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RAGE induces physiological activation of NADPH oxidase in neurons and astrocytes and neuroprotection.

Seryogina, ES ; Kamynina, AV ; et al.
In: The FEBS journal, Jg. 291 (2024-05-01), Heft 9, S. 1944-1957
Online academicJournal

Titel:
RAGE induces physiological activation of NADPH oxidase in neurons and astrocytes and neuroprotection.
Autor/in / Beteiligte Person: Seryogina, ES ; Kamynina, AV ; Koroev, DO ; Volpina, OM ; Vinokurov, AY ; Abramov, AY
Link:
Zeitschrift: The FEBS journal, Jg. 291 (2024-05-01), Heft 9, S. 1944-1957
Veröffentlichung: Oxford, UK : Published by Blackwell Pub. on behalf of the Federation of European Biochemical Societies, c2005-, 2024
Medientyp: academicJournal
ISSN: 1742-4658 (electronic)
DOI: 10.1111/febs.17086
Schlagwort:
  • Animals
  • Neuroprotection
  • Cells, Cultured
  • Oxidation-Reduction
  • Signal Transduction
  • Mice
  • Lipid Peroxidation drug effects
  • Rats
  • Enzyme Activation drug effects
  • Glutathione metabolism
  • Astrocytes metabolism
  • Astrocytes drug effects
  • Neurons metabolism
  • Neurons drug effects
  • Receptor for Advanced Glycation End Products metabolism
  • Receptor for Advanced Glycation End Products genetics
  • Reactive Oxygen Species metabolism
  • NADPH Oxidases metabolism
  • NADPH Oxidases genetics
  • Coculture Techniques
Sonstiges:
  • Nachgewiesen in: MEDLINE
  • Sprachen: English
  • Publication Type: Journal Article; Research Support, Non-U.S. Gov't
  • Language: English
  • [FEBS J] 2024 May; Vol. 291 (9), pp. 1944-1957. <i>Date of Electronic Publication: </i>2024 Feb 09.
  • MeSH Terms: Astrocytes* / metabolism ; Astrocytes* / drug effects ; Neurons* / metabolism ; Neurons* / drug effects ; Receptor for Advanced Glycation End Products* / metabolism ; Receptor for Advanced Glycation End Products* / genetics ; Reactive Oxygen Species* / metabolism ; NADPH Oxidases* / metabolism ; NADPH Oxidases* / genetics ; Coculture Techniques* ; Animals ; Neuroprotection ; Cells, Cultured ; Oxidation-Reduction ; Signal Transduction ; Mice ; Lipid Peroxidation / drug effects ; Rats ; Enzyme Activation / drug effects ; Glutathione / metabolism
  • References: Buckley S & Ehrhardt C (2010) The receptor for advanced glycation end products (RAGE) and the lung. J Biomed Biotechnol 2010, 917108. ; Ramasamy R, Vannucci S, Yan S, Herold K, Yan S & Schmidt A (2005) Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 15, 16R–28R. ; Kim J, Wan C, J O'carroll S, Shaikh S & Nicholson L (2012) The role of receptor for advanced glycation end products (RAGE) in neuronal differentiation. J Neurosci Res 90, 1136–1147. ; Kamynina A, Esteras N, Koroev D, Angelova P, Volpina O & Abramov A (2021) Activation of RAGE leads to the release of glutamate from astrocytes and stimulates calcium signal in neurons. J Cell Physiol 236, 6496–6506. ; Angelova P (2021) Sources and triggers of oxidative damage in neurodegeneration. Free Radic Biol Med 173, 52–63. ; Gandhi S & Abramov A (2012) Mechanism of oxidative stress in neurodegeneration. Oxid Med Cell Longev 2012, 428010. ; Abramov A, Jacobson J, Wientjes F, Hothersall J, Canevari L & Duchen M (2005) Expression and modulation of an NADPH oxidase in mammalian astrocytes. J Neurosci 25, 9176–9184. ; Abramov A, Canevari L & Duchen M (2004) β‐Amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 24, 565–575. ; Vermot A, Petit‐Härtlein I, Smith S & Fieschi F (2021) Nadph oxidases (Nox): an overview from discovery, molecular mechanisms to physiology and pathology. Antioxidants 10, 890. ; Piras S, Furfaro A, Domenicotti C, Traverso N, Marinari U, Pronzato M & Nitti M (2016) RAGE expression and ROS generation in neurons: differentiation versus damage. Oxid Med Cell Longev 2016, 9348651. ; Sangle G, Zhao R, Mizuno T & Shen G (2010) Involvement of RAGE, NADPH oxidase, and Ras/Raf‐1 pathway in glycated LDL‐induced expression of heat shock factor‐1 and plasminogen activator inhibitor‐1 in vascular endothelial cells. Endocrinology 151, 4455–4466. ; Borchi E, Bargelli V, Guidotti V, Berti A, Stefani M, Nediani C & Rigacci S (2014) Mild exposure of RIN‐5F β‐cells to human islet amyloid polypeptide aggregates upregulates antioxidant enzymes via NADPH oxidase‐RAGE: an hormetic stimulus. Redox Biol 2, 114–122. ; Kay A, Simpson C & Stewart J (2016) The role of AGE/RAGE signaling in diabetes‐mediated vascular calcification. J Diabetes Res 2016, 6809703. ; Lin C, Huang P, Chen C, Wu M, Chen J, Chen J & Lin S (2021) Sitagliptin attenuates arterial calcification by downregulating oxidative stress‐induced receptor for advanced