Plasmalogen phospholipids protect internodal myelin from oxidative damage

Free Radical Biology and Medicine

Volumn 84, Issue , 2015, Pages 296-310

  Luoma, Adrienne M ^a,c   Kuo, Fonghsu ^a   Cakici, Ozgur ^a   Crowther, Michelle N ^a   Denninger, Andrew R ^a   Avila, Robin L ^a,d   Brites, Pedro ^b   Kirschner, Daniel A ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF CHICAGO   (United States)

^d Renovoneural Inc   (United States)

Author keywords

Abbreviations AD Alzheimer's disease; CNS central nervous system; HP hydrogen peroxide; MBP myelin basic protein; MS multiple sclerosis; OP ortho phenanthroline; OS oxidative stress; P0 myelin protein zero; PBS phosphate buffered saline; PLP myelin proteolipid protein; PNS peripheral nervous system; PUFA polyunsaturated fatty acid; ROS reactive oxygen species; XRD X ray diffraction.

Indexed keywords

1,10 PHENANTHROLINE; ASCORBIC ACID; COPPER; EDETIC ACID; FORMIC ACID; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MYELIN; PHOSPHOLIPID; PLASMALOGEN; REACTIVE OXYGEN METABOLITE; CELL RECEPTOR; CHELATING AGENT; FORMIC ACID DERIVATIVE; PEROXISOMAL TARGETING SIGNAL 2 RECEPTOR; SCAVENGER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EX VIVO STUDY; MOUSE; MYELIN SHEATH; NONHUMAN; OPTIC NERVE; OXIDATIVE STRESS; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CARBONYLATION; SCIATIC NERVE; TISSUE INJURY; X RAY DIFFRACTION; ANIMAL; DRUG EFFECTS; DRUG SCREENING; GENETICS; KNOCKOUT MOUSE; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY;

MURINAE; MUS; VERTEBRATA;

ANIMALS; CHELATING AGENTS; DRUG EVALUATION, PRECLINICAL; EDETIC ACID; FORMATES; FREE RADICAL SCAVENGERS; MICE, KNOCKOUT; MYELIN SHEATH; OPTIC NERVE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLASMALOGENS; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SCIATIC NERVE;

EID: 84929162848     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.03.012     Document Type: Article

References (86)

