Chapter 1
Generation of Reactive Oxygen Species in the Brain: Signaling for Neural Cell Survival or Suicide
Akhlaq A. Farooqui,
Akhlaq A. Farooqui
Department of Molecular and Cellular Biochemistry, The Ohio State University, Columbus, Ohio, USA
Search for more papers by this authorAkhlaq A. Farooqui,
Akhlaq A. Farooqui
Department of Molecular and Cellular Biochemistry, The Ohio State University, Columbus, Ohio, USA
Search for more papers by this authorBook Editor(s):Tahira Farooqui,
Akhlaq A. Farooqui,
Tahira Farooqui
Department of Entomology/Center of Molecular Neurobiology, The Ohio State University, Columbus, Ohio, USA
Search for more papers by this authorAkhlaq A. Farooqui
Department of Molecular and Cellular Biochemistry, The Ohio State University, Columbus, Ohio, USA
Search for more papers by this authorSummary
This chapter contains sections titled:
-
Introduction
-
Role of Reactive Oxygen Species in Neural Cells
-
ROS-Mediated Survival Signaling in Neural Cells
-
ROS-Mediated Injury in Neural Cells
-
Conclusion
-
References
REFERENCES
- Halliwell, B. Oxidative stress and neurodegeneration: where are we now? J Neurochem 2006; 97: 1634–1658.
- Landriscina, M., Maddalena, F., Laudiero, G., Esposito F. Adaptation to oxidative stress, chemoresistance, and cell survival. Antioxid Redox Signal 2009; 11(11): 2701–2716.
- Farooqui, A.A. and Horrocks, L.A., Glycerophospholipids in the Brain: Phospholipases A2 in Neurological Disorders. New York, Springer, 2007.
- Farooqui, A.A., Ong W.Y. and Horrocks, L.A. Neuro-chemical Aspects of Excitotoxicity. New York: Springer, 2008.
-
Farooqui, A.A. Lipid Mediators in the Brain: the Good, the Bad, and the Ugly. New York: Springer, 2011.
10.1007/978-1-4419-9940-5 Google Scholar
-
Farooqui, A.A. Hot Topics in Neural Membrane Lipidology. New York: Springer, 2009.
10.1007/978-0-387-09693-3 Google Scholar
- Farooqui T., Farooqui, A.A. Aging: an important factor for the pathogenesis of neurodegenerative diseases. Mech Ageing Dev 2009; 130(4): 203–215.
- McIntyre, T.M., Zimmerman, G.A., Prescott, S.M. Biologically active oxidized phospholipids. J Biol Chem 1999; 274: 25189–25192.
- Bochkov, V.N., Leitinger, N. Anti-inflammatory properties of lipid oxidation products. J Mol Med 2003; 81(10): 613–626.
- Zaleska, M.M., Wilson, D.F. Lipid hydroperoxides inhibit reacylation of phospholipids in neuronal membranes. J Neurochem 1989; 52: 255–260.
- Van Kuijk, F.J., Handelman, G.J., Dratz, E.A. Consecutive action of phospholipase A2 and glutathione peroxidase is required for reduction of phospholipid hydroperoxides and provides a convenient method to determine peroxide values in membranes. J Free Radic Biol Med 1985; 1: 421–427.
- McLean, L.R., Hagaman, K.A., Davidson, W.S. Role of lipid structure in the activation of phospholipase A2 by peroxidized phospholipids. Lipids 1993; 28: 505–509.
- Imai, H., Nakagawa, Y. Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med., 2003; 34: 145–169.
- Fisher, A.B., Dodia, C., Manevich, Y., Chen, J.W., Feinstein, S.I. Phospholipid hydroperoxides are substrates for non-selenium glutathione peroxidase. J Biol Chem., 1999; 274: 21326–21334.
- Nakagawa, Y. Role of mitochondrial phospholipid hydro-peroxide glutathione peroxidase (PHGPx) as an antiapoptotic factor. Biol Pharmaceut Bull 2004; 27: 956–960.
- Farooqui, A.A., Horrocks, L.A., Farooqui, T. Deacylation and reacylation of neural membrane glycerophospholipids. J Mol Neurosci 2000; 14: 123–135.
