Circadian control of BDNF-mediated Nrf2 activation in astrocytes protects dopaminergic neurons from ferroptosis

Free Radical Biology and Medicine - Tập 133 - Trang 169-178 - 2019
Tetsuro Ishii1, Eiji Warabi1, Giovanni E. Mann2
1School of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8577, Japan
2School of Cardiovascular Medicine and Sciences, King’s British Heart Foundation Centre of Research Excellence, Faculty of Life Sciences and Medicine, King’s College London, London SE1 9NH, UK

Tóm tắt

Từ khóa


Tài liệu tham khảo

Xie, 2016, Ferroptosis: process and function, Cell Death Differ., 23, 369, 10.1038/cdd.2015.158

Stockwell, 2017, Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease, Cell, 171, 273, 10.1016/j.cell.2017.09.021

Lane, 2018, Iron and Alzheimer’s disease: an update on emerging mechanisms, J. Alzheimers Dis., 10.3233/JAD-179944

Codazzi, 2015, Iron entry in neurons and astrocytes: a link with synaptic activity, Front. Mol. Neurosci., 8, 18, 10.3389/fnmol.2015.00018

Lane, 2010, Two routes of iron accumulation in astrocytes: ascorbate-dependent ferrous iron uptake via the divalent metal transporter (DMT1) plus an independent rout for ferric iron, Biochem. J., 432, 123, 10.1042/BJ20101317

Bishop, 2010, Synergistic accumulation of iron and zinc by cultured astrocytes. J Neural accumulation of iron and zinc by cultured astrocytes, J. Neural Transm., 117, 809, 10.1007/s00702-010-0420-9

Pelizzoni, 1832, Iron uptake in quiescent and inflammation-activated astrocytes: a potentially neuroprotective control of iron burden, Biochem. Biophys. Acta, 2013, 1326

Hohnholt, 2013, Uptake and metabolism of iron and iron oxide nanoparticles in brain astrocytes, Biochem. Soc. Trans., 41, 1588, 10.1042/BST20130114

Morris, 2018, Why should neuroscientists worry about iron? The emrging role of ferroptosis in the pathophysiology of neuroprogressive diseases, Behav. Brain Res., 341, 154, 10.1016/j.bbr.2017.12.036

Zhang, 2017, Diurnal variations in iron concentrations and expression of genes involved in iron absorption and metabolism in pigs, Biochem. Biophys. Res. Commun., 490, 1210, 10.1016/j.bbrc.2017.06.187

Fricker, 2018, Neuronal cell death, Physiol. Rev., 98, 813, 10.1152/physrev.00011.2017

Genoud, 2017, Subcellular compartmentalization of copper, iron, manganese, and zinc in the Parkinson’s disease brain, Metallomics, 9, 1447, 10.1039/C7MT00244K

Liddell, 2017, Nexus between mitochondrial function, iron, copper and glutathione in Parkinson’s disease, Neurochem. Int.

Do Van, 2016, Ferroptosis, a newly characterized form of cell death in Parkinson’s disease that is regulated by PKC, Neurobiol. Dis., 94, 169, 10.1016/j.nbd.2016.05.011

Guiney, 2017, Ferroptosis and cell death mechanisms in Parkinson’s disease, Neurochem. Int., 104, 34, 10.1016/j.neuint.2017.01.004

Muñoz, 2016, Commentary: evaluation of models of Parkinson’s disease, Front. Neurosci., 10, 161

Sugimoto, 2005, 9,10-Phenanthraquinone in diesel exhaust particles downregulates Cu,Zn-SOD and HO-1 in human pulmonary epithelial cells: intracellular iron scavenger 1,10-phenanthroline affords protection against apoptosis, Free Radic. Biol. Med., 38, 388, 10.1016/j.freeradbiomed.2004.11.003

Zecca, 1994, Iron and other metals in neuromelanin, susbtantia nigra, and putamen of human brain, J. Neurochem., 62, 1097, 10.1046/j.1471-4159.1994.62031097.x

Zecca, 2001, Iron, neuromelanin and ferritin content in the substantia nigra of normal subjects at different ages: consequences for iron storage and neurodegenerative processes, J. Neurochem., 76, 1766, 10.1046/j.1471-4159.2001.00186.x

