Lipids and lipoxidation in human brain aging. Mitochondrial ATP-synthase as a key lipoxidation target

Lombard, 2012, The early evolution of lipid membranes and the three domains of life, Nat. Rev. Microbiol., 10, 507, 10.1038/nrmicro2815 Broadhurst, 2002, Brain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens, Comp. Biochem. Physiol. B. Biochem. Mol. Biol., 131, 653, 10.1016/S1096-4959(02)00002-7 Crawford, 2013, A quantum theory for the irreplaceable role of docosahexaenoic acid in neural cell signalling throughout evolution, Prostaglandins, Leukot. Essent. Fat. Acids, 88, 5, 10.1016/j.plefa.2012.08.005 Sastry, 1985, Lipids of nervous tissue: composition and metabolism, Prog. Lipid Res., 24, 69, 10.1016/0163-7827(85)90011-6 Piomelli, 2007, A neuroscientist's guide to lipidomics, Nat. Rev. Neurosci., 8, 743, 10.1038/nrn2233 Naudí, 2015, Lipidomics of human brain aging and Alzheimer's disease pathology, Int. Rev. Neurobiol., 122, 133, 10.1016/bs.irn.2015.05.008 Mattson, 2006, Ageing and neuronal vulnerability, Nat. Rev. Neurosci., 7, 278, 10.1038/nrn1886 Jové, 2014, Metabolomics of human brain aging and age-related neurodegenerative diseases, J. Neuropathol. Exp. Neurol., 73, 640, 10.1097/NEN.0000000000000091 O’Brien, 1965, Lipid composition of the normal human brain: gray matter, white matter, and myelin, J. Lipid Res., 6, 537, 10.1016/S0022-2275(20)39619-X Panganamala, 1971, Positions of double bonds in the monounsaturated alk-1-enyl groups from the plasmalogens of human heart and brain, Chem. Phys. Lipids, 6, 97, 10.1016/0009-3084(71)90031-4 Rouser, 1965, Lipid class composition of normal human brain and variations in Metachromatic Leucodystrophy, Tay-Sachs, Niemann-Pick, chronic Gaucher's and Alzheimer's diseases, J. Am. Oil Chem. Soc., 42, 404, 10.1007/BF02635576 Guan, 1994, Content and fatty acid composition of cardiolipin in the brain of patients with Alzheimer's disease, Neurochem. Int., 25, 295, 10.1016/0197-0186(94)90073-6 Hawrylycz, 2012, An anatomically comprehensive atlas of the adult human brain transcriptome, Nature, 489, 391, 10.1038/nature11405 Kim, 2014, A draft map of the human proteome, Nature, 509, 575, 10.1038/nature13302 Norris, 2015, Human prefrontal cortex phospholipids containing docosahexaenoic acid increase during normal adult aging, whereas those containing arachidonic acid decrease, Neurobiol. Aging, 36, 1659, 10.1016/j.neurobiolaging.2015.01.002 Hancock, 2015, Decreases in phospholipids containing adrenic and arachidonic acids occur in the human hippocampus over the adult lifespan, Lipids, 50, 861, 10.1007/s11745-015-4030-z Hancock, 2017, The phospholipid composition of the human entorhinal cortex remains relatively stable over 80 years of adult aging, GeroScience, 39, 73, 10.1007/s11357-017-9961-2 Yetukuri, 2008, Informatics and computational strategies for the study of lipids, Mol. Biosyst., 4, 121, 10.1039/B715468B Naudí, 1862, Region-specific vulnerability to lipid peroxidation and evidence of neuronal mechanisms for polyunsaturated fatty acid biosynthesis in the healthy adult human central nervous system, Biochim. Biophys. Acta, 2017, 485 Hulbert, 2007, Life and death: metabolic rate, membrane composition, and life span of animals, Physiol. Rev., 87, 1175, 10.1152/physrev.00047.2006 Pamplona, 2008, Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity, Biochim. Biophys. Acta, 1249, 