Salmonella Typhimurium discreet-invasion of the murine gut absorptive epithelium.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
05 2020
Historique:
received: 18 01 2020
accepted: 26 03 2020
revised: 14 05 2020
pubmed: 5 5 2020
medline: 22 7 2020
entrez: 5 5 2020
Statut: epublish

Résumé

Salmonella enterica serovar Typhimurium (S.Tm) infections of cultured cell lines have given rise to the ruffle model for epithelial cell invasion. According to this model, the Type-Three-Secretion-System-1 (TTSS-1) effectors SopB, SopE and SopE2 drive an explosive actin nucleation cascade, resulting in large lamellipodia- and filopodia-containing ruffles and cooperative S.Tm uptake. However, cell line experiments poorly recapitulate many of the cell and tissue features encountered in the host's gut mucosa. Here, we employed bacterial genetics and multiple imaging modalities to compare S.Tm invasion of cultured epithelial cell lines and the gut absorptive epithelium in vivo in mice. In contrast to the prevailing ruffle-model, we find that absorptive epithelial cell entry in the mouse gut occurs through "discreet-invasion". This distinct entry mode requires the conserved TTSS-1 effector SipA, involves modest elongation of local microvilli in the absence of expansive ruffles, and does not favor cooperative invasion. Discreet-invasion preferentially targets apicolateral hot spots at cell-cell junctions and shows strong dependence on local cell neighborhood. This proof-of-principle evidence challenges the current model for how S.Tm can enter gut absorptive epithelial cells in their intact in vivo context.

Identifiants

pubmed: 32365138
doi: 10.1371/journal.ppat.1008503
pii: PPATHOGENS-D-20-00095
pmc: PMC7224572
doi:

Substances chimiques

Bacterial Proteins 0
Guanine Nucleotide Exchange Factors 0
Microfilament Proteins 0
SipA protein, Salmonella 0
SopE protein, Salmonella 0
SopE2 protein, Salmonella typhimurium 0
Type I Secretion Systems 0
SopB protein, Salmonella EC 3.4.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1008503