Unger, 2014, Low brain iron effects and revesrsibility on striatal dopamine dynamics, Exp. Neurol., 261, 462, 10.1016/j.expneurol.2014.06.023

Bindoli, 1988, Lipid peroxidation in mitochondria, Free Radic. Biol. Med., 5, 247, 10.1016/0891-5849(88)90018-4

Jenner, 1991, Oxidative stress as a cause of Parkinson’s disease, Acta Neurol. Scand. Suppl., 136, 6, 10.1111/j.1600-0404.1991.tb05013.x

Fernández-Checa, 1997, GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect, Am. J. Physiol., 273, G7

Sagara, 1993, Maintenance of neuronal glutathione by glial cells, J. Neurochem., 61, 1672, 10.1111/j.1471-4159.1993.tb09802.x

Ishii, 2014, Redox status in mammalian cells and stem cells during culture in vitro: critical roles of Nrf2 and cystine transporter activity in the maintenance of redox balance, Redox Biol., 2, 786, 10.1016/j.redox.2014.04.008

Itoh, 1997, An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements, Biochem. Biophys. Res. Commun., 236, 313, 10.1006/bbrc.1997.6943

Ishii, 2000, Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages, J. Biol. Chem., 275, 16023, 10.1074/jbc.275.21.16023

Mann, 2015, Introduction to Special Issue on ‘Nerf2 regulated redox signaling and metabolism in physiology and medicine’, Free Radic. Biol. Med., 88, 91, 10.1016/j.freeradbiomed.2015.08.002

Cui, 2016, Ferrous iron induces Nrf2 expression in mouse brain astrocytes to prevent neurotoxicity, J. Biochem. Mol. Toxicol., 30, 396, 10.1002/jbt.21803

Kerins, 2017, The role of NRF2 in modulating cellular iron homeostasis, Antioxid. Redox Signal.

Ishii T, 2018, Circadian control of p75 neurotrophin receptor leads to alternate activation of Nrf2 and c-Rel to reset energy metabolism in astrocytes via brain-derived neurotrophic factor, Free Radic. Biol. Med., 119, 34, 10.1016/j.freeradbiomed.2018.01.026

Baquet, 2005, Brain-derived neurotrophic factor is required for the establishment of the proper number of dopaminergic neurons in the substantia nigra pars compacta, J. Neurosci., 25, 6251, 10.1523/JNEUROSCI.4601-04.2005

Kraft, 2004, Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult, J. Neurosci., 24, 1101, 10.1523/JNEUROSCI.3817-03.2004

Bannai, 1977, Effect of antioxidants on cultured human diploid fibroblasts exposed to cystine-free medium, Biochem. Biophys. Res. Commun., 74, 1582, 10.1016/0006-291X(77)90623-4

Bannai, 1986, Exchange of cystine and glutamate across plasma membrane of human fibroblasts, J. Biol. Chem., 261, 2256, 10.1016/S0021-9258(17)35926-4

Bannai, 1984, Transport of cystine and cysteine in mammalian cells, Biochim. Biophys. Acta, 779, 289, 10.1016/0304-4157(84)90014-5

Sato, 2002, Distribution of cystine/glutamate exchange transporter, system xc-, in the mouse brain, J. Neurosci., 22, 8028, 10.1523/JNEUROSCI.22-18-08028.2002

Sato, 2005, Redox imbalance in cystine/glutamate transporter-deficient mice, J. Biol. Chem., 280, 37423, 10.1074/jbc.M506439200

Ottestad-Hansen, 2018, The cystine-glutamate exchanger (xCT, Slc7a11) is expressed in significant concentrations in a subpopulation of astrocytes in the mouse brain, Glia, 66, 951, 10.1002/glia.23294

Sasaki, 2002, Electrophile response element-mediated induction of the cystine/glutamate exchange transporter gene expression, J. Biol. Chem., 277, 44765, 10.1074/jbc.M208704200

Ye, 2014, Nrf2- and ATF4-dependent upregulation of xCT modulates the sensitivity of T24 bladder caricinoma cells to proteasome inhibition, Mol. Cell. Biol., 34, 3421, 10.1128/MCB.00221-14

