Heat shock protein gp96 and NAD(P)H oxidase 4 play key roles in Toll-like receptor 4-activated apoptosis during renal ischemia/reperfusion injury

Ben Mkaddem, S; Pedruzzi, E; Werts, C; Coant, N; Bens, M; Cluzeaud, F; Goujon, J M; Ogier-Denis, E; Vandewalle, A

doi:10.1038/cdd.2010.26

Cited by 90Acute Kidney Injury ResearchImmune Response and InflammationCell death mechanisms and regulation

Heat shock protein gp96 and NAD(P)H oxidase 4 play key roles in Toll-like receptor 4-activated apoptosis during renal ischemia/reperfusion injury

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Ben Mkaddem, S, Pedruzzi, E, Werts, C, Coant, N, Bens, M, Cluzeaud, F, Goujon, J M, Ogier-Denis, E +1 more·2010·Cell Death & Differentiation

DOI 10.1038/cdd.2010.26

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Abstract

Ischemia/reperfusion injury (IRI) causes inflammation and cell injury as a result of activating innate immune signaling. Toll-like receptor 4 (TLR4) has a key role in mediating kidney damages during IRI, but the downstream signaling pathway(s) stimulating apoptosis remains debated. In this study we show that TLR4 mediates MyD88-dependent activation of TNF receptor-associated factor 2, apoptosis signal-regulating kinase 1 (ASK1), and Jun N-terminal kinase (JNK) and p38 MAP kinases in ischemic-reperfused kidneys and posthypoxic renal tubule epithelial cells (RTECs). Hypoxia stimulated the expression of the endoplasmic-resident gp96, which co-immunoprecipitated TLR4, whereas silencing gp96 mRNA expression impaired hypoxia-induced apoptosis in TLR4-expressing RTECs. NAD(P)H oxidase 4 (NOX4) was shown to interact with TLR4 and to be required in lipopolysaccharide-induced production of reactive oxygen species (ROS). IRI stimulated the expression of a 28-kDa NOX4 spliced isoform abundantly expressed in wild-type RTECs, which co-immunoprecipitated with TLR4, but not with gp96 in TLR4-deficient RTECs. Silencing NOX4 mRNA expression impaired hypoxia-induced activation of ASK1 and both JNK and p38, leading to the inhibition of ROS production and apoptosis in posthypoxic TLR4-expressing RTECs. These findings show that, concomitantly to the activation of p38, the gp96/TLR4 interaction is required for activation of ASK1/JNK signaling in posthypoxic mouse RTECs, and that the 28-kDa NOX4 has a key role in TLR4-mediated apoptosis during renal IRI.

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Toll-like receptor 4 (TLR4) has been shown to increase NOX4 activity.
“The membrane protein Toll-like receptor 4 (TLR4) has been shown to increase NOX4 activity (86, 724), and Tks4/5, a homolog of NOXO1, also regulates NOX4 activity (231).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [86]

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Authors: Ben Mkaddem, S., Pedruzzi, E., Werts, C., Coant, N., Bens, M., Cluzeaud, F., Goujon, J. M., Ogier-Denis, E., & Vandewalle, A.
Affiliations: Inserm (FR)
Université de Poitiers (FR)
Corresponding author: Vandewalle, A
ORCID: Werts, C
Coant, N
Venue: Cell Death & Differentiation
Publisher: Springer Science and Business Media LLC
Published: 2010-03-12
Volume: 17
Issue: 9
Pages: 1474-1485
ISSN: 1350-9047 (ISSN-L)
1476-5403
DOI: 10.1038/cdd.2010.26
OpenAlex: W1991987254
Cited by: 90
References: 41
Citations by year: 2026: 1 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 3 · 2017: 3 · 2016: 7 · 2015: 5 · 2014: 8 · 2013: 5 · 2012: 15
FWCI: 7.48
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
Locations: Cell Death and Differentiation (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
Funders: Agence Nationale de la Recherche (ANR-08-MIEN-0030)
Institut National de la Santé et de la Recherche Médicale
Medizinischen Hochschule Hannover
Topics: Health Sciences › Medicine › Nephrology › Acute Kidney Injury Research
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Keywords: heat shock protein gp96, TLR4, renal ischemia-reperfusion injury, apoptosis, MyD88 signaling, ASK1, JNK, p38 MAPK, reactive oxygen species, renal tubular epithelial cells, hypoxia, lipopolysaccharide, endoplasmic reticulum stress, innate immune signaling
MeSH terms: NADPH Oxidase 4, Animals, Epithelial Cells, Female, Isoenzymes, Kidney, Kidney Tubules, Membrane Glycoproteins, Mice, Inbred C57BL, Protein Binding, Signal Transduction, Reperfusion Injury, Cell Hypoxia, Apoptosis, Reactive Oxygen Species, Mice, Knockout, NADPH Oxidases, RNA, Small Interfering, Protein Kinase Inhibitors, TNF Receptor-Associated Factor 2, JNK Mitogen-Activated Protein Kinases, p38 Mitogen-Activated Protein Kinases, MAP Kinase Kinase Kinase 5, bcl-2-Associated X Protein, Toll-Like Receptor 4, Mice, Myeloid Differentiation Factor 88

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Heat shock protein gp96 and NAD(P)H oxidase 4 play key roles in Toll-like receptor 4-activated apoptosis during renal ischemia/reperfusion injury

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