The Shigella type III effector IpgD recodes Ca 2+ signals during invasion of epithelial cells

Autor: Ceren Simsek, Christophe Erneux, Benjamin Wacquier, Alexandre Lehman, Daniel I Aguilar, Philippe J. Sansonetti, Laurence Arbibe, Sylviane Boucherie, Kevin Denis, Guy Tran Van Nhieu, Chun Hui Sun, Geneviève Dupont, Cesar Valencia-Gallardo, Laurent Combettes, Jost Enninga, Nathalie Carayol
Přispěvatelé: Centre interdisciplinaire de recherche en biologie (CIRB), Labex MemoLife, École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI Paris), Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM), Intéractions cellulaires et physiopathologie hépathique (Orsay, Essonne) UMRS 1174 (ICPH ), Institut National de la Santé et de la Recherche Médicale (INSERM), Unité de Chronobiologie Théorique [Brussels, Belgium], Université libre de Bruxelles (ULB), Interdisciplinary Research Institute [Brussels, Belgium] (IRIBHM), Dynamique des Interactions Hôte-Pathogène - Dynamics of Host-Pathogen Interactions, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Institut Necker Enfants-Malades (INEM - UM 111 (UMR 8253 / U1151)), Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université Paris Descartes - Paris 5 (UPD5), Pathogénie microbienne moléculaire, Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Chaire Microbiologie et Maladies infectieuses, Collège de France (CdF (institution)), Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution)), The work was supported by the ANR grants MITOPATHO and PATHIMMUN, grant from Tournesol program No. 31268YG, and grants from the Labex Memolife and PSL IDEX Shigaforce. CHS is a recipient of a PhD grant from the China Scholarship Council. DA is a recipient of a CONACYT grant and Labex Memolife. CV‐G was a recipient of the PSL IDEX grant. NC is a recipient of a Marie‐Curie IRG grant. BW and GD are Research Fellow and Research Director at the Belgian F.R.S.‐F.N.R.S., respectively. This work was supported by the Fonds de la Recherche Scientifique‐FNRS under Grant No. J0043.14 and by the Fonds David and Alice Van Buuren. JE was supported by an ERC Starting ('Rupteffects' No. 261166) and a Consolidator Grant ('Endosubvert' No. 682809). LC, GD, and GTVN are recipients of a WBI‐France Exchange Program (Wallonie‐Bruxelles International, Fonds de la Recherche Scientifique, Ministère Français des Affaires étrangères et européennes, Ministère de l'Enseignement supérieur et de la Recherche dans le cadre des Partenariats Hubert Curien)., ANR-12-BSV3-0017,MITOPATHO,Rôle des mitochondries durant l'invasion des cellules par les bactéries Listeria et Shigella(2012), ANR-10-MIDI-0007,PATHIMMUN,Les pathogènes nous enseignent de nouvelles stratégies antiinflammatoires(2010), ANR-10-IDEX-0001,PSL,Paris Sciences et Lettres(2010), European Project: 261166,EC:FP7:ERC,ERC-2010-StG_20091118,RUPTEFFECTS(2011), European Project: 682809,EndoSubvert(2017), Langlais, Laurence, BLANC - Rôle des mitochondries durant l'invasion des cellules par les bactéries Listeria et Shigella - - MITOPATHO2012 - ANR-12-BSV3-0017 - BLANC - VALID, MECANISMES INTEGRES DE L'INFLAMMATION - Les pathogènes nous enseignent de nouvelles stratégies antiinflammatoires - - PATHIMMUN2010 - ANR-10-MIDI-0007 - MI2 - VALID, Initiative d'excellence - Paris Sciences et Lettres - - PSL2010 - ANR-10-IDEX-0001 - IDEX - VALID, Revealing the mechanism of host membrane rupture by invasive pathogens and its role in triggering the immune response - RUPTEFFECTS - - EC:FP7:ERC2011-03-01 - 2016-02-29 - 261166 - VALID, Common mechanisms of host membrane trafficking subversion by intracellular pathogens to rupture bacterial containing vacuoles - EndoSubvert - 2017-01-01 - 2021-12-31 - 682809 - VALID, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI Paris), Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM), Collège de France - Chaire Microbiologie et Maladies infectieuses, Université Paris sciences et lettres (PSL)
Jazyk: angličtina
Rok vydání: 2017
Předmět:
0301 basic medicine
MESH: Signal Transduction
MESH: Shigella flexneri
MESH: Calpain
Cell
Regulator
[SDV.BC.IC] Life Sciences [q-bio]/Cellular Biology/Cell Behavior [q-bio.CB]
Shigella flexneri
[SDV.BC.IC]Life Sciences [q-bio]/Cellular Biology/Cell Behavior [q-bio.CB]
[SDV.BBM.BC] Life Sciences [q-bio]/Biochemistry
Molecular Biology/Biochemistry [q-bio.BM]
MESH: Bacterial Proteins
biology
Effector
General Neuroscience
Calpain
Articles
Cell biology
Phosphotransferases (Alcohol Group Acceptor)
medicine.anatomical_structure
MESH: Calcium
Host-Pathogen Interactions
Second messenger system
MESH: Phosphoric Monoester Hydrolases
IpgD
medicine.symptom
calpain
Signal Transduction
Programmed cell death
MESH: Dysentery
Bacillary
Inflammation
General Biochemistry
Genetics and Molecular Biology
MESH: Cell Adhesion
03 medical and health sciences
Bacterial Proteins
Cell Adhesion
medicine
Humans
[SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Biochemistry [q-bio.BM]
Cell adhesion
Molecular Biology
Dysentery
Bacillary
calcium
MESH: Humans
General Immunology and Microbiology
talin
MESH: Host-Pathogen Interactions
MESH: Phosphotransferases (Alcohol Group Acceptor)
Phosphoric Monoester Hydrolases
030104 developmental biology
MESH: HeLa Cells
biology.protein
Shigella
HeLa Cells
Zdroj: EMBO Journal
EMBO Journal, EMBO Press, 2017, 36 (17), pp.2567-2580. ⟨10.15252/embj.201696272⟩
The EMBO Journal
EMBO Journal, 2017, 36 (17), pp.2567-2580. ⟨10.15252/embj.201696272⟩
ISSN: 0261-4189
1460-2075
DOI: 10.15252/embj.201696272⟩
Popis: The role of second messengers in the diversion of cellular processes by pathogens remains poorly studied despite their importance. Among these, Ca 2+ virtually regulates all known cell processes, including cytoskeletal reorganization, inflammation, or cell death pathways. Under physiological conditions, cytosolic Ca 2+ increases are transient and oscillatory, defining the so‐called Ca 2+ code that links cell responses to specific Ca 2+ oscillatory patterns. During cell invasion, Shigella induces atypical local and global Ca 2+ signals. Here, we show that by hydrolyzing phosphatidylinositol‐(4,5)bisphosphate, the Shigella type III effector IpgD dampens inositol‐(1,4,5)trisphosphate (InsP 3 ) levels. By modifying InsP 3 dynamics and diffusion, IpgD favors the elicitation of long‐lasting local Ca 2+ signals at Shigella invasion sites and converts Shigella ‐induced global oscillatory responses into erratic responses with atypical dynamics and amplitude. Furthermore, IpgD eventually inhibits InsP 3 ‐dependent responses during prolonged infection kinetics. IpgD thus acts as a pathogen regulator of the Ca 2+ code implicated in a versatility of cell functions. Consistent with this function, IpgD prevents the Ca 2+ ‐dependent activation of calpain, thereby preserving the integrity of cell adhesion structures during the early stages of infection.
Databáze: OpenAIRE
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