1. B. Halliwell, and J.M.C. Gutteridge Free radicals in biology and medicine 2007 Oxford University Press Oxford
2. J.R. Auclair, J.L. Johnson, Q. Liu, J.P. Salisbury, M.S. Rotunno, G.A. Petsko, D. Ringe, R.H. Brown Jr, D.A. Bosco, and J.N. Agar Post-translational modification by cysteine protects Cu/Zn-superoxide dismutase from oxidative damage Biochemistry 52 2013 6137 6144
3. J.M. McCord, and I. Fridovich Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J. Biol. Chem. 244 1969 6049 6055
4. M. Nordgren, and M. Fransen Peroxisomal metabolism and oxidative stress Biochimie 2013
5. E.R. Stadtman Protein oxidation and aging Science 257 1992 1220 1224
6. B. Halliwell Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344 1994 721 724
7. B. Su, X. Wang, A. Nunomura, P.I. Moreira, H.G. Lee, G. Perry, M.A. Smith, and X. Zhu Oxidative stress signaling in Alzheimer's disease Curr. Alzheimer Res. 5 2008 525 532
8. Miller, E.; Wachowicz, B.; Majsterek, I. Advances in antioxidative therapy of multiple sclerosis. Curr. Med. Chem.; 2013.
9. P. Kovacic, and R. Somanathan Redox processes in neurodegenerative disease involving reactive oxygen species Curr. Neuropharmacol. 10 2012 289 302
10. S.M. LeVine, and D.L. Wetzel Chemical analysis of multiple sclerosis lesions by FT-IR microspectroscopy Free Radic. Biol. Med. 25 1998 33 41
11. M. Chevion A site-specific mechanism for free radical induced biological damage: the essential role of redox-active transition metals Free Radic. Biol. Med. 5 1988 27 37
12. L.H. Sanders, and J. Timothy Greenamyre Oxidative damage to macromolecules in human Parkinson disease and the rotenone model Free Radic. Biol. Med. 62 2013 111 120
13. G.R. Buettner, and B.A. Jurkiewicz Catalytic metals, ascorbate and free radicals: combinations to avoid Radiat. Res. 145 1996 532 541
14. K.L. Fong, P.B. McCay, J.L. Poyer, B.B. Keele, and H. Misra Evidence that peroxidation of lysosomal membranes is initiated by hydroxyl free radicals produced during flavin enzyme activity J. Biol. Chem. 248 1973 7792 7797
15. J. McCord, and E.J. Day Superoxide-dependent production of hydroxyl radical catalyzed by iron-EDTA complex FEBS Lett. 86 1978
16. P. Wardman, and L.P. Candeias Fenton chemistry: an introduction Radiat. Res. 145 1996 523 531
17. S.E. Fridovich, and N.A. Porter Oxidation of arachidonic acid in micelles by superoxide and hydrogen peroxide J. Biol. Chem. 256 1981 260 265
18. E.R. Stadtman Metal ion-catalyzed oxidation of proteins: biochemical mechanism and biological consequences Free Radic. Biol. Med. 9 1990 315 325
19. E. Shinar, T. Navok, and M. Chevion The analogous mechanisms of enzymatic inactivation induced by ascorbate and superoxide in the presence of copper J. Biol. Chem. 258 1983 14778 14783
20. J.M. Gutteridge, and S. Wilkins Copper salt-dependent hydroxyl radical formation. Damage to proteins acting as antioxidants Biochim. Biophys. Acta 759 1983 38 41
21. J.S. Valentine, D.L. Wertz, T.J. Lyons, L.L. Liou, J.J. Goto, and E.B. Gralla The dark side of dioxygen biochemistry Curr. Opin. Chem. Biol. 2 1998 253 262
22. J.M. Gutteridge, and B. Halliwell The role of the superoxide and hydroxyl radicals in the degradation of DNA and deoxyribose induced by a copper-phenanthroline complex Biochem. Pharmacol. 31 1982 2801 2805
23. M. Valko, H. Morris, and M.T. Cronin Metals, toxicity and oxidative stress Curr. Med. Chem. 12 2005 1161 1208
24. K.J. Smith, R. Kapoor, and P.A. Felts Demyelination: the role of reactive oxygen and nitrogen species Brain Pathol. 9 1999 69 92
25. E.G. Tonkin, H.L. Valentine, D.M. Milatovic, and W.M. Valentine N,N-diethyldithiocarbamate produces copper accumulation, lipid peroxidation, and myelin injury in rat peripheral nerve Toxicol. Sci. 81 2004 160 171