10.1016/j.bbabio.2008.07.003 Möller, 2005, Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein, J. Biol. Chem., 280, 8850, 10.1074/jbc.M413699200 Gamliel, 2008, Determining radical penetration of lipid bilayers with new lipophilic spin traps, Free Radic. Biol. Med., 44, 1394, 10.1016/j.freeradbiomed.2007.12.028 Holman, 1954, Autoxidation of fats and related substances, Prog. Chem. Fats Other Lipids, 2, 51, 10.1016/0079-6832(54)90004-X Bielski, 1983, A study of the reactivity of HO2/O2- with unsaturated fatty acids, J. Biol. Chem., 258, 4759, 10.1016/S0021-9258(18)32488-8 Yin, 2011, Free radical lipid peroxidation: mechanisms and analysis, Chem. Rev., 111, 5944, 10.1021/cr200084z Esterbauer, 1991, Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes, Free Radic. Biol. Med., 11, 81, 10.1016/0891-5849(91)90192-6 Catalá, 2009, Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions, Chem. Phys. Lipids, 157, 1, 10.1016/j.chemphyslip.2008.09.004 Zimniak, 2011, Relationship of electrophilic stress to aging, Free Radic. Biol. Med., 51, 1087, 10.1016/j.freeradbiomed.2011.05.039 Fritz, 2013, An overview of the chemistry and biology of reactive aldehydes, Free Radic. Biol. Med., 59, 85, 10.1016/j.freeradbiomed.2012.06.025 Bernoud-Hubac, 2001, Formation of highly reactive γ-Ketoaldehydes (Neuroketals) as products of the neuroprostane pathway, J. Biol. Chem., 276, 30964, 10.1074/jbc.M103768200 Domingues, 2013, Lipoxidation adducts with peptides and proteins: deleterious modifications or signaling mechanisms?, J. Proteom., 92, 110, 10.1016/j.jprot.2013.06.004 Thorpe, 2003, Maillard reaction products in tissue proteins: new products and new perspectives, Amino Acids, 25, 275, 10.1007/s00726-003-0017-9 West, 2006, Endogenous reactive intermediates as modulators of cell signaling and cell death, Chem. Res. Toxicol., 19, 173, 10.1021/tx050321u Naudí, 2013, Non-enzymatic modification of aminophospholipids by carbonyl-amine reactions, Int. J. Mol. Sci., 14, 3285, 10.3390/ijms14023285 Pamplona, 2011, Advanced lipoxidation end-products, Chem. Biol. Interact., 192, 14, 10.1016/j.cbi.2011.01.007 Hannover, 1843, Mikroskopiske undersögelser af nerve systemet, det K, Dan. Vidensk. Selsk. Nat. Og. Math. Afh., 10, 1 Ottis, 2012, Human and rat brain lipofuscin proteome, Proteomics, 12, 2445, 10.1002/pmic.201100668 Higdon, 2012, Cell signalling by reactive lipid species: new concepts and molecular mechanisms, Biochem. J., 442, 453, 10.1042/BJ20111752 Brand, 2004, Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins, Free Radic. Biol. Med., 37, 755, 10.1016/j.freeradbiomed.2004.05.034 Echtay, 2003, A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling, EMBO J., 22, 4103, 10.1093/emboj/cdg412 Maher, 2010, The rise of antioxidant signaling--the evolution and hormetic actions of Nrf2, Toxicol. Appl. Pharmacol., 244, 4, 10.1016/j.taap.2010.01.011 Giles, 2009, Redox-controlled transcription factors and gene expression, 245 Imai, 2003, Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells, Free Radic. Biol. Med., 34, 145, 10.1016/S0891-5849(02)01197-8 Conrad, 2007, Physiological role of phospholipid hydroperoxide glutathione peroxidase in mammals, Biol. Chem., 388, 1019, 10.1515/BC.2007.130 Brigelius-Flohé, 2006, Glutathione peroxidases and redox-regulated transcription factors, Biol. Chem., 387, 1329, 10.1515/BC.2006.166 Casañas-Sánchez, 2015, Docosahexaenoic (DHA) modulates phospholipid-hydroperoxide glutathione peroxidase (Gpx4) gene expression to ensure self-protection from oxidative damage in hippocampal cells, Front. Physiol., 6, 203, 10.3389/fphys.2015.00203 Domínguez, 2016, Redox proteomic profiling of neuroketal-adducted proteins in human brain: regional vulnerability at middle age increases in the elderly, Free Radic. Biol. Med., 95, 1, 10.1016/j.freeradbiomed.2016.02.034 Domínguez-González, 2018, Regional vulnerability to lipoxidative damage and inflammation in normal human brain aging, Exp. Gerontol., 111, 218, 10.1016/j.exger.2018.07.023 Hagen, 2010, An allostatic control of membrane lipid composition by SREBP1, FEBS Lett., 584, 2689, 10.1016/j.febslet.2010.04.004 Burger, 1958, [Chemical biomorphosis of the human brain and sciatic nerve; a survey], Z. Alternsforsch., 12, 52 Rouser, 1968, Curvilinear regression course of human brain lipid composition changes with age, Lipids, 3, 284, 10.1007/BF02531202 Farooqui, 1988, Neurochemical aspects of Alzheimer's disease: involvement of membrane phospholipids, Metab. Brain Dis., 3, 19, 10.1007/BF01001351 Söderberg, 1990, Lipid compositions of different regions of the human brain during aging, J. Neurochem., 54, 415, 10.1111/j.1471-4159.1990.tb01889.x Svennerholm, 1991, Membrane lipids in the aging human brain, J. Neurochem., 56, 2051, 10.1111/j.1471-4159.1991.tb03466.x Svennerholm, 1994, Membrane lipids of adult human brain: lipid composition of frontal and temporal lobe in subjects of age 20 to 100 years, J. Neurochem., 63, 1802, 10.1046/j.1471-4159.1994.63051802.x Horrocks, 1981, Lipid changes in the ageing brain Martín, 2010, Lipid alterations in lipid rafts from Alzheimer's disease human brain cortex, J. Alzheimer's Dis., 19, 489, 10.3233/JAD-2010-1242 McNamara, 2008, The aging human orbitofrontal cortex: decreasing polyunsaturated fatty acid composition and associated increases in lipogenic gene expression and stearoyl-CoA desaturase activity, Prostaglandins, Leukot. Essent. Fat. Acids, 78, 293, 10.1016/j.plefa.2008.04.001 Cabré, 2018, Lipid profile in human frontal cortex is sustained throughout healthy adult lifespan to decay at advanced ages, J. Gerontol. Ser. A., 73, 703 Cabré, 2017, Sixty years old is the breakpoint of human frontal cortex aging, Free Radic. Biol. Med., 103, 14, 10.1016/j.freeradbiomed.2016.12.010 Braak, 2011, Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100 years, J. Neuropathol. Exp. Neurol., 70, 960, 10.1097/NEN.0b013e318232a379 Ferrer, 2012, Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia, Prog. Neurobiol., 97, 38, 10.1016/j.pneurobio.2012.03.005 Keller, 2004, Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain, Int. J. Biochem. Cell Biol., 36, 2376, 10.1016/j.biocel.2004.05.003 Gray, 2005, Lipofuscin and aging: a matter of toxic waste, Sci. Aging Knowl. Environ., 2005, 10.1126/sageke.2005.5.re1 Uhlen, 2015, Tissue-based map of the human proteome, Science, 347 Fernandez-Irigoyen, 2015, Toward defining the anatomo-proteomic puzzle of the human brain: an integrative analysis, Proteom. – Clin. Appl., 9, 796, 10.1002/prca.201400127 Ahmed, 2010, Protein modification and replicative senescence of WI-38 human embryonic fibroblasts, Aging Cell, 9, 252, 10.1111/j.1474-9726.2010.00555.x Oeste, 2014, Modification of cysteine residues by cyclopentenone prostaglandins: interplay with redox regulation of protein