Human TBK1 deficiency leads to autoinflammation driven by TNF-induced cell death.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
19 08 2021
Historique:
received: 23 12 2020
revised: 11 05 2021
accepted: 20 07 2021
pubmed: 8 8 2021
medline: 6 1 2022
entrez: 7 8 2021
Statut: ppublish

Résumé

TANK binding kinase 1 (TBK1) regulates IFN-I, NF-κB, and TNF-induced RIPK1-dependent cell death (RCD). In mice, biallelic loss of TBK1 is embryonically lethal. We discovered four humans, ages 32, 26, 7, and 8 from three unrelated consanguineous families with homozygous loss-of-function mutations in TBK1. All four patients suffer from chronic and systemic autoinflammation, but not severe viral infections. We demonstrate that TBK1 loss results in hypomorphic but sufficient IFN-I induction via RIG-I/MDA5, while the system retains near intact IL-6 induction through NF-κB. Autoinflammation is driven by TNF-induced RCD as patient-derived fibroblasts experienced higher rates of necroptosis in vitro, and CC3 was elevated in peripheral blood ex vivo. Treatment with anti-TNF dampened the baseline circulating inflammatory profile and ameliorated the clinical condition in vivo. These findings highlight the plasticity of the IFN-I response and underscore a cardinal role for TBK1 in the regulation of RCD.

Identifiants

pubmed: 34363755
pii: S0092-8674(21)00885-0
doi: 10.1016/j.cell.2021.07.026
pmc: PMC8380741
mid: NIHMS1727837
pii:
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Cytokines 0
Interferon Type I 0
MAVS protein, human 0
Receptors, Pattern Recognition 0
Toll-Like Receptor 3 0
Tumor Necrosis Factor-alpha 0
Interferon-gamma 82115-62-6
Protein Serine-Threonine Kinases EC 2.7.11.1
RIPK1 protein, human EC 2.7.11.1
Receptor-Interacting Protein Serine-Threonine Kinases EC 2.7.11.1
TBK1 protein, human EC 2.7.11.1
I-kappa B Kinase EC 2.7.11.10
CYLD protein, human EC 3.4.19.12
Deubiquitinating Enzyme CYLD EC 3.4.19.12

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

4447-4463.e20

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI127372
Pays : United States
Organisme : NIAID NIH HHS
ID : F31 AI138363
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI007647
Pays : United States
Organisme : Medical Research Council
ID : MR/S032304/1
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : R01 AI151029
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI052417
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI148963
Pays : United States

Informations de copyright

Copyright © 2021 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests D.B. is the founder of Lab11 Therapeutics.