26. F.J. Romero Antioxidants in peripheral nerve Free Radic. Biol. Med. 20 1996 925 932
27. Myelin biology and disorders R.A. Lazzarini 2004 Elsevier/Academic Press Amsterdam
28. S. Gebicki, and J.M. Gebicki Formation of peroxides in amino acids and proteins exposed to oxygen free radicals Biochem. J. 289 1993 743 749
29. K.J. Davies, M.E. Delsignore, and S.W. Lin Protein damage and degradation by oxygen radicals. II. Modification of amino acids J. Biol. Chem. 262 1987 9902 9907
30. D.G. Deavall, E.A. Martin, J.M. Horner, and R. Roberts Drug-induced oxidative stress and toxicity J. Toxicol 2012 2012 645460
31. S.P. Wolff, and R.T. Dean Fragmentation of proteins by free radicals and its effect on their susceptibility to enzymic hydrolysis Biochem. J. 234 1986 399 403
32. G. Bartzokis Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease Neurobiol. Aging 25 2004 5 18 author reply 49-62
33. A.A. Farooqui, and L.A. Horrocks Plasmalogens: workhorse lipids of membranes in normal and injured neurons and glia Neuroscientist 7 2001 232 245
34. S. Aggarwal, L. Yurlova, and M. Simons Central nervous system myelin: structure, synthesis and assembly Trends Cell Biol. 21 2011 585 593
35. O.H. Morand, R.A. Zoeller, and C.R. Raetz Disappearance of plasmalogens from membranes of animal cells subjected to photosensitized oxidation J. Biol. Chem. 263 1988 11597 11606
36. R.A. Zoeller, O.H. Morand, and C.R. Raetz A possible role for plasmalogens in protecting animal cells against photosensitized killing J. Biol. Chem. 263 1988 11590 11596
37. D. Reiss, K. Beyer, and B. Engelmann Delayed oxidative degradation of polyunsaturated diacyl phospholipids in the presence of plasmalogen phospholipids in vitro Biochem. J. 323 Pt 3 1997 807 814
38. J. Lessig, and B. Fuchs Plasmalogens in biological systems: their role in oxidative processes in biological membranes, their contribution to pathological processes and aging and plasmalogen analysis Curr. Med. Chem. 16 2009 2021 2041
39. R.L. Avila, H. Inouye, R. Baek, X. Yin, B.D. Trapp, M.L. Feltri, L. Wrabetz, and D.A. Kirschner Structure and stability of internodal myelin in mouse models of hereditary neuropathy J. Neuropathol. Exp. Neurol. 64 2005 976 990
40. P. Brites, A.M. Motley, P. Gressens, P.A. Mooyer, I. Ploegaert, V. Everts, P. Evrard, P. Carmeliet, M. Dewerchin, L. Schoonjans, M. Duran, H.R. Waterham, R.J. Wanders, and M. Baes Impaired neuronal migration and endochondral ossification in Pex7 knockout mice: a model for rhizomelic chondrodysplasia punctata Hum. Mol. Genet 12 2003 2255 2267
41. P. Brites, P.A. Mooyer, L. El Mrabet, H.R. Waterham, and R.J. Wanders Plasmalogens participate in very-long-chain fatty acid-induced pathology Brain 132 2009 482 492
42. B. Kosaras, and D.A. Kirschner Radial component of CNS myelin: junctional subunit structure and supramolecular assembly J. Neurocytol. 19 1990 187 199
43. W.T. Norton, and S.E. Poduslo Myelination in rat brain: method of myelin isolation J. Neurochem. 21 1973 749 757
44. R.L. Avila, M. D'Antonio, A. Bachi, H. Inouye, M.L. Feltri, L. Wrabetz, and D.A. Kirschner P0 (protein zero) mutation Ser34Cys underlies instability of internodal myelin in S63C mice J. Biol. Chem. 285 2010 42001 42012
45. D.A. Kirschner, and C.J. Hollingshead Processing for electron microscopy alters membrane structure and packing in myelin J. Ultrastruct. Res. 73 1980 211 232
46. P.C. Chan, O.G. Peller, and L. Kesner Copper(II)-catalyzed lipid peroxidation in liposomes and erythrocyte membranes Lipids 17 1982 331 337
47. B.G. Que, K.M. Downey, and A.G. So Degradation of deoxyribonucleic acid by a 1,10-phenanthroline-copper complex: the role of hydroxyl radicals Biochemistry 19 1980 5987 5991