Liu, 2014, FGF-2 induces neuronal death through upregulation of system xc-, Brain Res., 1547, 25, 10.1016/j.brainres.2013.12.018

Fei, 2010, Fibroblast growth factor 2 positively regulates expression of activating transcription factor 4 in osteoblasts, Biochem. Biophys. Res. Commun., 391, 335, 10.1016/j.bbrc.2009.11.059

Malabanan, 2008, Activation transcription factor-4 induced by fibroblast growth factor-2 regulates vascular endothelial growth factor-A transcription in vascular smooth muscle cells and mediates intimal thickening in rat arteries following balloon injury, Circ. Res., 103, 378, 10.1161/CIRCRESAHA.107.168682

Wei, 2015, ATF4: a novel potential therapeutic target for Alzheimer’s disease, Mol. Neurobiol., 52, 1765, 10.1007/s12035-014-8970-8

Kraft, 2006, Neuronal sensitivity to kainic acid is dependent on the Nrf2-mediated actions of the antioxidant response, J. Neurochem., 98, 1852, 10.1111/j.1471-4159.2006.04019.x

Hansson, 1999, Structural determinants in domain II of human glutathione transferase M2-2 govern the characteristic activities with aminochrome, 2-cyano-1,3-dimethyl-1-nitrosoguanidine, and 1,2-dichloro-4-nitrobenzene, Protein Sci., 8, 2742, 10.1110/ps.8.12.2742

Cuevas, 2015, Glutathione transferase-M2-2 secreted from glioblastoma cell protects SH-SY5Y cells from aminochrome neurotoxicity, Neurotox. Res., 27, 217, 10.1007/s12640-014-9500-1

Hambright, 2017, Ablation of ferroptosis regulator glutathione peroxidase 4 in forebrain neurons promotes cognitive impairment and neurodegeneration, Redox Biol., 12, 8, 10.1016/j.redox.2017.01.021

Fisher, 2011, Peroxiredoxin 6: a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities, Antioxid. Redox Signal., 15, 831, 10.1089/ars.2010.3412

Eismann, 2009, Peroxiredoxin-6 protects against mitochondrial dysfunction and liver injury during ischemia-reperfusion in mice, Am. J. Physiol. Gastrointest. Liver Physiol., 296, G266, 10.1152/ajpgi.90583.2008

Ma, 2016, Peroxiredoxin 6 is a crucial factor in the initial step of mitochondrial clearance and is upstream of the PINK1-Parkin pathway, Antioxid. Redox Signal., 24, 486, 10.1089/ars.2015.6336

Pietsch, 2003, Nrf2 mediates the induction of ferritin H in response to xenobiotics and cancer chemopreventive dithiolethiones, J. Biol. Chem., 278, 2361, 10.1074/jbc.M210664200

Lastres-Becker, 2016, Repurposing the NRF2 activator dimethyl fumarate as therapy against synucleinopathy in Parkinson’s disease, Antioxid. Redox Signal., 25, 61, 10.1089/ars.2015.6549

Ahuja, 2016, Distinct Nrf2 signaling mechanisms of fumaric acid esters and their role in neuroprotection against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced experimental Parkinson’s-like disease, J. Neurosci., 36, 6332, 10.1523/JNEUROSCI.0426-16.2016

Au, 1999, The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria, Proc. Natl. Acad. Sci. USA, 96, 4354, 10.1073/pnas.96.8.4354

Boerries, 2007, Ca2+-dependent interaction of S100A1 with F1-ATPase leads to an increased ATP content in cardiomyocytes, Mol. Cell. Biol., 27, 4365, 10.1128/MCB.02045-06

Kosaka, 2010, Role of Nrf2 and p62/ZIP in the neurite outgrowth by carnosic acid in PC12h cells, J. Biochem., 147, 73, 10.1093/jb/mvp149

Dobrowsky, 1994, Activation of the sphinogomyelin cycle through the low-affinity neurotrophin receptor, Science, 265, 1596, 10.1126/science.8079174