Références

Trends Mol Med. 2016 Jun;22(6):511-527
pubmed: 27211305
Proc Natl Acad Sci U S A. 2018 Jun 26;115(26):E5944-E5953
pubmed: 29891719
Nature. 2003 Aug 14;424(6950):801-5
pubmed: 12917691
Nature. 2003 Aug 14;424(6950):797-801
pubmed: 12917690
Science. 2009 Jul 17;325(5938):332-6
pubmed: 19498109
Nat Immunol. 2003 May;4(5):491-6
pubmed: 12692549
Mol Cell. 2014 Apr 10;54(1):133-146
pubmed: 24703947
J Virol. 2004 Oct;78(19):10636-49
pubmed: 15367631
J Immunol. 2014 Aug 15;193(4):1539-1543
pubmed: 25015821
J Exp Med. 2020 Jan 6;217(1):
pubmed: 31611248
J Exp Med. 2017 May 1;214(5):1493-1507
pubmed: 28356390
Cell Mol Immunol. 2019 Oct;16(10):800-809
pubmed: 29973649
J Clin Immunol. 2020 Jan;40(1):24-64
pubmed: 31953710
Cell Death Dis. 2020 Feb 5;11(2):94
pubmed: 32024820
J Immunol. 2017 Nov 1;199(9):3222-3233
pubmed: 28939760
Science. 2018 Aug 24;361(6404):810-813
pubmed: 30026316
Nat Methods. 2016 Feb;13(2):109-10
pubmed: 26820543
Cold Spring Harb Protoc. 2016 Mar 01;2016(3):pdb.prot087403
pubmed: 26933246
Nat Commun. 2017 Feb 10;8:14391
pubmed: 28186168
EMBO J. 2000 Sep 15;19(18):4976-85
pubmed: 10990461
Nature. 2020 May;581(7809):434-443
pubmed: 32461654
Science. 2011 Sep 16;333(6049):1593-602
pubmed: 21835983
Cells. 2018 Aug 13;7(8):
pubmed: 30104535
Nature. 2015 Jan 1;517(7532):89-93
pubmed: 25307056
Nat Immunol. 2012 Dec;13(12):1178-86
pubmed: 23104095
Genome Res. 2014 Feb;24(2):340-8
pubmed: 24162188
Mol Cell. 2009 May 14;34(4):461-72
pubmed: 19481526
Trends Immunol. 2016 Aug;37(8):535-545
pubmed: 27424290
Dev Cell. 2007 Nov;13(5):705-716
pubmed: 17981138
Cell Death Differ. 2017 Jul;24(7):1172-1183
pubmed: 28362430
Immunity. 2012 Aug 24;37(2):223-34
pubmed: 22921120
Autophagy. 2018;14(1):66-79
pubmed: 29394115
PLoS One. 2013 Oct 02;8(10):e76841
pubmed: 24098568
J Exp Med. 2004 Jun 21;199(12):1651-8
pubmed: 15210743
Nature. 2003 Aug 14;424(6950):793-6
pubmed: 12917689
J Exp Med. 2012 Aug 27;209(9):1567-82
pubmed: 22851595
Nat Neurosci. 2015 May;18(5):631-6
pubmed: 25803835
Trends Immunol. 2019 May;40(5):387-402
pubmed: 31003931
Hum Genet. 2020 Jun;139(6-7):745-757
pubmed: 32067110
Nat Genet. 2011 May;43(5):491-8
pubmed: 21478889
PLoS Biol. 2018 Jul 3;16(7):e2005970
pubmed: 29969450
Science. 2015 Mar 27;347(6229):1436-41
pubmed: 25700176
Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):233-8
pubmed: 14679297
Cell. 2003 Jul 25;114(2):181-90
pubmed: 12887920
Cell Rep. 2014 May 22;7(4):971-81
pubmed: 24813885
J Biol Chem. 2002 Apr 19;277(16):13840-7
pubmed: 11839743
Cell. 2018 Sep 6;174(6):1477-1491.e19
pubmed: 30146158
Mol Cell Biol. 2017 Feb 15;37(5):
pubmed: 27920255
Proc Natl Acad Sci U S A. 2016 Apr 12;113(15):4039-44
pubmed: 27035970
Immunity. 1999 Dec;11(6):721-31
pubmed: 10626894
J Leukoc Biol. 2010 Dec;88(6):1171-80
pubmed: 20651301
Nat Rev Neurosci. 2019 Jan;20(1):19-33
pubmed: 30467385
Nature. 2020 Jan;577(7788):109-114
pubmed: 31827280
Mol Cell Biol. 2002 Sep;22(17):6034-45
pubmed: 12167698
Science. 2003 May 16;300(5622):1148-51
pubmed: 12702806
J Med Genet. 2014 Feb;51(2):76-82
pubmed: 24262145
Nat Genet. 2014 Mar;46(3):310-5
pubmed: 24487276
Cell. 2018 May 17;173(5):1244-1253.e10
pubmed: 29681455
Nat Cell Biol. 2018 Dec;20(12):1389-1399
pubmed: 30420664
Mol Brain. 2017 Feb 2;10(1):5
pubmed: 28148298
PLoS One. 2014 Oct 31;9(10):e111548
pubmed: 25360890
Cell. 2009 Jun 12;137(6):1112-23
pubmed: 19524513
Rheumatology (Oxford). 2021 Feb 1;60(2):607-616
pubmed: 32447396
Mol Cell. 2018 Feb 15;69(4):566-580.e5
pubmed: 29452637
Curr Protoc Bioinformatics. 2013;43:11.10.1-11.10.33
pubmed: 25431634
Science. 2012 Sep 28;337(6102):1684-8
pubmed: 22859821
Nat Immunol. 2009 Nov;10(11):1215-21
pubmed: 19820708
Cell Res. 2013 Aug;23(8):994-1006
pubmed: 23835476
J Biol Chem. 2020 Dec 25;295(52):18226-18238
pubmed: 33106313
Cell. 2021 Jan 7;184(1):149-168.e17
pubmed: 33278357
Science. 2014 Mar 21;343(6177):1357-60
pubmed: 24557836
Nature. 2020 Jan;577(7788):103-108
pubmed: 31827281
PLoS Comput Biol. 2013;9(7):e1003153
pubmed: 23874191
Acta Neuropathol. 2015 Jul;130(1):77-92
pubmed: 25943890
Cell Rep. 2015 Dec 15;13(10):2258-72
pubmed: 26670046
J Exp Med. 2004 Jun 21;199(12):1641-50
pubmed: 15210742
Nat Cell Biol. 2014 Jan;16(1):55-65
pubmed: 24316671

