DOI QR코드

DOI QR Code

Salsolinol, a tetrahydroisoquinoline-derived neurotoxin, induces oxidative modification of neurofilament-L: protection by histidyl dipeptides

  • 투고 : 2011.10.07
  • 심사 : 2011.10.25
  • 발행 : 2012.02.29

초록

Salsolinol (1-methyl-6,7-dihydroxy-1,2,3,4-tetrahydroisoquinoline) is a compound derived from dopamine metabolism and is capable of causing dopaminergic neurodegeneration. Oxidative modification of neurofilament proteins has been implicated in the pathogenesis of neurodegenerative disorders. In this study, oxidative modification of neurofilament-L (NF-L) by salsolinol and the inhibitory effects of histidyl dipeptides on NF-L modification were investigated. When NF-L was incubated with 0.5 mM salsolinol, the aggregation of protein was increased in a time-dependent manner. We also found that the generation of hydroxyl radicals (${\bullet}OH$) was linear with respect to the concentrations of salsolinol as a function of incubation time. NF-L exposure to salsolinol produced losses of glutamate, lysine and proline residues. These results suggest that the aggregation of NF-L by salsolinol may be due to oxidative damage resulting from free radicals. Carnosine, histidyl dipeptide, is involved in many cellular defense processes, including free radical detoxification. Carnosine, and anserine were shown to significantly prevent salsolinol-mediated NF-L aggregation. Both compounds also inhibited the generation of ${\bullet}OH$ induced by salsolinol. The results indicated that carnosine and related compounds may prevent salsolinol-mediated NF-L modification via free radical scavenging.

