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The reactive species interactome: Evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine

The reactive species interactome: Evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine
The reactive species interactome: Evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine

SIGNIFICANCE: Oxidative stress is thought to account for aberrant redox homeostasis and contribute to aging and disease. However, more often than not administration of antioxidants is ineffective, suggesting our current understanding of the underlying regulatory processes is incomplete. Recent Advances. Similar to reactive oxygen and nitrogen species (ROS, RNS), reactive sulfur species (RSS) are now emerging as important signaling molecules, targeting regulatory cysteine redox switches in proteins, affecting gene regulation, ion transport, intermediary metabolism and mitochondrial function. To rationalize the complexity of chemical interactions of reactive species with themselves and their targets and help define their role in systemic metabolic control, we here introduce a novel integrative concept coined the reactive species interactome (RSI). The RSI is a primeval multi-level redox-regulatory system whose architecture, together with the physicochemical characteristics of its constituents, allows efficient sensing and rapid adaptation to environmental changes and various other stresses to enhance fitness and resilience at the local and whole-organism level.

CRITICAL ISSUES: To better characterise the RSI-related processes that determine fluxes through specific pathways and enable integration, it is necessary to disentangle the chemical biology and activity of reactive species (including precursors and reaction products), their targets, communication systems and effects on cellular, organ and whole-organism bioenergetics using systems-level/network analyses.

FUTURE DIRECTIONS: Understanding the mechanisms through which the RSI operates will enable a better appreciation of the possibilities to modulate the entire biological system; moreover, unveiling molecular signatures that characterize specific environmental challenges or other stresses will provide new prevention/intervention opportunities for personalized medicine.

Journal Article
1523-0864
684-712
Cortese-Krott, Miriam Margherita
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Koning, Anne
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Kuhnle, Gunter Georg
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Nagy, Peter
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Bianco, Christopher
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Pasch, Andreas
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Wink, David A
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Fukuto, Jon
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Jackson, Alan A
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van Goor, Harry
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Olson, Kenneth R
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Feelisch, Martin
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Cortese-Krott, Miriam Margherita
2d88d4d1-a018-4716-bd54-094b1d016021
Koning, Anne
fd7e43e0-8061-4ef9-a64a-bd86a39ad494
Kuhnle, Gunter Georg
79d3cae0-21eb-4478-b70e-dc7ab07bfd90
Nagy, Peter
ef870ecd-2ce8-494f-86da-7260d2a7c2a4
Bianco, Christopher
094ce550-2655-4575-8bd6-5fa43b4ef38e
Pasch, Andreas
5f5d9b34-4d9e-40a4-9326-fa1cd352717d
Wink, David A
008b5aec-8c2b-4035-8912-fb6fd530413c
Fukuto, Jon
b49c4f1a-3095-4154-821f-c3eee66d668b
Jackson, Alan A
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van Goor, Harry
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Olson, Kenneth R
82b73d34-60b6-4915-9328-c50805bea090
Feelisch, Martin
8c1b9965-8614-4e85-b2c6-458a2e17eafd

Cortese-Krott, Miriam Margherita, Koning, Anne, Kuhnle, Gunter Georg, Nagy, Peter, Bianco, Christopher, Pasch, Andreas, Wink, David A, Fukuto, Jon, Jackson, Alan A, van Goor, Harry, Olson, Kenneth R and Feelisch, Martin (2017) The reactive species interactome: Evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine. Antioxidants & Redox Signaling, 27 (10), 684-712. (doi:10.1089/ars.2017.7083).

Record type: Article

Abstract

SIGNIFICANCE: Oxidative stress is thought to account for aberrant redox homeostasis and contribute to aging and disease. However, more often than not administration of antioxidants is ineffective, suggesting our current understanding of the underlying regulatory processes is incomplete. Recent Advances. Similar to reactive oxygen and nitrogen species (ROS, RNS), reactive sulfur species (RSS) are now emerging as important signaling molecules, targeting regulatory cysteine redox switches in proteins, affecting gene regulation, ion transport, intermediary metabolism and mitochondrial function. To rationalize the complexity of chemical interactions of reactive species with themselves and their targets and help define their role in systemic metabolic control, we here introduce a novel integrative concept coined the reactive species interactome (RSI). The RSI is a primeval multi-level redox-regulatory system whose architecture, together with the physicochemical characteristics of its constituents, allows efficient sensing and rapid adaptation to environmental changes and various other stresses to enhance fitness and resilience at the local and whole-organism level.

CRITICAL ISSUES: To better characterise the RSI-related processes that determine fluxes through specific pathways and enable integration, it is necessary to disentangle the chemical biology and activity of reactive species (including precursors and reaction products), their targets, communication systems and effects on cellular, organ and whole-organism bioenergetics using systems-level/network analyses.

FUTURE DIRECTIONS: Understanding the mechanisms through which the RSI operates will enable a better appreciation of the possibilities to modulate the entire biological system; moreover, unveiling molecular signatures that characterize specific environmental challenges or other stresses will provide new prevention/intervention opportunities for personalized medicine.

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ars.2017.7083 - Version of Record
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More information

Accepted/In Press date: 1 April 2016
e-pub ahead of print date: 6 June 2017
Published date: 1 October 2017
Keywords: Journal Article

Identifiers

Local EPrints ID: 414115
URI: https://eprints.soton.ac.uk/id/eprint/414115
ISSN: 1523-0864
PURE UUID: bab52caf-3f03-4e35-beb1-cbd0fd03c6eb
ORCID for Martin Feelisch: ORCID iD orcid.org/0000-0003-2320-1158

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Date deposited: 14 Sep 2017 16:32
Last modified: 10 Dec 2019 01:37

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