Auteurs

Justin Taft (J)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Michael Markson (M)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Diana Legarda (D)

Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Roosheel Patel (R)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Mark Chan (M)

Department of Immunology, Mayo Clinic, Rochester, MN, 55905, USA.

Louise Malle (L)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Ashley Richardson (A)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Conor Gruber (C)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Marta Martín-Fernández (M)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Grazia M S Mancini (GMS)

Department of Clinical Genetics, Erasmus University Medical Center, 3015GD Rotterdam, the Netherlands.

Jan A M van Laar (JAM)

Department of Immunology, Erasmus University Medical Center, 3015GD Rotterdam, the Netherlands.

Philomine van Pelt (P)

Department of Rheumatology, Erasmus University Medical Center, 3015GD Rotterdam, the Netherlands.

Sofija Buta (S)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Beatrijs H A Wokke (BHA)

Department of Neurology, Erasmus University Medical Center, 3015GD Rotterdam, the Netherlands.

Ira K D Sabli (IKD)

Department of Paediatric Infectious Diseases and Virology, Imperial College London, London, UK; Centre for Paediatrics and Child Health, Faculty of Medicine, Imperial College London, London, UK.

Vanessa Sancho-Shimizu (V)

Department of Paediatric Infectious Diseases and Virology, Imperial College London, London, UK; Centre for Paediatrics and Child Health, Faculty of Medicine, Imperial College London, London, UK.

Pallavi Pimpale Chavan (PP)

Inflammatory Disease Section, National Human Genome Research Institute, Bethesda, MD, 20892, USA; Pediatric Rheumatology, SRCC Children's Hospital, Mumbai, India.

Oskar Schnappauf (O)

Inflammatory Disease Section, National Human Genome Research Institute, Bethesda, MD, 20892, USA.

Raju Khubchandani (R)

Pediatric Rheumatology, SRCC Children's Hospital, Mumbai, India; Consultant Pediatrician, Jaslok and Breach Candy Hospitals, Mumbai, India.

Müşerref Kasap Cüceoğlu (MK)

Department of Pediatric Rheumatology, Hacettepe University, Ankara, Turkey.

Seza Özen (S)

Department of Pediatric Rheumatology, Hacettepe University, Ankara, Turkey.

Daniel L Kastner (DL)

Inflammatory Disease Section, National Human Genome Research Institute, Bethesda, MD, 20892, USA.

Adrian T Ting (AT)

Department of Immunology, Mayo Clinic, Rochester, MN, 55905, USA.

Ivona Aksentijevich (I)

Inflammatory Disease Section, National Human Genome Research Institute, Bethesda, MD, 20892, USA.

Iris H I M Hollink (IHIM)

Department of Clinical Genetics, Erasmus University Medical Center, 3015GD Rotterdam, the Netherlands.

Dusan Bogunovic (D)

Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA. Electronic address: dusan.bogunovic@mssm.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH