A comparative study of protein carbonylation and mitochondrial dysfunction using the neurotoxicants 1,3-dinitrobenzene, 3-nitropropionic acid, and 3-chloropropanediol

NeuroToxicology

Volumn 37, Issue , 2013, Pages 74-84

  Steiner, Stephen R ^a,b   Milton, Evan ^a   Philbert, Martin A ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b NONE   (United States)

Author keywords

1,3 Dinitrobenzene; 3 Chloropropanediol; 3 Nitropropionic acid; Carbonylation; Mitochondria; Oxidative stress

Indexed keywords

1,3 DINITROBENZENE; 3 CHLOROPROPANEDIOL; 3 NITROPROPIONIC ACID; DEFEROXAMINE; FLUORESCENT DYE; NEUROTOXIN; TETRAMETHYL RHODAMINE METHYL ESTER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOTTING; CELL VIABILITY; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FLUORESCENCE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE CARBONYLATION; OXIDATIVE STRESS; OXYBLOT ANALYSIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN MODIFICATION; RAT; TANDEM MASS SPECTROMETRY;

ALPHA-CHLOROHYDRIN; ANIMALS; ANTIOXIDANTS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DINITROBENZENES; DOSE-RESPONSE RELATIONSHIP, DRUG; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEURONS; NITRO COMPOUNDS; OXIDATIVE STRESS; PROPIONATES; PROTEIN CARBONYLATION; RATS;

EID: 84877813802     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2013.04.004     Document Type: Article

References (42)

