amyotrophic lateral sclerosis; glutathione levels in the brain; membrane excitability; motor cortex; oxidative stress; postnatal development; Food Science; Physiology; Biochemistry; Molecular Biology; Clinical Biochemistry; Cell Biology
Abstract :
[en] Oxidative stress is one of the main proposed mechanisms involved in neuronal degeneration. To evaluate the consequences of oxidative stress on motor cortex pyramidal neurons during postnatal development, rats were classified into three groups: Newborn (P2-P7); infantile (P11-P15); and young adult (P20-P40). Oxidative stress was induced by 10 µM of cumene hydroperoxide (CH) application. In newborn rats, using the whole cell patch-clamp technique in brain slices, no significant modifications in membrane excitability were found. In infantile rats, the input resistance increased and rheobase decreased due to the blockage of GABAergic tonic conductance. Lipid peroxidation induced by CH resulted in a noticeable increase in protein-bound 4-hidroxynonenal in homogenates in only infantile and young adult rat slices. Interestingly, homogenates of newborn rat brain slices showed the highest capacity to respond to oxidative stress by dramatically increasing their glutathione and free thiol content. This increase correlated with a time-dependent increase in the glutathione reductase activity, suggesting a greater buffering capacity of newborn rats to resist oxidative stress. Furthermore, pre-treatment of the slices with glutathione monoethyl ester acted as a neuroprotector in pyramidal neurons of infantile rats. We conclude that during maturation, the vulnerability to oxidative stress in rat motor neurons increases with age.
Carrascal, Livia; Departament of Physiology, Pharmacy School, University of Seville, 41012 Seville, Spain ; Biomedical Research and Innovation Institute of Cadiz (INIBICA), 11003 Cadiz, Spain
Gorton, Ella; Departament of Physiology, Pharmacy School, University of Seville, 41012 Seville, Spain
Pardillo-Díaz, Ricardo; Area of Physiology, School of Medicine, University of Cádiz, 11003 Cadiz, Spain ; Biomedical Research and Innovation Institute of Cadiz (INIBICA), 11003 Cadiz, Spain
Perez-García, Patricia; Departament of Physiology, Pharmacy School, University of Seville, 41012 Seville, Spain
Gómez Oliva, Ricardo ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Molecular Regulation of Neurogenesis ; Area of Physiology, School of Medicine, University of Cádiz, 11003 Cadiz, Spain ; Biomedical Research and Innovation Institute of Cadiz (INIBICA), 11003 Cadiz, Spain
Castro, Carmen ; Area of Physiology, School of Medicine, University of Cádiz, 11003 Cadiz, Spain ; Biomedical Research and Innovation Institute of Cadiz (INIBICA), 11003 Cadiz, Spain
Nunez-Abades, Pedro ; Departament of Physiology, Pharmacy School, University of Seville, 41012 Seville, Spain ; Biomedical Research and Innovation Institute of Cadiz (INIBICA), 11003 Cadiz, Spain
Language :
English
Title :
Age-Dependent Vulnerability to Oxidative Stress of Postnatal Rat Pyramidal Motor Cortex Neurons.
MICINN - Ministerio de Ciencia, Innovación y Universidades Junta de Andalucía. Consejería de Economía, Conocimiento, Empresas y Universidad
Funding text :
Funding: This work was partially supported by Spanish Ministerio de Ciencia, Innovación y Universidades (RTI2018-099908-B-C21) and co-financed by the 2014-2020 ERDF Operational Programme and by the Department of Economy, Knowledge, Business and University of the Regional Government of Andalusia (FEDER-UCA18-106647) Acknowledgments: Ella Gorton is a visiting fellow of the University of Manchester, UK, supported by a Erasmus Practicas grant. Ricardo Gomez-Oliva is a fellow of the University of Cadiz fellowship program. Ricardo Pardillo-Díaz is a postdoctoral fellow of the University of Cadiz.This work was partially supported by Spanish Ministerio de Ciencia, Innovaci?n y Universidades (RTI2018-099908-B-C21) and co-financed by the 2014-2020 ERDF Operational Programme and by the Department of Economy, Knowledge, Business and University of the Regional Government of Andalusia (FEDER-UCA18-106647).
Ghosh: N.; Das, A.; Chaffee, S.; Roy, S.; Sen, C.K. Reactive oxygen species, oxidative damage and cell death. In Immunity Inflammation in Health and Disease; Academic Press: Cambridge, MA, USA, 2018; pp. 45–55.
Ray, P.D.; Huang, B.W.; Tsuji, Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 2012, 24, 981–990.
Forman, H.J.; Zhang, H.; Rinna, A. Glutathione: Overview of its protective roles, measurement, and biosynthesis. Mol. Asp. Med. 2009, 30, 1–12.