48. B. Stinefelt, S.S. Leonard, K.P. Blemings, X. Shi, and H. Klandorf Free radical scavenging, DNA protection, and inhibition of lipid peroxidation mediated by uric acid Ann. Clin. Lab. Sci. 35 2005 37 45
49. S. Stadelmann-Ingrand, S. Favreliere, B. Fauconneau, G. Mauco, and C. Tallineau Plasmalogen degradation by oxidative stress: production and disappearance of specific fatty aldehydes and fatty alpha-hydroxyaldehydes Free Radic. Biol. Med. 31 2001 1263 1271
50. D.A. Kirschner, and A.E. Blaurock Organization, phylogenetic variations and dynamic transitions of myelin structure R.E. Martenson, Myelin: biology and chemistry 1992 CRC Press Boca Raton 3 78
51. D.A. Kirschner, L. Wrabetz, and M.L. Feltri The P0 gene R.A. Lazzarini, J.W. Griffin, H. Lassmann, K.-A. Nave, R.H. Miller, B.D. Trapp, Myelin biology and disorders 1 2004 Elsevier/Academic Press Amsterdam 523 545
52. L. Shapiro, J.P. Doyle, P. Hensley, D.R. Colman, and W.A. Hendrickson Crystal structure of the extracellular domain from P0, the major structural protein of peripheral nerve myelin Neuron 17 1996 435 449
53. X. Yin, R.C. Baek, D.A. Kirschner, A. Peterson, Y. Fujii, K.A. Nave, W.B. Macklin, and B.D. Trapp Evolution of a neuroprotective function of central nervous system myelin J. Cell Biol. 172 2006 469 478
54. J.M. Gutteridge Reactivity of hydroxyl and hydroxyl-like radicals discriminated by release of thiobarbituric acid-reactive material from deoxy sugars, nucleosides and benzoate Biochem. J. 224 1984 761 767
55. A. Samuni, J. Aronovitch, D. Godinger, M. Chevion, and G. Czapski On the cytotoxicity of vitamin C and metal ions. A site-specific Fenton mechanism Eur. J. Biochem. 137 1983 119 124
56. E.R. Bongarzone, J.M. Pasquini, and E.F. Soto Oxidative damage to proteins and lipids of CNS myelin produced by in vitro generated reactive oxygen species J. Neurosci. Res. 41 1995 213 221
57. G.W. Konat, and R.C. Wiggins Effect of reactive oxygen species on myelin membrane proteins J. Neurochem. 45 1985 1113 1118
58. D.A. Kirschner, and D.L. Caspar Myelin structure transformed by dimethylsulfoxide Proc. Natl. Acad. Sci. USA 72 1975 3513 3517
59. C.J. Hollingshead, D.L. Caspar, V. Melchior, and D.A. Kirschner Compaction and particle segregation in myelin membrane arrays J. Cell Biol. 89 1981 631 644
60. Y. Fu, H. Wang, T.B. Huff, R. Shi, and J.X. Cheng Coherent anti-Stokes Raman scattering imaging of myelin degradation reveals a calcium-dependent pathway in lyso-PtdCho-induced demyelination J. Neurosci. Res. 85 2007 2870 2881
61. S.C. Payne, C.A. Bartlett, A.R. Harvey, S.A. Dunlop, and M. Fitzgerald Myelin sheath decompaction, axon swelling, and functional loss during chronic secondary degeneration in rat optic nerve Invest. Ophthalmol. Vis. Sci. 53 2012 6093 6101
62. J. Nagai, H. Uchida, Y. Matsushita, R. Yano, M. Ueda, M. Niwa, J. Aoki, J. Chun, and H. Ueda Autotaxin and lysophosphatidic acid1 receptor-mediated demyelination of dorsal root fibers by sciatic nerve injury and intrathecal lysophosphatidylcholine Mol. Pain 6 2010 78
63. D.A. Kirschner, C.J. Hollingshead, C. Thaxton, D.L. Caspar, and D.A. Goodenough Structural states of myelin observed by x-ray diffraction and freeze-fracture electron microscopy J. Cell Biol. 82 1979 140 149
64. A.T. Campagnoni, and R.P. Skoff The pathobiology of myelin mutants reveal novel biological functions of the MBP and PLP genes Brain Pathol. 11 2001 74 91
65. N.P. Franks, V. Melchior, D.A. Kirshner, and D.L. Caspar Structure of myelin lipid bilayers. Changes during maturation J. Mol. Biol. 155 1982 133 153
66. J.P. Castro, C. Ott, T. Jung, T. Grune, and H. Almeida Carbonylation of the cytoskeletal protein actin leads to aggregate formation Free Radic. Biol. Med. 53 2012 916 925