키워드

참고문헌

  1. Naoi, M., Maruyama, W. and Nagy, G. M. (2004) Dopaminederived salsolinol derivatives as endogenous monoamine oxidase inhibitors: occurrence, metabolism and function in human brains. Neurotoxicology 25, 193-204. https://doi.org/10.1016/S0161-813X(03)00099-8
  2. Yi, S., Akao, Y., Maruyama, W., Chen, K., Siih, J. and Naoi, M. (2006) Type A monoamine oxidase is the target of an endogenous dopaminergic neurotoxin, N-methyl(R)salsolinol, leading to apoptosis in SH-SY5Y cells. J. Neurochem. 96, 541-549. https://doi.org/10.1111/j.1471-4159.2005.03573.x
  3. Gerlach, M., Koutsilieri, E. and Riederer, P. (1998) N-methyl-(R)-salsolinol and its relevance to Parkinson's disease. Lancet 351, 850-851. https://doi.org/10.1016/S0140-6736(05)70284-1
  4. Maruyama, W., Abe, T., Tohgi, H. and Naoi, M. (1999) An endogenous MPTP-like dopaminergic neurotoxin, N-methyl( R)salsolinol, in the cerebrospinal fluid decreases with progression of Parkinson's disease. Neurosci. Lett. 262, 13-16. https://doi.org/10.1016/S0304-3940(99)00003-8
  5. Naoi, M., Maruyama, W., Akao, Y. and Yi, H. (2002) Dopamine-derived endogenous N-methyl-(R)-salsolinol: its role in Parkinson's disease. Neurotoxicol. Teratol. 24, 579-591. https://doi.org/10.1016/S0892-0362(02)00211-8
  6. Deisenhammer, F., Egg, R., Giovannoni, G., Hemmer, B., Petzold, A., Sellebbjerg, F., Teunissen, C. and Tumani, H. (2009) EFNS guidelines on disease-specific CSF investigation. Eur. J. Neurol. 16, 760-770. https://doi.org/10.1111/j.1468-1331.2009.02595.x
  7. Petzold, A., Brassat, D., Mas, P., Rejdak, K., Keir, G., Giovannoni, G. and Thompson, E. J. (2004) Treatment response in relation to inflammatory and axonal surrogate markers in multiple sclerosis. Mult. Scler. 10, 281-283. https://doi.org/10.1191/1352458504ms1021sr
  8. Teunissen, C. E., Iacobaeus, E., Khademi, M., Brundin, L., Norgren, N., Koel-Simmelink, M. J., Schepens, M., Bouwman, F., Twaalfhoven, H. A., Blom, H. J., Jakobs, C. and Dijkstra, C. D. (2009) Combination of CSF N-acetylaspartate and neurofilaments in multiple sclerosis. Neurology 72, 1322-1329. https://doi.org/10.1212/WNL.0b013e3181a0fe3f
  9. Nixon, R. A. and Lewis, S. E. (1986) Differential turnover of phosphate groups on neurofilament subunits in mammalian neurons in vivo. J. Biol. Chem. 26, 16298-16301.
  10. Nixon, R. A. and Shea, T. B. (1992) Dynamics of neuronal intermediate filaments: a developmental perspective. Cell. Motil. Cytoskeleton. 22, 81-91. https://doi.org/10.1002/cm.970220202
  11. Perrot, R., Berges, R., Bocquet, A. and Eyer, J. (2008) Review of the multiple aspects of neurofilament functions and their possible contribution to neurodegeneration. Mol. Neurobiol. 38, 27-65. https://doi.org/10.1007/s12035-008-8033-0
  12. Shepherd, C. E., McCann, H., Thiel, E. and Halliday, G. M. (2002) Neurofilament-immunoreactive neurons in Alzheimer's disease and dementia with Lewy bodies. Neurobiol. Dis. 9, 249-257. https://doi.org/10.1006/nbdi.2001.0469
  13. Collard, J. F., Cote, F. and Jullien, J. P. (1995) Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375, 61-64. https://doi.org/10.1038/375061a0
  14. Riess, O., Kuhn, W. and Kruger, R. (2000) Genetic influence on the development of Parkinson's disease. J. Neurol. 247, II69-II74. https://doi.org/10.1007/PL00007764
  15. Kohen, R., Yamamoto, Y., Cundy, K. C. and Ames, B. N. (1988) Antioxidant activity of carnosine, homocarnosine, and anserine present in muscle and brain. Proc. Natl. Acad. Sci. U.S.A. 85, 3175-3179. https://doi.org/10.1073/pnas.85.9.3175
  16. Gille, J. J., Pasman, P., van Berkel, C. G. and Joenje, H. (1991) Effect of antioxidants on hyperoxia-induced chromosomal breakage in Chinese hamster ovary cells: protection by carnosine. Mutagenesis 6, 313-318. https://doi.org/10.1093/mutage/6.4.313
  17. Dobrota, D., Fedorova, T., Stvolinsky, S., Babusikova, E., Likaveanova, K., Drgova, A., Strapkova, A. and Boldyrev, A. (2005) Carnosine protects the brain of rats and Mongoliangerbils against ischemic injury: after-stroke-effect. Neurochem. Res. 30, 1283-1288. https://doi.org/10.1007/s11064-005-8799-7
  18. Ozel Turkcu, U., Bilgihan, A., Biberoglu, G. and Mertoglu Caglar, O. (2010) Carnosine supplementation protects rat brain tissue against ethanol-induced oxidative stress. Mol. Cell. Biochem. 339, 55-61. https://doi.org/10.1007/s11010-009-0369-x
  19. Stvolinsky, S., Kukley, M., Dobrota, D., Mezesova, V., Boldyrev, V. and Boldyrev, A. (2000) Carnosine protects rats under global ischemia. Brain Res. Bull. 53, 445-448. https://doi.org/10.1016/S0361-9230(00)00366-X
  20. Rahner, N., Holzmann, C., Kruger, R., Schols, L., Berger, K. and Riess, O. (2002) Neurofilament L gene is not a genetic factor of sporadic and familial Parkinson's disease. Brain Res. 951, 82-86. https://doi.org/10.1016/S0006-8993(02)03138-4
  21. Kim, H. J., Yoon, H. R., Washington, S., Chang, I. I. Oh, Y. J. and Surh, Y. J. (1997) DNA strand scission and PC12 cell death induced by salsolinol and copper. Neurosci. Lett. 238, 95-98. https://doi.org/10.1016/S0304-3940(97)00866-5
  22. Jung, Y. and Surh, Y. J. (2001) Oxidative DNA damage and cytotoxicity induced by copper-stimulated redox cycling of salsolinol, a neurotoxic tetrahydroisoquinoline alkaloid. Free Radic. Biol. Med. 30, 1407-1417. https://doi.org/10.1016/S0891-5849(01)00548-2