Betteridge, D.J. What is oxidative stress? Metabolism 2000, 49, 3–8.
Rekatsina, M.; Paladini, A.; Piroli, A.; Zis, P.; Pergolizzi, J.V.; Varrassi, G. Pathophysiology and therapeutic perspectives of oxidative stress and neurodegenerative diseases: A narrative review. Adv. Ther. 2019, 37, 113–139.
Rysz, J.; Franczyk, B.; Ławiński, J.; Gluba-Brzózka, A. Oxidative stress in ESRD patients on dialysis and the risk of cardiovascular diseases. Antioxidants 2020, 9, E1079.
García-Sánchez, A.; Miranda-Díaz, A.G.; Cardona-Muñoz, E.G. The role of oxidative stress in physiopathology and pharmacological treatment with pro-and antioxidant properties in chronic diseases. Oxid. Med. Cell. Longev. 2020, 2020, 2082145.
Ragagnin, A.M.G.; Shadfar, S.; Vidal, M.; Jamali, M.S.; Atkin, J.D. Motor neuron susceptibility in ALS/FTD. Front. Neurosci. 2019, 13, 532.
Obrador, E.; Salvador, R.; López-Blanch, R.; Jihad-Jebbar, A.; Vallés, S.L.; Estrela, J.M. Oxidative stress, neuroinflammation and mitochondria in the pathophysiology of amyotrophic lateral sclerosis. Antioxidants 2020, 9, 901.
Jovanovic, Z.; Jovanovic, S. Comparison of the effects of cumene hydroperoxide and hydrogen peroxide on Retzius nerve cells of the leech Haemopis sanguisuga. Exp. Anim. 2013, 62, 9–17.
Ayala, A.; Muñoz, M.F.; Argüelles, S. Lipid Peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-Hydroxy-2-Nonenal. Oxid. Med. Cell. Longev. 2014, 2014, 1–31.
Pardillo-Díaz, R.; Carrascal, L.; Ayala, A.; Nunez-Abades, P. Oxidative stress induced by cumene hydroperoxide evokes changes in neuronal excitability of rat motor cortex neurons. Neuroscience 2015, 289, 85–98.
Carrascal, L.; Nieto-Gonzalez, J.L.; Núñez-Abades, P.; Torres, B. Temporal sequence of changes in electrophysiological properties of oculomotor motoneurons during postnatal development. Neuroscience 2006, 140, 1223–1237.
Carrascal, L.; Luque, M.A.; Sobrino, V.; Torres, B.; Nunez-Abades, P. Postnatal development enhances the effects of cholinergic inputs on recruitment threshold and firing rate of rat oculomotor nucleus motoneurons. Neuroscience 2010, 171, 613–621.
Carrascal, L.; Nieto-González, J.L.; Torres, B.; Nunez-Abades, P. Diminution of voltage threshold plays a key role in determining recruitment of oculomotor nucleus motoneurons during postnatal development. PLoS ONE 2011, 6, E28748.
Pardillo-Díaz, R.; Carrascal, L.; Muñoz, M.F.; Ayala, A.; Nunez-Abades, P. Time and dose dependent effects of oxidative stress induced by cumene hydroperoxide in neuronal excitability of rat motor cortex neurons. Neurotoxicology 2016, 53, 201–214.
Segev, A.; Garcia-Oscos, F.; Kourrich, S. Whole-cell patch-clamp recordings in brain slices. J. Vis. Exp. 2016, 112, E54024.
Torres-Torrelo, J.; Rodriguez-Rosell, D.; Nunez-Abades, P.; Carrascal, L.; Torres, B. Glutamate modulates the firing rate in oculomotor nucleus motoneurons as a function of the recruitment threshold current. J. Physiol. 2012, 590, 3113–3127.
Nieto-Gonzalez, J.L.; Carrascal, L.; Nunez-Abades, P.; Torres, B. Phasic and tonic firing properties in rat oculomotor nucleus motoneurons, studied in vitro. Eur. J. Neurosci. 2007, 25, 2682–2696.
Nieto-Gonzalez, J.L.; Carrascal, L.; Nunez-Abades, P.; Torres, B. Muscarinic modulation of recruitment threshold and firing rate in rat oculomotor nucleus motoneurons. J. Neurophysiol. 2009, 101, 100–111.
Torres-Torrelo, J.; Torres, B.; Carrascal, L. Modulation of the input-output function by GABAA receptor-mediated currents in rat oculomotor nucleus motoneurons. J. Physiol. 2014, 592, 5047–5064.
Corrales, F.J.; Ruiz, F.; Mato, J.M. In vivo regulation by glutathione of methionine adenosyltransferase S-nitrosylation in rat liver. J. Hepatol. 1999, 31, 887–894.
