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Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes.

ABSTRACT: Cellular accumulation of reactive oxygen species (ROS) is associated with a wide range of developmental and stress responses. Although cells have evolved to use ROS as signaling molecules, their chemically reactive nature also poses a threat. Antioxidant systems are required to detoxify ROS and prevent cellular damage, but little is known about how these systems manage to function in hostile, ROS-rich environments. Here we show that during oxidative stress in plant cells, the pathogen-inducible oxidoreductase Nucleoredoxin 1 (NRX1) targets enzymes of major hydrogen peroxide (H₂O₂)-scavenging pathways, including catalases. Mutant nrx1 plants displayed reduced catalase activity and were hypersensitive to oxidative stress. Remarkably, catalase was maintained in a reduced state by substrate-interaction with NRX1, a process necessary for its H₂O₂-scavenging activity. These data suggest that unexpectedly H₂O₂-scavenging enzymes experience oxidative distress in ROS-rich environments and require reductive protection from NRX1 for optimal activity.

SUBMITTER: Kneeshaw S

PROVIDER: S-EPMC5547615 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes.

Kneeshaw Sophie S Keyani Rumana R Delorme-Hinoux Valérie V Imrie Lisa L Loake Gary J GJ Le Bihan Thierry T Reichheld Jean-Philippe JP Spoel Steven H SH

Proceedings of the National Academy of Sciences of the United States of America 20170719 31

Cellular accumulation of reactive oxygen species (ROS) is associated with a wide range of developmental and stress responses. Although cells have evolved to use ROS as signaling molecules, their chemically reactive nature also poses a threat. Antioxidant systems are required to detoxify ROS and prevent cellular damage, but little is known about how these systems manage to function in hostile, ROS-rich environments. Here we show that during oxidative stress in plant cells, the pathogen-inducible ...[more]

PMID: 28724723

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Project description:BACKGROUND: Ageing is associated with gastrointestinal dysfunction, which can have a major impact on quality of life of the elderly. A number of changes in the innervation of the gut during ageing have been reported, including neuronal loss and degenerative changes. Evidence indicates that reactive oxygen species (ROS) are elevated in ageing enteric neurons, but that neurotrophic factors may reduce generation of neuronal ROS. Two such factors, glial cell line derived neurotrophic factor (GDNF) and neurotrophin-3 (NT-3) have also been found to protect enteric neurons against oxidative stress induced cell death of enteric ganglion cells in vitro. We have investigated the possible roles of neurotrophic factors further, by examining their expression in the gut during ageing, and by analysing their effects on antioxidant enzyme production in cultures of enteric ganglion cells. RESULTS: Analysis of the expression of GDNF and its receptors c-Ret and GFR ??-?1 in rat gut by RT-PCR showed that expression continues throughout life and into ageing, in both ad libitum(AL) and calorically-restricted (CR) animals. Levels of expression of GDNF and GFR ??-?1 were elevated in 24?month AL animals compared to 24?month CR animals, and to 24 CR and 6?month control animals respectively. The related factor Neurturin and its receptor GFR ??-?2 were also expressed throughout life, the levels of the GFR - ?-2(b) isoform were reduced in 24?m AL animals. Immunolabelling showed that c-Ret and GFR ??-?1 proteins were expressed by myenteric neurons in ageing animals. GDNF, but not NT-3, was found to increase expression of Cu/Zn superoxide dismutase and catalase by cultured enteric ganglion cells. CONCLUSIONS: The neurotrophic factors GDNF and neurturin and their receptors continue to be expressed in the ageing gut. Changes in the levels of expression of GDNF , GFR ?-1 and GFR ?-2(b) isoform occurred in 24?m AL animals. GDNF, but not NT-3, increased the levels of antioxidant enzymes in cultured enteric ganglion cells, indicating a possible mechanism for the reported protective effect of GDNF against menadione-induced neuronal apoptosis in the ageing gut. Together these data suggest that GDNF family members may play a protective role in the gut throughout life, and support the suggestion that dysregulation of neurotrophic factor support could contribute to neuronal ageing in the gut.

Dataset Information

Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes.

Publications

Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes.

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