Blöchl, 1996, Neurotrophins stimulate the release of dopamine from rat mesencephalic neurons via Trk and p75Lntr receptors, J. Biol. Chem., 271, 21100, 10.1074/jbc.271.35.21100

Müller, 1995, PKCζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid, EMBO J., 14, 1961, 10.1002/j.1460-2075.1995.tb07188.x

Apopa, 2008, Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells, J. Biochem. Mol. Toxicol., 22, 63, 10.1002/jbt.20212

Afonyuskin, 2011, Involvement of CK2 in activation of electrophilic genes in endothelial cells by oxidized phospholipids, J. Lipid Res., 52, 98, 10.1194/jlr.M009480

Baeza-Raja, 2013, neurotrophin receptor is a clock gene that regulates oscillatory components of circadian and metabolic networks, J. Neurosci., 33, 10221, 10.1523/JNEUROSCI.2757-12.2013

Schmutz, 2010, The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors, Genes Dev., 24, 345, 10.1101/gad.564110

Zhao, 2014, Nuclear receptor rock around the clock, EMBO Rep., 15, 518, 10.1002/embr.201338271

Hood, 2010, Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors, J. Neurosci., 30, 14046, 10.1523/JNEUROSCI.2128-10.2010

Lamont, 2005, The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2, Pros. Natl. Acad. USA, 102, 4180, 10.1073/pnas.0500901102

Chung, 2014, Impact of circadian nuclear receptor REV-ERBα on midbrain dopamine production and mood regulation, Cell, 157, 858, 10.1016/j.cell.2014.03.039

Jager, 2014, Benhavioral changes and dopaminergic dysregulation in mice lacking the nuclear receptor Rev-erbα, Mol. Endocrinol., 28, 490, 10.1210/me.2013-1351

Gerbeth, 2013, Glucose-induced regulation of protein import receptor Tom22 by cytosolic and mitochondria-bound kinases, Cell Metab., 18, 578, 10.1016/j.cmet.2013.09.006

Chalfant, 1999, Long chain ceramide activate protein phosphatase-1 and protein phosphatase-2A. Activation is stereospecific and regulated by phosphatidic acid, J. Biol. Chem., 274, 20313, 10.1074/jbc.274.29.20313

Roach, 2012, Glycogen and its metabolism: some new developments and old themes, Biochem. J., 441, 763, 10.1042/BJ20111416

Escudero, 2014, The p75 neurotrophin receptor evades the endolysosomal route in neuronal cells, favouring multivesicular bodies specialized for exsosomal release, J. Cell Sci., 127, 1966

Gomes, 2012, Excitotoxicity downregulates TrkB.FL signaling and upregulates the neuroprotective truncated TrkB receptors in cultured hippocampal and striatal neurons, J. Neurosci., 32, 4610, 10.1523/JNEUROSCI.0374-12.2012

Ishii, 2018, When and how does BDNF activate Nrf2 in astrocytes and neurons?, Neural Regen. Res., 13, 803, 10.4103/1673-5374.232468

Yacoubian, 2000, Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth, Nat. Neurosci., 3, 342, 10.1038/73911

Strack, 1997, Protein serine/threonine phosphatase 1 and 2A associate with and dephosphorylate neurofilaments, Brain Res. Mol. Brain Res., 49, 15, 10.1016/S0169-328X(97)00117-4

Morfini, 2004, A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-deriven motility in neurons, EMBO J., 23, 2235, 10.1038/sj.emboj.7600237

Habas, 2013, Neuronal activity regulates astrocytic Nrf2 signaling, Proc. Natl. Acad. Sci. USA, 110, 18291, 10.1073/pnas.1208764110

Kuczewski, 2008, Back-propagating action potential: a key contributor in activity-dependent dendritic release of BDNF, Commun. Integr. Biol., 1, 153, 10.4161/cib.1.2.7058

Park, 2014, Essential role of presynaptic NMDA receptors in activity-dependent BDNF secretion and corticostriatal LTP, Neuron, 84, 1009, 10.1016/j.neuron.2014.10.045

Wong, 2015, Activity-dependent BDNF release via endocytic pathways is regulated by synaptotagmin-6 and complexin, Proc. Natl. Acad. Sci. USA, 112, E4475, 10.1073/pnas.1511830112