67. T. Nystrom Role of oxidative carbonylation in protein quality control and senescence EMBO J. 24 2005 1311 1317
68. R.T. Hamilton, A. Bhattacharya, M.E. Walsh, Y. Shi, R. Wei, Y. Zhang, K.A. Rodriguez, R. Buffenstein, A.R. Chaudhuri, and H. Van Remmen Elevated protein carbonylation, and misfolding in sciatic nerve from db/db and Sod1(-/-) mice: plausible link between oxidative stress and demyelination PLoS One 8 2013 e65725
69. I. Dalle-Donne, R. Rossi, R. Colombo, D. Giustarini, and A. Milzani Biomarkers of oxidative damage in human disease Clin. Chem. 52 2006 601 623
70. D.A. Bota, H. Van Remmen, and K.J. Davies Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress FEBS Lett. 532 2002 103 106
71. T. Grune, T. Jung, K. Merker, and K.J. Davies Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease Int. J. Biochem. Cell Biol. 36 2004 2519 2530
72. E. Maisonneuve, L. Fraysse, S. Lignon, L. Capron, and S. Dukan Carbonylated proteins are detectable only in a degradation-resistant aggregate state in Escherichia coli J. Bacteriol. 190 2008 6609 6614
73. K.M. Schaich Metals and lipid oxidation. Contemporary issues Lipids 27 1992 209 218
74. S. Goldstein, and G. Czapski The role and mechanism of metal ions and their complexes in enhancing damage in biological systems or in protecting these systems from the toxicity of O2 J. Free Radic. Biol. Med. 2 1986 3 11
75. H. Inouye, and D.A. Kirschner Membrane interactions in nerve myelin. I. Determination of surface charge from effects of pH and ionic strength on period Biophys. J. 53 1988 235 245
76. A. Teigler, D. Komljenovic, A. Draguhn, K. Gorgas, and W.W. Just Defects in myelination, paranode organization and Purkinje cell innervation in the ether lipid-deficient mouse cerebellum Hum. Mol. Genet 18 2009 1897 1908
77. C. Rodemer, T.P. Thai, B. Brugger, T. Kaercher, H. Werner, K.A. Nave, F. Wieland, K. Gorgas, and W.W. Just Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice Hum. Mol. Genet 12 2003 1881 1895
78. T. Aboshi, R. Nishida, and N. Mori Identification of plasmalogen in the gut of silkworm (Bombyx mori) Insect Biochem. Mol. Biol. 42 2012 596 601
79. R. Chrast, G. Saher, K.A. Nave, and M.H. Verheijen Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models J. Lipid Res. 52 2011 419 434
80. D.A. Kirschner, and A.L. Ganser Myelin labeled with mercuric chloride. Asymmetric localization of phosphatidylethanolamine plasmalogen J. Mol. Biol. 157 1982 635 658
81. A. Broniec, R. Klosinski, A. Pawlak, M. Wrona-Krol, D. Thompson, and T. Sarna Interactions of plasmalogens and their diacyl analogs with singlet oxygen in selected model systems Free Radic. Biol. Med. 50 2011 892 898
82. S. Morandat, M. Bortolato, G. Anker, A. Doutheau, M. Lagarde, J.P. Chauvet, and B. Roux Plasmalogens protect unsaturated lipids against UV-induced oxidation in monolayer Biochim. Biophys. Acta 1616 2003 137 146
83. R.C. Murphy Free-radical-induced oxidation of arachidonoyl plasmalogen phospholipids: antioxidant mechanism and precursor pathway for bioactive eicosanoids Chem. Res. Toxicol. 14 2001 463 472
84. S. Stadelmann-Ingrand, R. Pontcharraud, and B. Fauconneau Evidence for the reactivity of fatty aldehydes released from oxidized plasmalogens with phosphatidylethanolamine to form Schiff base adducts in rat brain homogenates Chem. Phys. Lipids 131 2004 93 105
85. P.J. Sindelar, Z. Guan, G. Dallner, and L. Ernster The protective role of plasmalogens in iron-induced lipid peroxidation Free Radic. Biol. Med. 26 1999 318 324
86. H. Nagara, and K. Suzuki Radial component of the central myelin in neurologic mutant mice Lab. Invest. 47 1982 51 59