Castro, C.; Millian, N.S.; Garrow, T.A. Liver betaine-homocysteine S-methyltransferase activity undergoes a redox switch at the active site zinc. Arch. Biochem. Biophys. 2008, 472, 26–33.
Rabaneda, L.G.; Geribaldi-Doldán, N.; Murillo-Carretero, M.; Carrasco, M.; Martínez-Salas, J.M.; Verástegui, C.; Castro, C. Altered regulation of the Spry2/Dyrk1A/PP2A triad by homocysteine impairs neural progenitor cell proliferation. Biochim. Biophys. Acta 2016, 1863, 3015–3026.
Carrasco, M.; Rabaneda, L.G.; Murillo-Carretero, M.; Ortega-Martínez, S.; Martínez-Chantar, M.L.; Woodhoo, A.; Luka, Z.; Wagner, C.; Lu, S.C.; Mato, J.M.; et al. Glycine N-methyltransferase expression in the hippocampus and its role in neurogenesis and cognitive performance. Hippocampus 2014, 24, 840–852.
Pardillo-Diaz, R.; Carrascal, L.; Barrionuevo, G.; Nunez-Abades, P. Oxidative stress induced by cumene hydroperoxide produces synaptic depression and transient hyperexcitability in rat primary motor cortex neurons. Mol. Cell. Neurosci. 2017, 82, 204–217.
Klein, J.A.; Ackerman, S.L. Oxidative stress, cell cycle, and neurodegeneration. J. Clin. Invest. 2003, 111, 785-793.
Vimard, F.; Saucet, M.; Nicole, O.; Feuilloley, M.; Duval, D. Toxicity induced by cumene hydroperoxide in PC12 cells: Protective role of thiol donors. J. Biochem. Mol. Toxicol. 2011, 25, 205–215.
Vimard, F.; Nouvelot, A.; Duval, D. Cytotoxic effects of an oxidative stress on neuronal-like pheochromocytoma cells (PC12). Biochem. Pharmacol. 1996, 51, 1389–1395.
Nakaya, H.; Takeda, Y.; Tohse, N.; Kanno, M. Mechanism of the membrane depolarization induced by oxidative stress in guinea-pig ventricular cells. J. Mol. Cell. Cardiol. 1992, 24, 523–534.
Sakmann, B.; Trube, G. Voltage-dependent inactivation of inward-rectifying single-channel currents in the guinea-pig heart cell membrane. J. Physiol. 1984, 347, 659-683.
Fisher, N.D.; Nistri, A. Substance P and TRH share a common effector pathway in rat spinal motoneurones: An in vitro electrophysiological investigation. Neurosci. Lett. 1993, 153, 115–119.
Nani, F.; Cifra, A.; Nistri, A. Transient oxidative stress evokes early changes in the functional properties of neonatal rat hypoglossal motoneurons in vitro. Eur. J. Neurosci. 2010, 31, 951–966.
Dantzler, H.A.; Matott, M.P.; Martinez, D.; Kline, D.D. Hydrogen peroxide inhibits neurons in the paraventricular nucleus of the hypothalamus via potassium channel activation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2019, 317, 121–133.
Ohashi, M.; Hirano, T.; Watanabe, K.; Shoji, H.; Ohashi, N.; Baba, H.; Endo, N.; Kohno, T. Hydrogen peroxide modulates neuronal excitability and membrane properties in ventral horn neurons of the rat spinal cord. Neuroscience 2016, 331, 206–220.
Frantseva, M.V.; Perez Velazquez, J.L.; Carlen, P.L. Changes in membrane and synaptic properties of thalamocortical circuitry caused by hydrogen peroxide. J. Neurophysiol. 1998, 80, 1317–1326.
Zanette, G.; Tamburin, S.; Manganotti, P.; Refatti, N.; Forgione, A.; Rizzuto, N. Different mechanisms contribute to motor cortex hyperexcitability in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2002, 113, 1688–1697.
Ziemann, U.; Winter, M.; Reimers, C.D.; Reimers, K.; Tergau, F.; Paulus, W. Impaired motor cortex inhibition in patients with amyotrophic lateral sclerosis. Evidence from paired transcranial magnetic stimulation. Neurology 1997, 49, 1292–1298.
Sebe, J.Y.; Looke-Stewart, E.C.; Estrada, R.C.; Baraban, S.C. Robust tonic GABA currents can inhibit cell firing in mouse newborn neocortical pyramidal cells. Eur. J. Neurosci. 2010, 32, 1310–1318.
Nieto-Gonzalez, J.L.; Moser, J.; Lauritzen, M.; Schmitt-John, T.; Jensen, K. Reduced GABAergic inhibition explains cortical hyperexcitability in the wobbler mouse model of ALS. Cereb. Cortex 2011, 21, 625–635.