Sasi, 2017, Neurobiology of local and intercellular BDNF signaling, Eur. J. Physiol., 469, 593, 10.1007/s00424-017-1964-4

Gray, 2008, Activation of pro-BDNF by the pericellular serine protease plasmin, FEBS Lett., 582, 907, 10.1016/j.febslet.2008.02.026

Shin, 2004, Rapid, activity-induced increase in tissue plasminogen activator is mediated by metabotropic glutamate receptor-dependent mRNA translation, J. Neurosci., 24, 9425, 10.1523/JNEUROSCI.2457-04.2004

Liu, 2000, Plasminogen enhances the secretion of plasminogen activator inhibitor-1 from cultured rat astrocytes, Neurosci. Lett., 282, 137, 10.1016/S0304-3940(00)00860-0

Vignoli, 2017, Glioactive ATP controls BDNF recycling in cortical astrocytes, Commun. Integr. Biol., 10, e1277296, 10.1080/19420889.2016.1277296

Wang, 2014, The membrane protein Pannexin1 forms two open-channel conformations depending on the mode of activation, Sci. Signal., 7, ra69, 10.1126/scisignal.2005431

Scemes, 2012, Extracellular K+ and astrocyte signaling via connexin and pannexin channels, Neurochem. Res., 37, 2310, 10.1007/s11064-012-0759-4

Puchałowicz, 2014, P2X and P2Y receptors-role in the pathophysiology of the nervous system, Int. J. Mol. Sci., 15, 23672, 10.3390/ijms151223672

Khakh, 2012, Neuromodulation by extracellular ATP and P2X receptors in the CNS, Neuron, 76, 51, 10.1016/j.neuron.2012.09.024

Bianco, 2009, Acid sphingomyelinase activity triggers microparticle release from glial cells, EMBO J., 28, 1043, 10.1038/emboj.2009.45

Basso, 2016, Extracellular vesicles and a novel form of communication in the brain, Front. Neurosci., 10, 127, 10.3389/fnins.2016.00127

Verkhratsky, 2016, Astrocytes as secretory cells of the central nervous system: idiosyncrasies of vesicular secretion, EMBO J., 35, 239, 10.15252/embj.201592705

Vardjan, 2016, Loos excitation-secretion coupling in astrocytes, Glia, 64, 655, 10.1002/glia.22920

Colombo, 2014, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles, Annu. Rev. Cell Dev. Biol., 30, 255, 10.1146/annurev-cellbio-101512-122326

Cocucci, 2015, Ectosomes and exosomes: shedding the confusion between extracellular vesicles, Trends Cell Biol., 25, 364, 10.1016/j.tcb.2015.01.004

Qu, 2009, P2X7 receptors regulate multiple types of membrane trafficking responses and non-classical secretion pathways, Purinergic Signal., 5, 163, 10.1007/s11302-009-9132-8

North, 2016, P2X receptors, Philos. Trans. R. Soc. Lond. B Biol. Sci., 371

Verkhratsky, 2016, Astrocytes as secretory cells of the central nervous system: idiosyncrasies of vesicular secretion, EMBO J., 35, 239, 10.15252/embj.201592705

Vardjan, 2016, Loose excitation-secretion coupling in astrocytes, Glia, 64, 655, 10.1002/glia.22920

Checconi, 2015, Redox proteomics of the inflammatory secretome identifies a common set of redoxins and other glutathionylated proteins released in inflammation, influenza virus infection and oxidative stress, PLoS One, 10, e0127086, 10.1371/journal.pone.0127086

Truman-Rosentsvit, 2018, Ferritin is secreted via 2 distinct nonclassical vesicular pathways, Blood, 131, 342, 10.1182/blood-2017-02-768580

Pinet, 2016, TrkB-containing exosomes promote the transfer of glioblastoma aggressiveness to YKL-40-inactivated glioblastoma cells, Oncotarget, 7, 50349, 10.18632/oncotarget.10387

Basso, 2016, Extracellular vesicles and a novel form of communication in the brain, Front. Neurosci., 10, 127, 10.3389/fnins.2016.00127

