Literature DB >> 27466361

Secretion of the Intimin Passenger Domain Is Driven by Protein Folding.

Jack C Leo1, Philipp Oberhettinger2, Shogo Yoshimoto3, D B R K Gupta Udatha1, J Preben Morth4, Monika Schütz2, Katsutoshi Hori3, Dirk Linke5.   

Abstract

Intimin is an essential adhesin of attaching and effacing organisms such as entropathogenic Escherichia coli It is also the prototype of type Ve secretion or inverse autotransport, where the extracellular C-terminal region or passenger is exported with the help of an N-terminal transmembrane β-barrel domain. We recently reported a stalled secretion intermediate of intimin, where the passenger is located in the periplasm but the β-barrel is already inserted into the membrane. Stalling of this mutant is due to the insertion of an epitope tag at the very N terminus of the passenger. Here, we examined how this insertion disrupts autotransport and found that it causes misfolding of the N-terminal immunoglobulin (Ig)-like domain D00. We could also stall the secretion by making an internal deletion in D00, and introducing the epitope tag into the second Ig-like domain, D0, also resulted in reduced passenger secretion. In contrast to many classical autotransporters, where a proximal folding core in the passenger is required for secretion, the D00 domain is dispensable, as the passenger of an intimin mutant lacking D00 entirely is efficiently exported. Furthermore, the D00 domain is slightly less stable than the D0 and D1 domains, unfolding at ∼200 piconewtons (pN) compared with ∼250 pN for D0 and D1 domains as measured by atomic force microscopy. Our results support a model where the secretion of the passenger is driven by sequential folding of the extracellular Ig-like domains, leading to vectorial transport of the passenger domain across the outer membrane in an N to C direction.
© 2016 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  atomic force microscopy (AFM); bacterial pathogenesis; immunoglobulin-like domain; protein folding; protein secretion; type V secretion system

Mesh:

Substances:

Year:  2016        PMID: 27466361      PMCID: PMC5025694          DOI: 10.1074/jbc.M116.731497

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  46 in total

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Authors:  Denisse L Leyton; Amanda E Rossiter; Ian R Henderson
Journal:  Nat Rev Microbiol       Date:  2012-02-16       Impact factor: 60.633

2.  Assessing the Outer Membrane Insertion and Folding of Multimeric Transmembrane β-Barrel Proteins.

Authors:  Jack C Leo; Philipp Oberhettinger; Dirk Linke
Journal:  Methods Mol Biol       Date:  2015

3.  Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins.

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Journal:  Proc Natl Acad Sci U S A       Date:  2006-03-20       Impact factor: 11.205

4.  Role of periplasmic chaperones and BamA (YaeT/Omp85) in folding and secretion of intimin from enteropathogenic Escherichia coli strains.

Authors:  Gustavo Bodelón; Elvira Marín; Luis Angel Fernández
Journal:  J Bacteriol       Date:  2009-06-12       Impact factor: 3.490

Review 5.  Two-partner secretion: as simple as it sounds?

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Review 6.  Of linkers and autochaperones: an unambiguous nomenclature to identify common and uncommon themes for autotransporter secretion.

Authors:  Igor Drobnak; Esther Braselmann; Julie L Chaney; Denisse L Leyton; Harris D Bernstein; Trevor Lithgow; Joen Luirink; James P Nataro; Patricia L Clark
Journal:  Mol Microbiol       Date:  2014-11-24       Impact factor: 3.501

7.  Protein production by auto-induction in high density shaking cultures.

Authors:  F William Studier
Journal:  Protein Expr Purif       Date:  2005-05       Impact factor: 1.650

8.  The bacterial intimins and invasins: a large and novel family of secreted proteins.

Authors:  Jennifer C Tsai; Ming-Ren Yen; Rostislav Castillo; Denisse L Leyton; Ian R Henderson; Milton H Saier
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9.  Kalign--an accurate and fast multiple sequence alignment algorithm.

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Journal:  BMC Bioinformatics       Date:  2005-12-12       Impact factor: 3.169

10.  LOMETS: a local meta-threading-server for protein structure prediction.

Authors:  Sitao Wu; Yang Zhang
Journal:  Nucleic Acids Res       Date:  2007-05-03       Impact factor: 16.971

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Review 2.  Phylogenetic Classification and Functional Review of Autotransporters.

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3.  The extracellular juncture domains in the intimin passenger adopt a constitutively extended conformation inducing restraints to its sphere of action.

Authors:  Julia Weikum; Alina Kulakova; Giulio Tesei; Shogo Yoshimoto; Line Vejby Jægerum; Monika Schütz; Katsutoshi Hori; Marie Skepö; Pernille Harris; Jack C Leo; J Preben Morth
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4.  A New Strain Collection for Improved Expression of Outer Membrane Proteins.

Authors:  Ina Meuskens; Marcin Michalik; Nandini Chauhan; Dirk Linke; Jack C Leo
Journal:  Front Cell Infect Microbiol       Date:  2017-11-07       Impact factor: 5.293

5.  Evolving Accelerated Amidation by SpyTag/SpyCatcher to Analyze Membrane Dynamics.

Authors:  Anthony H Keeble; Anusuya Banerjee; Matteo P Ferla; Samuel C Reddington; Irsyad N A Khairil Anuar; Mark Howarth
Journal:  Angew Chem Int Ed Engl       Date:  2017-12-05       Impact factor: 15.336

Review 6.  Catching a SPY: Using the SpyCatcher-SpyTag and Related Systems for Labeling and Localizing Bacterial Proteins.

Authors:  Daniel Hatlem; Thomas Trunk; Dirk Linke; Jack C Leo
Journal:  Int J Mol Sci       Date:  2019-04-30       Impact factor: 5.923

Review 7.  Folding Control in the Path of Type 5 Secretion.

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Journal:  Toxins (Basel)       Date:  2021-05-11       Impact factor: 4.546

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