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Microbiology. 2011 Mar;157(Pt 3):839-847
pubmed: 21109565
EMBO J. 2001 May 1;20(9):2131-9
pubmed: 11331579
Infect Immun. 2002 Jul;70(7):3843-55
pubmed: 12065528
Vet Pathol. 1997 Sep;34(5):369-86
pubmed: 9381648
Nature. 2013 Apr 11;496(7444):233-7
pubmed: 23542589
Gene Expr Patterns. 2010 Oct-Dec;10(7-8):345-50
pubmed: 20723621
Cell Host Microbe. 2014 Aug 13;16(2):249-256
pubmed: 25121752
Cell Host Microbe. 2015 Feb 11;17(2):164-77
pubmed: 25600187
Cell Host Microbe. 2012 Jan 19;11(1):19-32
pubmed: 22264510
PLoS Biol. 2008 Apr 8;6(4):e74
pubmed: 18399718
Mucosal Immunol. 2020 May;13(3):530-544
pubmed: 31953493
Cell Microbiol. 2010 Jan;12(1):84-98
pubmed: 19732055
Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9845-50
pubmed: 10449782
Cell Microbiol. 2015 Nov;17(11):1561-9
pubmed: 26294173
Infect Immun. 2010 Jun;78(6):2700-13
pubmed: 20368348
Am J Physiol. 1996 Jun;270(6 Pt 1):C1666-74
pubmed: 8764149
Nat Microbiol. 2018 Oct;3(10):1122-1130
pubmed: 30224799
Cell. 1998 May 29;93(5):815-26
pubmed: 9630225
Methods Mol Biol. 2017;1615:353-375
pubmed: 28667625
mBio. 2013 Mar 05;4(2):
pubmed: 23462113
J Bacteriol. 2000 Apr;182(8):2341-4
pubmed: 10735884
PLoS Pathog. 2018 Mar 9;14(3):e1006925
pubmed: 29522566
J Bacteriol. 2001 Apr;183(7):2348-58
pubmed: 11244077
J Immunol. 2005 Feb 1;174(3):1675-85
pubmed: 15661931
J Struct Biol. 2007 Jan;157(1):138-47
pubmed: 16904341
Cell Microbiol. 2009 Mar;11(3):475-87
pubmed: 19046340
J Cell Biol. 2006 Nov 6;175(3):453-63
pubmed: 17074883
Nature. 2004 Jul 8;430(6996):213-8
pubmed: 15190255
Nat Rev Cancer. 2002 Feb;2(2):133-42
pubmed: 12635176
Ultramicroscopy. 2018 Jul;190:1-11
pubmed: 29655973
Cell Microbiol. 2006 Dec;8(12):1946-57
pubmed: 16869830
Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12283-8
pubmed: 11050248
Cell Microbiol. 2014 Dec;16(12):1723-35
pubmed: 25052734
Cell Microbiol. 2007 Jul;9(7):1834-50
pubmed: 17388786
Immunol Rev. 2012 Jan;245(1):56-83
pubmed: 22168414
Proc Natl Acad Sci U S A. 2010 Oct 12;107(41):17733-8
pubmed: 20876119
PLoS Pathog. 2012;8(7):e1002810
pubmed: 22911370
Mol Microbiol. 2000 Jun;36(6):1206-21
pubmed: 10931274
Nature. 1981 May 21;291(5812):238-9
pubmed: 7015147
PLoS Pathog. 2014 Sep 11;10(9):e1004385
pubmed: 25210785
Cell Microbiol. 2008 Nov;10(11):2364-76
pubmed: 18671822
Cell Host Microbe. 2009 Aug 20;6(2):125-36
pubmed: 19683679
EMBO J. 1999 Sep 15;18(18):4926-34
pubmed: 10487745
Cell Host Microbe. 2017 Apr 12;21(4):443-454
pubmed: 28407482
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Infect Immun. 2003 May;71(5):2839-58
pubmed: 12704158
Mol Microbiol. 2001 Jan;39(2):248-59
pubmed: 11136447
Mol Microbiol. 2002 Mar;43(5):1089-103
pubmed: 11918798
Proc Natl Acad Sci U S A. 2005 Aug 30;102(35):12548-53
pubmed: 16107539
J Microsc. 2008 May;230(Pt 2):212-7
pubmed: 18445149
Vet Pathol. 2002 Mar;39(2):200-15
pubmed: 12009058
Mol Microbiol. 2019 Oct;112(4):1270-1283
pubmed: 31370104
Nat Cell Biol. 2002 Oct;4(10):766-73
pubmed: 12360287
PLoS One. 2016 Sep 14;11(9):e0161965
pubmed: 27627128
Am J Pathol. 1967 Jan;50(1):109-36
pubmed: 5334433
Cell Rep. 2019 May 28;27(9):2665-2678.e3
pubmed: 31141690
Vet Pathol. 2003 Jul;40(4):371-5
pubmed: 12824508
Cell Host Microbe. 2007 Mar 15;1(1):63-75
pubmed: 18005682
Cell Host Microbe. 2012 Feb 16;11(2):129-39
pubmed: 22341462
mBio. 2017 Dec 5;8(6):
pubmed: 29208746
Cell Microbiol. 2002 Jun;4(6):357-65
pubmed: 12116966
Curr Opin Microbiol. 2006 Feb;9(1):46-54
pubmed: 16406778
Cell Microbiol. 2018 Apr;20(4):
pubmed: 29250873
Infect Immun. 2005 Jan;73(1):146-54
pubmed: 15618149
Mol Microbiol. 1997 May;24(4):747-56
pubmed: 9194702
Cell Microbiol. 2018 Oct;20(10):e12938
pubmed: 30010242
Mol Cell. 2004 Feb 27;13(4):497-510
pubmed: 14992720
Infect Immun. 2014 Jun;82(6):2657-67
pubmed: 24711567
mBio. 2012 Jun 12;3(3):
pubmed: 22691391
Proc Natl Acad Sci U S A. 1989 Aug;86(16):6383-7
pubmed: 2548211
Trends Microbiol. 1998 Sep;6(9):359-65
pubmed: 9778729
Mol Microbiol. 1996 Oct;22(2):327-38
pubmed: 8930917
Int J Med Microbiol. 2000 Dec;290(7):605-17
pubmed: 11200542
Science. 1999 Mar 26;283(5410):2092-5
pubmed: 10092234
Front Cell Infect Microbiol. 2017 Aug 09;7:348
pubmed: 28848711
Mol Syst Biol. 2011 Mar 15;7:474
pubmed: 21407211
Infect Immun. 2004 Feb;72(2):795-809
pubmed: 14742523
PLoS Med. 2015 Dec 03;12(12):e1001921
pubmed: 26633831
Cell Microbiol. 2001 Jun;3(6):417-26
pubmed: 11422084
Cell Host Microbe. 2014 Aug 13;16(2):237-248
pubmed: 25121751
mBio. 2019 May 21;10(3):
pubmed: 31113898
Cell Microbiol. 2014 Jan;16(1):64-77
pubmed: 23931152

Auteurs

Stefan A Fattinger (SA)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.
Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

Desirée Böck (D)

Institute of Molecular Biology & Biophysics, Department of Biology, ETH Zürich, Zürich, Switzerland.

Maria Letizia Di Martino (ML)

Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

Sabrina Deuring (S)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.

Pilar Samperio Ventayol (P)

Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

Viktor Ek (V)

Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

Markus Furter (M)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.

Saskia Kreibich (S)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.

Francesco Bosia (F)

Institute of Molecular Biology & Biophysics, Department of Biology, ETH Zürich, Zürich, Switzerland.

Anna A Müller-Hauser (AA)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.

Bidong D Nguyen (BD)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.

Manfred Rohde (M)

Central Facility for Microscopy, Helmholtz Centre for Infection Research, Braunschweig, Germany.

Martin Pilhofer (M)

Institute of Molecular Biology & Biophysics, Department of Biology, ETH Zürich, Zürich, Switzerland.

Wolf-Dietrich Hardt (WD)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.

Mikael E Sellin (ME)

Institute of Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland.
Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

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