TLR4 signaling and macrophage inflammatory responses are dampened by GIV/Girdin.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
27 10 2020
Historique:
pubmed: 16 10 2020
medline: 18 12 2020
entrez: 15 10 2020
Statut: ppublish

Résumé

Sensing of pathogens by Toll-like receptor 4 (TLR4) induces an inflammatory response; controlled responses confer immunity but uncontrolled responses cause harm. Here we define how a multimodular scaffold, GIV (a.k.a. Girdin), titrates such inflammatory response in macrophages. Upon challenge with either live microbes or microbe-derived lipopolysaccharides (a ligand for TLR4), macrophages with GIV mount a more tolerant (hypo-reactive) transcriptional response and suppress proinflammatory cytokines and signaling pathways (i.e., NFkB and CREB) downstream of TLR4 compared to their GIV-depleted counterparts. Myeloid-specific gene-depletion studies confirmed that the presence of GIV ameliorates dextran sodium sulfate-induced colitis and sepsis-induced death. The antiinflammatory actions of GIV are mediated via its C-terminally located TIR-like BB-loop (TILL) motif which binds the cytoplasmic TIR modules of TLR4 in a manner that precludes receptor dimerization; such dimerization is a prerequisite for proinflammatory signaling. Binding of GIV's TILL motif to TIR modules inhibits proinflammatory signaling via other TLRs, suggesting a convergent paradigm for fine-tuning macrophage inflammatory responses.

Identifiants

pubmed: 33055214
pii: 2011667117
doi: 10.1073/pnas.2011667117
pmc: PMC7604444
doi:

Substances chimiques

Ccdc88a protein, mouse 0
Microfilament Proteins 0
Tlr4 protein, mouse 0
Toll-Like Receptor 4 0
Vesicular Transport Proteins 0
girdin protein, mouse 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

26895-26906

Subventions

Organisme : NCI NIH HHS
ID : R01 CA238042
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001442
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA100768
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA160911
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI155696
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI118985
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK107585
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI141630
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK007202
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA023100
Pays : United States

Déclaration de conflit d'intérêts

The authors declare no competing interest.

Références

J Mol Biol. 2014 Sep 23;426(19):3305-3313
pubmed: 25088687
J Biol Chem. 2013 Apr 26;288(17):12054-66
pubmed: 23460645
Infect Immun. 2008 Aug;76(8):3360-73
pubmed: 18474643
Mol Cell Biol. 2003 Apr;23(7):2543-55
pubmed: 12640135
Nat Rev Immunol. 2009 Aug;9(8):556-67
pubmed: 19575028
Bioessays. 2016 Apr;38(4):379-93
pubmed: 26879989
J Immunol. 2006 Feb 15;176(4):2219-28
pubmed: 16455978
Nat Rev Mol Cell Biol. 2015 Jan;16(1):18-29
pubmed: 25531225
Proteins. 1997;Suppl 1:29-37
pubmed: 9485492
J Biomed Sci. 2019 Jun 12;26(1):46
pubmed: 31189465
PLoS One. 2011;6(8):e23989
pubmed: 21897866
Mol Nutr Food Res. 2018 Apr;62(7):e1700931
pubmed: 29336524
PLoS One. 2007 Aug 29;2(8):e788
pubmed: 17726518
Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):14966-71
pubmed: 19706440
J Immunol. 2017 Feb 1;198(3):1006-1014
pubmed: 28115590
Nature. 2000 Nov 2;408(6808):111-5
pubmed: 11081518
J Immunol. 2008 May 1;180(9):5771-7
pubmed: 18424693
Proc Natl Acad Sci U S A. 2016 Sep 27;113(39):E5721-30
pubmed: 27621449
Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10260-5
pubmed: 19506249
Am J Physiol Cell Physiol. 2005 Aug;289(2):C293-301
pubmed: 15788486
Front Immunol. 2018 Nov 27;9:2764
pubmed: 30542349
Cytokine. 2008 May;42(2):145-151
pubmed: 18304834
Science. 2017 May 5;356(6337):513-519
pubmed: 28473584
J Biol Chem. 2015 Mar 13;290(11):6697-704
pubmed: 25605737
Immunol Rev. 2018 Sep;285(1):147-167
pubmed: 30129209
Annu Rev Physiol. 2017 Feb 10;79:541-566
pubmed: 27813830
Cell Cycle. 2015;14(16):2561-5
pubmed: 26126131
Cell Mol Gastroenterol Hepatol. 2015 Apr 1;1(3):311-324
pubmed: 26878033
J Clin Med. 2016 Dec 17;5(12):
pubmed: 27999328
Sci Signal. 2009 Jun 16;2(75):pe37
pubmed: 19531801
Trends Immunol. 2005 Sep;26(9):469-76
pubmed: 16006187
Cell Cycle. 2017 Apr 3;16(7):607-612
pubmed: 28287365
J Biol Chem. 2008 May 2;283(18):11861-5
pubmed: 18332149
Front Immunol. 2018 Jan 30;9:87
pubmed: 29441068
J Biol Chem. 2012 Feb 3;287(6):4088-98
pubmed: 22139835
Front Immunol. 2019 Aug 27;10:2031
pubmed: 31507616
Br J Pharmacol. 2005 Aug;145(8):1093-102
pubmed: 15937518
Front Immunol. 2015 Dec 07;6:613
pubmed: 26697009
J Endotoxin Res. 2002;8(6):427-35
pubmed: 12701623
Shock. 2003 Nov;20(5):386-401
pubmed: 14560102
Nat Rev Gastroenterol Hepatol. 2019 Sep;16(9):531-543
pubmed: 31312042
PLoS One. 2012;7(9):e45466
pubmed: 23029029
J Vis Exp. 2013 Jun 23;(76):
pubmed: 23851980
Transgenic Res. 1999 Aug;8(4):265-77
pubmed: 10621974
Mol Biol Cell. 2019 Jun 15;30(13):1621-1633
pubmed: 31017840
Mol Biol Cell. 2010 Jul 1;21(13):2338-54
pubmed: 20462955
J Mol Biol. 1994 Jan 21;235(3):983-1002
pubmed: 8289329
J Vis Exp. 2012 Feb 01;(60):
pubmed: 22331082
Nature. 2013 Apr 25;496(7446):445-55
pubmed: 23619691
iScience. 2020 Jun 26;23(6):101209
pubmed: 32535026
Biochem Biophys Res Commun. 2012 Oct 5;426(4):533-8
pubmed: 22974978
PLoS Pathog. 2007 Apr;3(4):e60
pubmed: 17465679
Nat Struct Mol Biol. 2017 Sep;24(9):743-751
pubmed: 28759049
Am J Physiol Heart Circ Physiol. 2011 Dec;301(6):H2246-53
pubmed: 21949112
Science. 1998 Dec 11;282(5396):2085-8
pubmed: 9851930
Front Immunol. 2019 May 24;10:1084
pubmed: 31178859
Mol Immunol. 2010 Apr;47(7-8):1396-403
pubmed: 20303596

Auteurs

Lee Swanson (L)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Gajanan D Katkar (GD)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Julian Tam (J)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Rama F Pranadinata (RF)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Yogitha Chareddy (Y)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Jane Coates (J)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Mahitha Shree Anandachar (MS)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Vanessa Castillo (V)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093.

Joshua Olson (J)

Department of Pediatrics, University of California San Diego, La Jolla, CA 92093.

Victor Nizet (V)

Department of Pediatrics, University of California San Diego, La Jolla, CA 92093.
Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA 92093.

Irina Kufareva (I)

Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA 92093.

Soumita Das (S)

Department of Pathology, University of California San Diego, La Jolla, CA 92093.

Pradipta Ghosh (P)

Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093; prghosh@ucsd.edu.
Department of Medicine, University of California San Diego, La Jolla, CA 92093.

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Classifications MeSH