1. Aksenov M.Y., Aksenova M.V., Butterfield D.A., Geddes J.W., Markesbery W.R. Protein oxidation in the brain in Alzheimer's disease. Neuroscience 2001, 103:373-383.
2. Bizzozero O.A., Ziegler J.L., De Jesus G., Bolognani F. Acute depletion of reduced glutathione causes extensive carbonylation of rat brain proteins. J Neurosci Res 2006, 83:656-667.
3. Brown A.M., Skamarauskas J., Lister T., Madjd A., Ray D.E. Differential susceptibility of astrocytic and neuronal function to 3-chloropropanediol in the rat inferior colliculus. J Neurochem 2011, 116:996-1004.
4. Brouillet E., Guyot M.C., Mittoux V., Altairac S., Condé F., Palfi S., et al. Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J Neurochem 1998, 70:794-805.
5. Castegna A., Aksenov M., Aksenova M., Thongboonkerd V., Klein J.B., Pierce W.M., et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I. Creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 2002, 33:562-571.
6. Cavanagh J.B., Nolan C.C. The neurotoxicity of alpha-chlorohydrin in rats and mice. II. Lesion topography and factors in selective vulnerability in acute energy deprivation syndromes. Neuropathol Appl Neurobiol 1993, 19:471-479.
7. Ceccarini V., Gee J., Fioretti E., Amici M., Angeletti M., Eleuteri A.M., et al. Protein oxidation and cellular homeostasis: emphasis on metabolism. Biochem Biophys Acta 2007, 1773:93-104.
8. 25-35 in Alzheimer's fibroblasts. Biochim Biophys Acta 2003, 1637:135-141.
9. Cody T.E., Witherup S., Hastings L., Stemmer K., Christian R.T. 1,3-Dinitrobenzene: toxic effects in vivo and in vitro. J Toxicol Environ Health 1981, 7:829-847.
10. Dalle-Donne I., Aldini G., Carini M., Colombo R., Rossi R., Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med 2006, 10:389-406.
11. Dasgupta A., Zheng J., Bizzozero O.A. Protein carbonylation and aggregation precede neuronal apoptosis induced by partial glutathione depletion. ASN NEURO 2012, 4:161-174.
12. Dihazi H., Asif A.R., Agarwal N.K., Doncheva Y., Müller G.A. Proteomic analysis of cellular response to osmotic stress in thick ascending limb of Henle's loop (TALH) cells. Mol Cell Proteomics 2005, 4:1445-1458.
13. Floor E., Wetzel M.G. Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay. J Neurochem 1998, 70:268-275.
14. Gibson B.W. The human mitochondrial proteome: oxidative stress, protein modifications and oxidative phosphorylation. Int J Biochem Cell Biol 2005, 37:927-934.
15. Gould D.H., Wilson M.P., Hamar D.W. Brain enzyme and clinical alterations induced in rats and mice by nitroaliphatic toxicants. Toxicol Lett 1985, 27(1-3):83-89.
16. Huang L., Sun G., Cobessi D., Wang A.C., Shen J.T., Tung E.Y., et al. 3-Nitropropionic acid is a suicide inhibitor of mitochondrial respiration that, upon oxidation by complex II, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme. J Biol Chem 2006, 281:5965-5972.
17. Je J.H., Lee T.H., Kim D.H., Cho Y.H., Lee J.H., Kim S.C., et al. Mitochondrial ATP synthase is a target for TNBS-induced protein carbonylation in XS-106 dendritic cells. Proteomics 2008, 8:2384-2393.
18. Kuo M.W., Wang S.H., Chang J.C., Chang C.H., Huang L.J., Lin H.H., et al. A novel puf-A gene predicted from evolutionary analysis is involved in the development of eyes and primordial germ-cells. PLoS One 2009, 4(3):1-12.
19. La Fontaine M.A., Geddes J.W., Banks A., Butterfield D.A. 3-Nitropropionic acid induced in vivo protein oxidation in striatal and cortical synaptosomes: insights into Huntington's disease. Brain Res 2000, 858:356-362.
20. Linares M., Marín-García P., Méndez D., Puyet A., Diez A., Bautista J.M. Proteomic approaches to identifying carbonylated proteins in brain tissue. J Proteome Res 2011, 10:1719-1727.
21. Madian A.G., Regnier F.E. Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res 2011, 9:3766-3780.
22. Miller J.A., Runkle S.A., Tjalkens R.B., Philbert M.A. 1,3-Dinitrobenzene-induced metabolic impairment through inactivation of the pyruvate dehydrogenase complex. Toxicol Sci 2011, 122:502-511.
23. Nyström T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J 2005, 24:1311-1317.
24. Phelka A.D., Beck M.J., Philbert M.A. 1,3-Dinitrobenzene inhibits mitochondrial complex II in rat and mouse brainstem and cortical astrocytes. Neurotoxicology 2003, 24:403-415.
25. Philbert M.A., Nolan C.C., Cremer J.E., Tucker D., Brown A.W. 1,3-Dinitrobenzene-induced encephalopathy in rats. Neuropathol Appl Neurobiol 1987, 13:371-389.
26. Philbert M.A., Billingsley M.L., Reuhl K. Mechanisms of injury in the central nervous system. Toxicol Pathol 2000, 28:43-53.
27. Prokai L., Yan L.-J., Vera-Serrano J.L., Stevens S.M., Forster M.J. Mass spectrometry-based survey of age-associated protein carbonylation in rat brain mitochondria. J Mass Spectrom 2007, 42:1583-1589.
28. Rabek J.P., Boylston W.H., Papaconstantinou J. Carbonylation of ER chaperone proteins in aged mouse liver. Biochem Biophys Res Commun 2003, 305:566-572.
29. Radany E.H., Brenner M., Besnard F., Bigornia V., Bishop J.M., Deschepper C.F. Directed establishment of rat brain cell lines with the phenotypic characteristics of type 1 astrocytes. Proc Natl Acad Sci USA 1992, 89:6467-6471.
30. Romero I.A., Lister T., Richards H.K., Seville M.P., Wylie S.P., Ray D.E. Early metabolic changes during m-dinitrobenzene neurotoxicity and the possible role of oxidative stress. Free Radic Biol Med 1995, 18:311-319.
31. Romero I.A., Ray D.E., Chan M.W.K., Abbott N.J. An in vitro study of m-dinitrobenzene toxicity on the cellular components of the blood-brain barrier, astrocytes and endothelial cells. Toxicol Appl Pharmacol 1996, 139:94-101.
32. Sandhir R., Mehrotra A., Kamboj S.S. Lycopene prevents 3-nitroproprionic acid-induced mitochondrial oxidative stress and dysfunctions in nervous system. Neurochem Int 2010, 57:579-587.
33. Sas K., Robotka H., Toldi J., Vécsei L. Mitochondria, metabolic disturbances, oxidative stress and the kynurenine system, with focus on neurodegenerative disorders. J Neurol Sci 2007, 257:221-239.
34. Skamarauskas J., Carter W., Fowler M., Madjd A., Lister T., Mavroudis G., et al. The selective neurotoxicity produced by 3-chloropropanediol in the rat is not a result of energy deprivation. Toxicology 2007, 232:268-276.
35. Smerjac S.M., Bizzozero O.A. Cytoskeletal protein carbonylation and degradation in experimental autoimmune encephalomyelitis. J Neurochem 2008, 105:763-772.
36. Smith M.A., Sayre L.M., Anderson V.E., Harris P.L.R., Beal M.F., Kowall N., et al. Cytochemical demonstration of oxidative damage in Alzheimer disease by immunochemical enhancement of the carbonyl reaction with 2,4-dinitrophenylhydrazine. J Histochem Cytochem 1998, 46:731-735.
37. Steiner S.R., Philbert M.A. Proteomic identification of carbonylated proteins in 1,3-dinitrobenzene neurotoxicity. Neurotoxicology 2011, 32:362-373.
38. Temple A., Yen T., Gronert S. Identification of specific protein carbonylation sites in model oxidations of human serum albumin. J Am Soc Mass Spectrom 2006, 17:1172-1180.
39. Tengowski M.W., Feng D., Sutovsky M., Sutovsky P. Differential expression of genes encoding constitutive and inducible 20S proteasomal core subunits in the testis and epididymis of theophylline- or 1,3-dinitrobenzene-exposed rats. Biol Reprod 2007, 76:149-163.
40. Tjalkens R.B., Ewing M.M., Philbert M.A. Differential cellular regulation of the mitochondrial permeability transition in an in vitro model of 1,3-dinitrobenzene-induced encephalopathy. Brain Res 2000, 874:165-177.
41. Wang Y., Liu X., Schneider B., Zverina E.A., Russ K., Wijeyesakere S.J., et al. Mixed inhibition of adenosine deaminase activity by 1,3-dinitrobenzene: a model for understanding cell-selective neurotoxicity in chemically-induced energy deprivation syndromes in brain. Toxicol Sci 2012, 125:509-521.
42. Willis C.L., Nolan C.C., Reith S.N., Lister T., Prior M.J.W., Guerin C.J., et al. Focal astrocyte loss is followed by microvascular damage, with subsequent repair of the blood-brain barrier in the apparent absence of direct astrocyte contact. Glia 2004, 45:325-337.