- Bourdon, E., Blache, D. The importance of proteins in defense against oxidation. Antioxid Redox Signal 2001; 3: 293–311.
- Michiels, C., Raes, M., Toussaint, O., Remacle, J. Importance of Se-glutathione peroxidase, catalase, and Cu,ZnSOD for cell survival against oxidative stress. Free Radic Biol Med., 1994; 17: 235–248.
- Lillig, C.H., Holmgren, A. Thioredoxin and related molecules: from biology to health and disease. Antioxid Redox Signal 2007; 9: 25–47.
- Takada, Y., Mukhopadhyay A., Kundu G.C., Mahabeleshwar H.H., Singh S., Aggarwal B.B. Hydrogen peroxide activates NF-kappa B through tyrosine phosphorylation of I kappa B alpha and serine phosphorylation of p65: evidence for the involvement of I kappa B alpha kinase and Syk protein-tyrosine kinase. J Biol Chem 2003; 278: 24233–24241.
- Touyz, R.M. Reactive oxygen species as mediators of calcium signaling by angiotensin II: implications in vascular physiology and pathophysiology. Antioxid Redox Signal 2005; 7: 1302–1314.
- Groeger, G., Quiney, C., Cotter, T.G. Hydrogen peroxide as a cell-survival signaling molecule. Antioxid Redox Signal 2009; 11(11): 2655–2671.
- Kuban-Jankowska, A., Górska, M., Debicki, A., Popowska, U., Knap, N., Woźniak, M. Protein tyrosine phosphatases—endogenous markers of oxidative stress. Postepy Biochem 2010; 56(3): 269–273.
- Rajagopalan, S., Meng, X.P., Ramasamy, S., Harrison, D.G., Galis, Z.S. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. J Clin Invest 1996; 98: 2572–2579.
- Adler, V., Yin, Z., Tew, K.D., Ronai, Z. Role of redox potential and reactive oxygen species in stress signaling. Oncogene 1999; 18(45): 6104–6111.
- Lu, D., Maulik, N., Moraru, II., Kreutzer, D.L., Das, D.K. Molecular adaptation of vascular endothelial cells to oxidative stress. Am J Physiol Cell Physiol 1993; 264(3 Pt 1): C715–C722.
- Crawford, D.R., Davies, K.J. Adaptive response and oxidative stress. Environ Health Perspect 1994; 102 Suppl 10: 25–28.
- Bhunia, A.K., Arai, T., Bulkley, G., Chatterjee, S. Lactosylceramide mediates tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 (ICAM-1) expression and the adhesion of neutrophil in human umbilical vein endothelial cells. J Biol Chem 1998; 273(51): 34349–34357.
- Chen, X.L., Tummala, P.E., Olbrych, M.T., Alexander, R.W., Medford, R.M. Angiotensin II induces monocyte chemoattractant protein-1 gene expression in rat vascular smooth muscle cells. Circ Res 1998; 83(9): 952–959.
- Marumo, T., Schini-Kerth, V.B., Fisslthaler, B., Busse, R. Platelet-derived growth factor-stimulated superoxide anion production modulates activation of transcription factor NF-kappaB and expression of monocyte chemoattractant protein 1 in human aortic smooth muscle cells. Circulation 1997; 96(7): 2361–2367.
- Jung, K.A., Keak, M.K. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010; 15(10): 7266–7291.
- Katsuoka, F., Motohashi, H., Ishii, T., Aburatani, H., Engel, J.D., Yamamoto, M. Genetic evidence that small maf proteins are essential for the activation of antioxidant response element-dependent genes. Mol Cell Biol 2005; 25: 8044–8051.
- Motohashi, H., Katsuoka, F., Engel, J.D., Yamamoto, M. Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway. Proc Natl Acad Sci USA 2004; 101: 6379–6384.
- Prestera, T., Zhang, Y., Spencer, S.R., Wilczak, C.A., Talalay P. The electrophile counterattack response: protection against neoplasia and toxicity. Adv Enzyme Regul 1993; 33: 281–296.
- Rangasamy, T., Cho, C.Y., Thimmulappa, R.K., Zhen, L., Srisuma, S.S., Kensler, T.W., Yamamoto, M., Petrache, I., Tuder, R.M., Biswal, S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 2004; 114: 1248–1259.