glycation end products in LDLR knockout mice. Sci Rep 11, 1–14. ; Volpina O, Samokhin A, Koroev D, Nesterova I, Volkova T, Medvinskaya N, Nekrasov P, Tatarnikova O, Kamynina A, Balasanyants S et al. (2018) Synthetic fragment of receptor for advanced glycation end products prevents memory loss and protects brain neurons in olfactory bulbectomized mice. J Alzheimers Dis 61, 1061–1076. ; Koroev D, Volpina O, Volkova T, Kamynina A, Samokhin A, Filatova M & Bobkova N (2019) A synthetic fragment of the receptor for glycation end products and its analogue improve memory in transgenic Alzheimer's disease mouse model. Russ J Bioorg Chem 45, 361–365. ; Kamynina A, Esteras N, Koroev D, Bobkova N, Balasanyants S, Simonyan R, Avetisyan A, Abramov A & Volpina O (2018) Synthetic fragments of receptor for advanced glycation end products bind beta‐amyloid 1–40 and protect primary brain cells from beta‐amyloid toxicity. Front Neurosci 12, 1–9. ; Volpina O, Koroev D, Serebryakova M, Volkova T, Kamynina A & Bobkova N (2021) Proteolytic degradation patterns of the receptor for advanced glycation end products peptide fragments correlate with their neuroprotective activity in Alzheimer's disease models. Drug Dev Res 82, 1217–1226. ; Cho S, Wood A & Bowlby M (2007) Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr Neuropharmacol 5, 19–33. ; Domijan A‐M, Kovac S & Abramov A (2014) Lipid peroxidation is essential for phospholipase C activity and the inositol‐trisphosphate‐related Ca(2)(+) signal. J Cell Sci 127, 21–26. ; Vinokurov A, Stelmashuk O, Ukolova P, Zherebtsov E & Abramov A (2021) Brain region specificity in reactive oxygen species production and maintenance of redox balance. Free Radic Biol Med 174, 195–201. ; Yan S, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J et al. (1996) RAGE and amyloid‐beta peptide neurotoxicity in Alzheimer's disease. Nature 382, 685–691. ; Wautier M, Chappey O, Corda S, Stern D, Schmidt A & Wautier J (2001) Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280, E685–E694. ; Carrano A, Hoozemans J, van der Vies S, Rozemuller A, van Horssen J & de Vries H (2011) Amyloid beta induces oxidative stress‐mediated blood–brain barrier changes in capillary amyloid angiopathy. Antioxid Redox Signal 15, 1167–1178. ; Abramov A, Ionov M, Pavlov E & Duchen M (2011) Membrane cholesterol content plays a key role in the neurotoxicity of β‐amyloid: implications for Alzheimer's disease. Aging Cell 10, 595–603. ; Thallas‐Bonke V, Thorpe S, Coughlan M, Fukami K, Yap F, Sourris K, Penfold S, Bach L, Cooper M & Forbes J (2008) Inhibition of NADPH oxidase prevents advanced glycation end product‐mediated damage in diabetic nephropathy through a protein kinase C‐α‐dependent pathway. Diabetes 57, 460–469. ; Narayan P, Holmström K, Kim D, Whitcomb D, Wilson M, St. George‐Hyslop P, Wood N, Dobson C, Cho K, Abramov A et al. (2014) Rare individual amyloid‐β oligomers act on astrocytes to initiate neuronal damage. Biochemistry 53, 2442–2453. ; Vaarmann A, Gandhi S & Abramov A (2010) Dopamine induces Ca2+ signaling in astrocytes through reactive oxygen species generated by monoamine oxidase. J Biol Chem 285, 25018–25023. ; Novikova I, Manole A, Zherebtsov E, Stavtsev D, Vukolova M, Dunaev A, Angelova P & Abramov A (2020) Adrenaline induces calcium signal in astrocytes and vasoconstriction via activation of monoamine oxidase. Free Radic Biol Med 159, 15–22. ; Gola L, Bierhansl L, Csatári J, Schroeter C, Korn L, Narayanan V, Cerina M, Abdolahi S, Speicher A, Hermann A et al. (2023) NOX4‐derived ROS are neuroprotective by balancing intracellular calcium stores. Cell Mol Life Sci 80, 127. ; Esteras N, Blacker T, Zherebtsov E, Stelmashchuk O, Zhang Y, Wigley W, Duchen M, Dinkova‐Kostova A & Abramov A (2023) Nrf2 regulates glucose uptake and metabolism in neurons and astrocytes. Redox Biol 62, 102672. ; Vinokurov A, Dremin V, Piavchenko G, Stelmashchuk O, Angelova P & Abramov A (2021) Assessment of mitochondrial membrane potential and NADH redox state in acute brain slices. Methods Mol Biol 2276, 193–202.
  • Grant Information: 23-74-00024 Russian Science Foundation; 075-15-2022-1095 Russian Federation Government
  • Contributed Indexing: Keywords: NADPH oxidase; RAGE; astrocytes; neurons; reactive oxygen species; β‐amyloid
  • Substance Nomenclature: 0 (Receptor for Advanced Glycation End Products) ; 0 (Reactive Oxygen Species) ; EC 1.6.3.- (NADPH Oxidases) ; GAN16C9B8O (Glutathione)
  • Entry Date(s): Date Created: 20240209 Date Completed: 20240503 Latest Revision: 20240523
  • Update Code: 20240523

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