK globular domains, driven by an interconnecting linker region, may promote oligomerization into ring structures. Finally, we used electron microscopy-guided symmetry modeling to propose a structural model for the intimately associated PrgH-PrgK ring interaction within the assembled basal body. ",

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AU - Bergeron, Julien R C

AU - Worrall, Liam J

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AU - Sgourakis, Nikolaos G

AU - Cheung, Adrienne H

AU - Lameignere, Emilie

AU - Okon, Mark

AU - Wasney, Gregory A

AU - Baker, David

AU - McIntosh, Lawrence P

AU - Strynadka, Natalie C J

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N2 - The type III secretion system (T3SS) is a large macromolecular assembly found at the surface of many pathogenic Gram-negative bacteria. Its role is to inject toxic "effector" proteins into the cells of infected organisms. The molecular details of the assembly of this large, multimembrane-spanning complex remain poorly understood. Here, we report structural, biochemical, and functional analyses of PrgK, an inner-membrane component of the prototypical Salmonella typhimurium T3SS. We have obtained the atomic structures of the two ring building globular domains and show that the C-terminal transmembrane helix is not essential for assembly and secretion. We also demonstrate that structural rearrangement of the two PrgK globular domains, driven by an interconnecting linker region, may promote oligomerization into ring structures. Finally, we used electron microscopy-guided symmetry modeling to propose a structural model for the intimately associated PrgH-PrgK ring interaction within the assembled basal body.

AB - The type III secretion system (T3SS) is a large macromolecular assembly found at the surface of many pathogenic Gram-negative bacteria. Its role is to inject toxic "effector" proteins into the cells of infected organisms. The molecular details of the assembly of this large, multimembrane-spanning complex remain poorly understood. Here, we report structural, biochemical, and functional analyses of PrgK, an inner-membrane component of the prototypical Salmonella typhimurium T3SS. We have obtained the atomic structures of the two ring building globular domains and show that the C-terminal transmembrane helix is not essential for assembly and secretion. We also demonstrate that structural rearrangement of the two PrgK globular domains, driven by an interconnecting linker region, may promote oligomerization into ring structures. Finally, we used electron microscopy-guided symmetry modeling to propose a structural model for the intimately associated PrgH-PrgK ring interaction within the assembled basal body.

KW - Bacterial Proteins/chemistry

KW - Basal Bodies/chemistry

KW - Membrane Microdomains/chemistry

KW - Membrane Proteins/chemistry

KW - Models, Molecular

KW - Protein Multimerization

KW - Protein Structure, Secondary

KW - Salmonella typhimurium

KW - Secretory Pathway

KW - Secretory Vesicles/chemistry

U2 - 10.1016/j.str.2014.10.021

DO - 10.1016/j.str.2014.10.021

M3 - Article

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SN - 0969-2126

VL - 23

SP - 161

EP - 172

JO - Structure

JF - Structure

IS - 1

ER -

The modular structure of the inner-membrane ring component PrgK facilitates assembly of the type III secretion system basal body

Abstract

Keywords

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