- Rao, G.N., Alexander, R.W., Runge, M.S. Linoleic acid and its metabolites, hydroperoxyoctadecadienoic acids, stimulate c-fos,c-jun, and c-myc mRNA expression, mitogen-activated protein kinase activation, and growth in rat aortic smooth muscle cells. J Clin Invest 1995; 96 (2): 842–847.
- Spiecker, M., Darius, H., Kaboth, K., Hübner, F., Liao, J. K. Differential regulation of endothelial cell adhesion molecule expression by nitric oxide donors and antioxidants. J Leukoc Biol 1998; 63(6): 732–739.
- Barchowsky, A., Munro, S.R., Morana, S.J., Vincenti, M.P, Treadwell, M. Oxidant-sensitive and phosphorylation-dependent activation of NF-kappaB and AP-1 in endothelial cells. Am J Physiol Lung Mol Cell Physiol 1995; 269 (6 Pt 1): L829–L836.
- Dalton, T.P., Shertzer, H.G., Puga, A. Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol Toxicol 1999; 39: 67–101.
- Huang, L.E., Arany, Z., Livingston, D.M., Bunn, H.F. Activation of hypoxia-inducible transcription factor depends primarily on redox-sensitive stabilization of its subunit. J Biol Chem 1996; 271(50): 32253–32259.
- Matthews, J.R., Wakasugi, N., Virelizier, J.L., Yodoi, J., Hay, R.T. Thioredoxin regulates the DNA binding activity of NF-kappaB by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 1992; 20: 3821–3830.
- Mahieux, F. Hippocampal sclerosis and dementia. Psychol Neuropsychiatr Vieil 2003; 1: 179–186.
- Hyslop, P.A., Zhang, Z., Pearson, D.V., Phebus, L.A. Measurement of striatal H2O2 by microdialysis following global forebrain ischemia and reperfusion in the rat: correlation with the cytotoxic potential of H2O2 in vitro. Brain Res 1995; 671: 181–186.
- Kamsler, A., Segal, M. Hydrogen peroxide modulation of synaptic plasticity. J Neurosci 2003; 23: 269–276.
- Kamsler, A., Segal, M. Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol Neurobiol 2004; 29: 167–178.
- Hu, D., Serrano, F., Oury, T.D., Klann, E. Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 2006; 326: 3933–3941.
- Winder, D.G., Sweatt, J.D. Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nat Rev Neurosci 2001; 2: 461–474.
- Fukunaga, K., Muller, D., Ohmitsu, M., Bako, E., DePaoli-Roach, A.A., Miyamoto, E. Decreased protein phosphatase 2A activity in hippocampal long-term potentiation. J Neurochem 2000; 74: 807–817.
- Noh, H.S., Lee, H.P., Kim, D.W., Kang, S.S., Cho, G.J., Rho, J.M., Choi, W.S. A cDNA microarray analysis of gene expression profiles in rat hippocampus following a ketogenic diet. Brain Res Mol Brain Res 2004; 129: 80–87.
- Maalouf, M., Rho, J.M. Oxidative impairment of hippo-campal long-term potentiation involves activation of protein phosphatase 2A and is prevented by ketone bodies. J Neurosci Res 2008; 86: 3322–3330.
- Kamsler, A., Segal, M. Control of neuronal plasticity by reactive oxygen species. Antioxid Redox Signal 2007; 9: 165–167.
- Kishida, K.T., Klann, E. Sources and targets of reactive oxygen species in synaptic plasticity and memory. AntioxidRedox Signal 2007; 9: 233–249.
- Radi, R., Peluffo, G., Alvarez, M.N.; Naviliat, M., Cayota, A. Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med., 2001; 30: 463–488.
- Poppek, D., Grune, T. Proteasomal defense of oxidative protein modifications. AntioxidRedox Signal 2006; 8: 173–184.
- Haghdoost, S., Czene, S., Naslund, I., Skog, S., Harms-Ringdahl, M. Extracellular 8-oxo-dG as a sensitive parameter for oxidative stress in vivo and in vitro. Free Radic Res 2005; 39: 153–162.