function, Mass Spectrom. Rev., 33, 110, 10.1002/mas.21383 Aldini, 2015, Protein lipoxidation: detection strategies and challenges, Redox Biol., 5, 253, 10.1016/j.redox.2015.05.003 Vistoli, 2017, Key factors regulating protein carbonylation by α,β unsaturated carbonyls: a structural study based on a retrospective meta-analysis, Biophys. Chem., 230, 20, 10.1016/j.bpc.2017.08.002 Harman, 2001, Aging: overview, Ann. N.Y. Acad. Sci., 928, 1, 10.1111/j.1749-6632.2001.tb05631.x Pamplona, 2006, Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection, Biochim. Biophys. Acta – Bioenergy, 1757, 496, 10.1016/j.bbabio.2006.01.009 Bishop, 2010, Neural mechanisms of ageing and cognitive decline, Nature, 464, 529, 10.1038/nature08983 Magistretti, 2000, Cellular bases of functional brain imaging: insights from neuron-glia metabolic coupling, Brain Res., 886, 108, 10.1016/S0006-8993(00)02945-0 Wallimann, 1992, Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the “phosphocreatine circuit” for cellular energy homeostasis, Biochem. J., 281, 21, 10.1042/bj2810021 Reed, 2008, Redox proteomic identification of 4-Hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role of lipid peroxidation in the progression and pathogenesis of Alzheimer's disease, Neurobiol. Dis., 30, 107, 10.1016/j.nbd.2007.12.007 Perluigi, 2009, Redox proteomics identification of 4-hydroxynonenal-modified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis, Proteom. - Clin. Appl., 3, 682, 10.1002/prca.200800161 Reed, 2009, Proteomic identification of HNE-bound proteins in early Alzheimer disease: insights into the role of lipid peroxidation in the progression of AD, Brain Res., 1274, 66, 10.1016/j.brainres.2009.04.009 Terni, 2010, Mitochondrial ATP-synthase in the entorhinal cortex is a target of oxidative stress at stages I/II of Alzheimer's disease pathology, Brain Pathol., 20, 222, 10.1111/j.1750-3639.2009.00266.x Di Domenico, 2017, Role of 4-hydroxy-2-nonenal (HNE) in the pathogenesis of alzheimer disease and other selected age-related neurodegenerative disorders, Free Radic. Biol. Med., 111, 253, 10.1016/j.freeradbiomed.2016.10.490 Burke, 2006, Neural plasticity in the ageing brain, Nat. Rev. Neurosci., 7, 30, 10.1038/nrn1809 Perry, 2013, Neurofilaments are the major neuronal target of hydroxynonenal-mediated protein cross-links, Free Radic. Res., 47, 507, 10.3109/10715762.2013.794265 Wataya, 2002, High molecular weight neurofilament proteins are physiological substrates of adduction by the lipid peroxidation product hydroxynonenal, J. Biol. Chem., 277, 4644, 10.1074/jbc.M110913200 Graham, 2017, Life and death in the trash heap: the ubiquitin proteasome pathway and UCHL1 in brain aging, neurodegenerative disease and cerebral Ischemia, Ageing Res. Rev., 34, 30, 10.1016/j.arr.2016.09.011 Boelens, 2014, Cell biological roles of αB-crystallin, Prog. Biophys. Mol. Biol., 115, 3, 10.1016/j.pbiomolbio.2014.02.005 Martínez de Toda, 2015, The role of Hsp70 in oxi-inflamm-aging and its use as a potential biomarker of lifespan, Biogerontology, 16, 709, 10.1007/s10522-015-9607-7 Porto, 2018, HSP70 facilitates memory consolidation of fear conditioning through MAPK pathway in the hippocampus, Neuroscience, 375, 108, 10.1016/j.neuroscience.2018.01.028 Deane, 2018, Knockdown of Heat Shock Proteins HSPA6 (Hsp70B’) and HSPA1A (Hsp70-1) sensitizes differentiated human neuronal cells to cellular