Hermosilla, 1783, Direct Thy-1/αvβ3 integrin interaction mediates neuron to astrocyte communication, Biochim. Biophys. Acta, 2008, 1111

Avalos, 2009, Neuronal Thy-1 induces astrocyte adhesion by engaging syndecan-4 in a cooperative interaction with αvβ3 integrin that activates PKCα and RhoA, J. Cell Sci., 122, 3462, 10.1242/jcs.034827

Henríquez, 2011, ATP release due to Thy-a-integrin binding induces P2X7-mediated calcium entry required for focal adhesion formation, J. Cell Sci., 124, 1581, 10.1242/jcs.073171

Lagos-Cabré, 2017, αvβ3 Integrin regulates astrocyte reactivity, J. Neuroinflamm., 14, 194, 10.1186/s12974-017-0968-5

Shentu, 2017, Thy-1 dependent uptake of mesenchymal stem cee-derived extracellular vesicles blocks myofibroblastic differentiation, Sci. Rep., 7, 18052, 10.1038/s41598-017-18288-9

Hoshino, 2015, exosome integrins determine organotropic metastasis, Nature, 527, 329, 10.1038/nature15756

Singh, 2016, Exosome-mediated transfer of αvβ3 integrin from tumorigenic to nontumorigenic cells promotes a migratory phenotype, Mol. Cancer Res., 14, 1136, 10.1158/1541-7786.MCR-16-0058

Womac, 2009, Circadian rhythms of extracellular ATP accumulation in suprachiasmatic nucleus cells and cultured astrocytes, Eur. J. Neurosci., 30, 869, 10.1111/j.1460-9568.2009.06874.x

Marpegan, 2011, Circadian regulation of ATP release in astrocytes, J. Neurosci., 31, 8342, 10.1523/JNEUROSCI.6537-10.2011

Burkeen, 2011, Mitochondrial calcium signaling mediates rhythmic extracellular ATP accumulation in suprachiasmatic nucleus astrocytes, J. Neurosci., 31, 8432, 10.1523/JNEUROSCI.6576-10.2011

Hastings, 2003, A clockwork web: circadian timing in brain and periphery, in health and disease, Nat. Rev. Neurosci., 4, 649, 10.1038/nrn1177

Harbour, 2014, Phase differences in expression of circadian clock genes in the central nucleus of the amygdala, dentate gyrus, and suprachiasmatic nucleus in the rat, PLos One, 9, e103309, 10.1371/journal.pone.0103309

Moore, 1972, Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat, Brain Res., 42, 201, 10.1016/0006-8993(72)90054-6

Meyer-Bernstein, 1999, Effects of suprachiasmatic trnasplants on circadian rhythms of neuroendocrine function in golden hamsters, Endocrinol, 140, 207, 10.1210/endo.140.1.6428

Cuesta, 2015, Glucocorticoids entrain molecular clock components in human peripheral cells, FASEB J., 29, 1360, 10.1096/fj.14-265686

Son, 2011, The adrenal peripheral clock: glucocorticoid and the circadian timing system, Front. Neuroendocrinol., 32, 451, 10.1016/j.yfrne.2011.07.003

Koyanagi, 2016, Glucocorticoid regulation of ATP release from spinal astrocytes underlies diurnal exacerbation of neuropathic mechanical allodynia, Nat. Commun., 7, 13102, 10.1038/ncomms13102

Reddy, 2010, Healthy clocks, healthy body, healthy mind, Trends Cell Biol., 20, 36, 10.1016/j.tcb.2009.10.005

Videnovic, 2014, ‘The clocks that time us'—circadian rhtyhms in neurodegerative disorders, Nat. Rev. Neurol., 10, 683, 10.1038/nrneurol.2014.206

Musiek, 2016, Mechanisms linking circadian clocks, sleep, and neurodegeneration, Science, 354, 1004, 10.1126/science.aah4968

Mattis, 2016, Circadian rhythms, sleep, and disorders of aging, Trends Endocrinol. Metab., 27, 192, 10.1016/j.tem.2016.02.003

Sfera, 2017, Ferrosenescence: the iron age of neurodegeneration?, Mech. Ageing Dev.