- Squier, T.C. Oxidative stress and protein aggregation during biological aging. Exp Gerontol 2001; 36: 1539–1550.
- Poli, G., Leonarduzzi, G., Biasi, F., Chiarpotto, E. Oxidative stress and cell signalling. Curr Med Chem 2004; 11: 1163–1182.
- Farooqui, A.A. Neurochemical Aspects of Neurotraumatic and Neurodegenerative Diseases. New York: Springer, 2010.
- Hannun, Y.A., Obeid, L.M. The ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J Biol Chem 2002; 277: 25847–25850.
- Pamplona, R., Dalfó, E., Ayala, V., Bellmunt, M.J., Prat, J., Ferrer, I., Portero-Otín, M. Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation. Effects of Alzheimer disease and identification of lipoxidation targets. J Biol Chem 2005; 280: 21522–21530.
- Ray, P., Ray, R., Broomfield, C.A., Berman, J.D. Inhibition of bioenergetics alters intracellular calcium, membrane composition, and fluidity in a neuronal cell line. Neurochem Res 1994; 19: 57–63.
- Awasthi, Y.C., Yang, Y., Tiwari, N.K., Patrick, B., Sharma, A., Li, J., Awasthi, S. Regulation of 4-hydroxynonenal-mediated signaling by glutathione S-transferases. Free Radic Biol Med., 2004; 37: 607–619.
- Wang, C.C., Fang, K.M., Yang, C.S., Tzeng, S.F. (2009). Reactive oxygen species-induced cell death of rat primary astrocytes through mitochondria-mediated mechanism. J Cell Biochem 2009; 107: 933–943.
- Szabo, C. DNA strand breakage and activation of polyADP ribosyltransferase: a cytotoxic pathway triggered by peroxynitrite. Free Radic Biol Med 2003; 21: 855–869.
- Uehara, T. Accumulation of misfolded protein through nitrosative stress linked to neurodegenerative disorders. AntioxidRedox Signal 2007; 9: 597–601.
- Nakamura, T., Lipton, S.A. Cell death: protein misfolding and neurodegenerative diseases. Apoptosis 2009; 14: 455–468.
- Benhar, M., Forrester, M.T., Stamler, J.J. Nitrosative stress in the ER: a new role for S-nitrosylation in neuro-degenerative diseases. ACS Chem Biol 2006; 1: 355–358.
- He, J., Wang, T., Wang, P., Han, P., Chen, C. A novel mechanism underlying the susceptibility of neuronal cells to nitric oxide: the occurrence and regulation of protein S-nitrosylation is the checkpoint. J Neurochem 2007; 102: 1863–1874.
- Moncada, S., Bolanos, J.P. Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 2006; 97: 1676–1689.
- Farooqui, A.A., Horrocks, L.A., Farooqui, T. Interactions between neural membrane glycerophospholipid and sphingolipid mediators: a recipe for neural cell survival or suicide. J Neurosci Res 2007; 85: 1834–1850.
- Fraga, C.G., Shigenaga, M.K., Park, J.W., Degan, P., Ames, B.N. Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proc Natl Acad Sci USA 1990; 87(12): 4533–4537.
- Choudhury, S., Pan, J., Amin, S., Chung, F.L., Roy R. Repair kinetics of trans-4-hydroxynonenal-induced cyclic 1,N2-propanodeoxyguanine DNA adducts by human cell nuclear extracts. Biochemistry 2004; 43: 7514–7521.
- Huang, H., Kozekov, I.D., Kozekova, A., Wang, H., Lloyd, R.S., Rizzo, C.J., Stone, M.P. DNA cross-link induced by trans-4-hydroxynonenal. Environ Mol Mutagen 2010; 51: 625–634.
- Ahmad, R., Rasheed, Z., Ahsan, H. Biochemical and cellular toxicology of peroxynitrite: implications in cell death and autoimmune phenomenon. Immunopharmacol Immunotoxicol 2009; 31: 388–396.
- Wang, J.Y., Wen, L.L., Huang, Y.N., Chen, Y. T., Ku, M.C. Dual effects of antioxidants in neurodegeneration: direct neuroprotection against oxidative stress and indirect protection via suppression of glia-mediated inflammation. Curr Pharmaceut Design 2006; 12: 3521–3533.