stress, Neurochem. Res., 43, 340, 10.1007/s11064-017-2429-z Richarme, 2015, Parkinsonism-associated protein DJ-1/Park7 is a major protein deglycase that repairs methylglyoxal- and glyoxal-glycated cysteine, arginine, and lysine residues, J. Biol. Chem., 290, 1885, 10.1074/jbc.M114.597815 Wilhelmus, 2012, Involvement and interplay of Parkin, PINK1, and DJ1 in neurodegenerative and neuroinflammatory disorders, Free Radic. Biol. Med., 53, 983, 10.1016/j.freeradbiomed.2012.05.040 Wilson, 2011, The role of cysteine oxidation in DJ-1 function and dysfunction, Antioxid. Redox Signal., 15, 111, 10.1089/ars.2010.3481 Oh, 2018, Cytoprotective mechanisms of DJ-1 against oxidative stress through modulating ERK1/2 and ASK1 signal transduction, Redox Biol., 14, 211, 10.1016/j.redox.2017.09.008 Kiss, 2017, Structural features of human DJ-1 in distinct Cys106 oxidative states and their relevance to its loss of function in disease, Biochim. Biophys. Acta - Gen. Subj., 1861, 2619, 10.1016/j.bbagen.2017.08.017 Meulener, 2006, Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging, Proc. Natl. Acad. Sci. USA, 103, 12517, 10.1073/pnas.0601891103 Baranano, 2002, Biliverdin reductase: a major physiologic cytoprotectant, Proc. Natl. Acad. Sci. USA, 99, 16093, 10.1073/pnas.252626999 Biagioli, 2009, Unexpected expression of alpha- and beta-globin in mesencephalic dopaminergic neurons and glial cells, Proc. Natl. Acad. Sci. USA, 106, 15454, 10.1073/pnas.0813216106 Mayer, 2008 Hoppe, 2010, Life and destruction: ubiquitin-mediated proteolysis in aging and longevity, F1000 Biol. Rep., 2, 79, 10.3410/B2-79 Wagner, 2011, Quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles, Mol. Cell. Proteom., 10, 10.1074/mcp.M111.013284 McDowell, 2016, New insights into the role of ubiquitylation of proteins, Int. Rev. Cell Mol. Biol., 325, 35, 10.1016/bs.ircmb.2016.02.002 Kagawa, 1997, Genes of human ATP synthase: their roles in physiology and aging, Biosci. Rep., 17, 115, 10.1023/A:1027329328504 Allegretti, 2015, Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase, Nature, 521, 237, 10.1038/nature14185 Morales-Rios, 2015, Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallography at 4.0 Å resolution, Proc. Natl. Acad. Sci., 112, 13231, 10.1073/pnas.1517542112 Zhou, 2015, Structure and conformational states of the bovine mitochondrial ATP synthase by cryo-EM, Elife, 4, 10.7554/eLife.10180 Dautant, 2018, ATP synthase diseases of mitochondrial genetic origin, Front. Physiol., 9, 329, 10.3389/fphys.2018.00329 Hahn, 2016, Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology, Mol. Cell., 63, 445, 10.1016/j.molcel.2016.05.037 Parsons, 1963, Mitochondrial structure: two types of subunits on negatively stained mitochondrial membranes, Science, 140, 985, 10.1126/science.140.3570.985 Strauss, 2008, Dimer ribbons of ATP synthase shape the inner mitochondrial membrane, EMBO J., 27, 1154, 10.1038/emboj.2008.35 Duncan, 2016, Cardiolipin binds selectively but transiently to conserved lysine residues in the rotor of metazoan ATP synthases, Proc. Natl. Acad. Sci., 113, 8687, 10.1073/pnas.1608396113 Nesci, 2017, Post-translational modifications of the mitochondrial F1FO-ATPase, Biochim. Biophys. Acta - Gen. Subj., 1861, 2902, 10.1016/j.bbagen.2017.08.007 Pamplona, 2005, Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation, J. Biol. Chem., 280, 21522, 10.1074/jbc.M502255200