Pouokam, E.; Rehn, M.; Diener, M. Effects of H2O2 at rat myenteric neurones in culture. Eur. J. Pharmacol. 2009, 615, 40–49.
Huang, W.-F.; Ouyang, S.; Zhang, H. The characteristics and oxidative modulation of large-conductance calcium-activated potassium channels in guinea-pig colon smooth muscle cells. Acta Physiol. Sin. 2009, 61, 285–291.
Hasan, S.M.; Joe, M.; Alshuaib, W.B. Oxidative stress alters physiological and morphological neuronal properties. Neurochem. Res. 2007, 32, 1169–1178.
Hasan, S.M.K.; Redzic, Z.B.; Alshuaib, W.B. Hydrogen peroxide-induced reduction of delayed rectifier potassium current in hippocampal neurons involves oxidation of sulfhydryl groups. Brain Res. 2013, 1520, 61–69.
Jovanovic, Z.D.; Stanojevic, M.B.; Nedeljkov, V.B. The neurotoxic effects of hydrogen peroxide and copper in Retzius nerve cells of the leech Haemopis sanguisuga. Biol. Open 2016, 5, 381–388.
Cabungcal, J.H.; Counotte, D.S.; Lewis, E.; Tejeda, H.A.; Piantadosi, P.; Pollock, C.; Calhoon, G.G.; Sullivan, E.; Presgraves, E.; Kil, J.; et al. Juvenile antioxidant treatment prevents adult deficits in a developmental model of schizophrenia. Neuron 2014, 83, 1073–1084.
Carrascal, L.; Nunez-Abades, P.; Ayala, A.; Cano, M. Role of melatonin in the inflammatory process and its therapeutic potential. Curr. Pharm. Des. 2018, 24, 1563–1588.
Park, H.-A.; Ellis, A.C. Dietary antioxidants and Parkinson’s disease. Antioxidants 2020, 9, 570.
Galano, A.; Tan, D.X.; Reiter, R.J. Melatonin as a natural ally against oxidative stress: A physicochemical examination. J. Pineal Res. 2011, 51, 1–16.
Mehrabadi, S.; Sadr, S.S. Administration of Vitamin D3 and E supplements reduces neuronal loss and oxidative stress in a model of rats with Alzheimer’s disease. Neurol. Res. 2020, 42, 862–868.
Oh, S.; Kim, Y.J.; Lee, E.K.; Park, S.W.; Yu, H.G. Antioxidative effects of ascorbic acid and astaxanthin on arpe-19 cells in an oxidative stress model. Antioxidants 2020, 9, 833.
Deepashree, S.; Niveditha, S.; Shivanandappa, T.; Ramesh, S.R. Oxidative stress resistance as a factor in aging: Evidence from an extended longevity phenotype of Drosophila melanogaster. Biogerontology 2019, 20, 497–513.
Guevara, R.; Gianotti, M.; Oliver, J.; Roca, P. Age and sex-related changes in rat brain mitochondrial oxidative status. Exp. Gerontol. 2011, 46, 923–928.
Cassarino, D.S.; Bennett, J.P. An evaluation of the role of mitochondria in neurodegenerative diseases: Mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 1999, 29, 1–25.
Zou, S.; Meadows, S.; Sharp, L.; Jan, L.Y.; Jan, Y.N. Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2000, 97, 13726–13731.
Castelli, V.; Benedetti, E.; Antonosante, A.; Catanesi, M.; Pitari, G.; Ippoliti, R.; Cimini, A.; d’Angelo, M. Neuronal cells rearrangement during aging and neurodegenerative disease: Metabolism, oxidative stress and organelles dynamic. Front. Mol. Neurosci. 2019, 12, 132.
Porcellotti, S.; Fanelli, F.; Fracassi, A.; Sepe, S.; Cecconi, F.; Bernardi, C.; Cimini, A.; Cerù, M.P.; Moreno, S. Oxidative stress during the progression of β-amyloid pathology in the neocortex of the Tg2576 mouse model of Alzheimer’s disease. Oxid. Med. Cell. Longev. 2015, 2015, 967203.
Bjørklund, G.; Peana, M.; Maes, M.; Dadar, M.; Severin, B. The glutathione system in Parkinson’s disease and its progression. Neurosci. Biobehav. Rev. 2020, doi:10.1016/j.neubiorev.2020.10.004.
Kussmaul, L.; Hamprecht, B.; Dringen, R. The detoxification of cumene hydroperoxide by the glutathione system of cultured astroglial cells hinges on hexose availability for the regeneration of NADPH. J. Neurochem. 1999, 73, 1246–1253.
Dringen, R.; Pawlowski, P.G.; Hirrlinger, J. Peroxide detoxification by brain cells. J. Neurosci. Res. 2005, 79, 157–165.