  23. Surh, Y. J., Jung, Y. J., Jang, J. H., Lee, J. S. and Yoon, H. R. (2002) Iron enhancement of oxidative DNA damage and neuronal cell death induced by salsolinol. J. Toxicol Environ. Health A. 65, 473-488. https://doi.org/10.1080/15287390252808127
  24. Halliwell, B. and Gutteridge, J. M. (1981) Formation of thiobarbituric-acid-reactive substance from deoxyribose in the presence of iron salts: the role of superoxide and hydroxyl radicals. FEBS Lett. 128, 347-352. https://doi.org/10.1016/0014-5793(81)80114-7
  25. Refsgaardm, H. H., Tsai, L. and Stadman, E. R. (2000) Modification of proteins by polyunsaturated fatty acid peroxidation products. Proc. Natl. Acad. Sci. U.S.A. 97, 611-616. https://doi.org/10.1073/pnas.97.2.611
  26. Ching, G. Y. and Liem, R. K. (1993) Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments. J. Cell. Biol. 122, 1323-1335. https://doi.org/10.1083/jcb.122.6.1323
  27. Lee, M. K., Xu, Z., Wong, P. C. and Cleveland, D. W. (1993) Neurofilaments are obligate heteropolymers in vivo. J. Cell. Biol. 122, 1337-1350. https://doi.org/10.1083/jcb.122.6.1337
  28. Geisler, N., Kaufmann, E., Fischer, S., Plessmann, U. and Weber, K. (1983) Neurofilament architecture combine structural principles of intermediate filaments with carboxyl-terminal extensions increasing in size between triplet proteins. EMBO J. 2, 1295-1302.
  29. Reilly, M. M. (2000) Classification of the hereditary motor and sensory neuropathies. Curr. Opin. Neurol. 13, 561-564. https://doi.org/10.1097/00019052-200010000-00009
  30. Brownlees, J., Ackerley, S., Grierson, A. J., Jacobsen, N. J., Shea, K., Anderton, B. H., Leigh, P. N., Shaw, C. E. and Miller, C. C. (2002) Charcot-Marie-Tooth disease neurofilament mutations disrupt neurofilament assembly and axonal transport. Hum. Mol. Genet. 11, 2837-2844. https://doi.org/10.1093/hmg/11.23.2837
  31. Perez-Olle, R., Jones, S. T. and Liem, R. K. (2004) Phenotypic analysis of neurofilament light gene mutations linked to Charcot-Marie-Tooth disease in cell culture models. Hum. Mol. Genet. 13, 2207-2220. https://doi.org/10.1093/hmg/ddh236
  32. Zhai, J., Lin, H., Julien, J.-P. and Schlaepfer, W. W. (2007) Disruption of neurofilament net work with aggregation of light neurofilament protein: a common pathway leading to motor neuron degeneration due to Charcot-Marie-Tooth diseaselinked mutations in NFL and HSPB1. Hum. Mol. Genet. 16, 3103-3116. https://doi.org/10.1093/hmg/ddm272
  33. Sasaki, T., Gotow, T., Shiozaki, M., Sakaue, F., Saito, T., Julien, J., Uchiyama, Y. and Isanaga, S. (2006) Aggregate formation and phosphorylation of neurofilament-L Pro22 Charcot-Marie-Tooth disease mutants. Hum. Mol. Gent. 15, 943-952. https://doi.org/10.1093/hmg/ddl011
  34. Boldyrev, A. A., Dupin, A. M., Pindel, E. V. and Severin, S. E. (1988) Antioxidative properties of histidine-containing dipeptides from skeletal muscles of vertebrates. Comp. Biochem. Physiol. 89, 245-250.
  35. Auroma, O. I., Laughton, M. J. and Halliwell, B. (1989) Carnosine, homocarnosine and anserine: could they act as antioxidants in vivo? Biochem. J. 264, 863-869. https://doi.org/10.1042/bj2640863
  36. Brown, C. E. (1981) Interactions among carnosine, anserine, ophidine and copper in biochemical adaptation. J. Theor. Biol. 88, 245-256. https://doi.org/10.1016/0022-5193(81)90073-4
  37. Decker, E. A., Crum, A. D. and Calvert, J. T. (1992) Differences in the Antioxidant mechanism of carnosine in the presence of copper and iron. J. Agric. Food Chem. 40, 756-759. https://doi.org/10.1021/jf00017a009
  38. Rajanikant, G. K., Zemke, D., Senut, M. C., Frenkel, M. B., Chen, A. F., Gupta, R. and Makid, A. (2007) Carnosine is neuroprotective against permanent focal cerebral ischemia in mice. Stroke 38, 3023-3031. https://doi.org/10.1161/STROKEAHA.107.488502
  39. Tabakman, R., Lazarovici, P. and Kohen, R. (2002) Neuroprotective effects of carnosine and homocarnosine on pheochromocytoma PC12 cells exposed to ischemia. J. Neurosci. Res. 68, 463-469. https://doi.org/10.1002/jnr.10228
  40. Aldini, G, Carini, M., Beretta, G., Bradamante, S. and Facino, R. M. (2002) Carnosine is a quencher of 4-hydroxy-nonenal: through what mechanism of reaction? Biochem. Biophys. Res. Commun. 298, 699-706. https://doi.org/10.1016/S0006-291X(02)02545-7
  41. Kim, N. H. and Kang, J. H. (2003) Oxidative modification of neurofilament-L by copper-catalyzed reaction. J. Biochem. Mol. Biol. 36, 488-492. https://doi.org/10.5483/BMBRep.2003.36.5.488
  42. Smith, M. A., Rudnicka-Nawrot, M., Richey, P. L., Praprotnik, D., Mulvihill, P., Miller, C. A., Sayre, L. M. and Perry, G. (1995) Carbonyl-related posttranslational modification of neurofilament protein in the neurofibrillary pathology of Alzheimer's disease. J. Neurochem. 64, 2660-2666. https://doi.org/10.1046/j.1471-4159.1995.64062660.x
  43. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685. https://doi.org/10.1038/227680a0
  44. Kim, N. H. and Kang, J. H. (2006) Oxidative damage of DNA induced by the cytochrome c and hydrogen peroxide system. J. Biochem. Mol. Biol. 39, 452-456. https://doi.org/10.5483/BMBRep.2006.39.4.452
  45. Hugli, T. E. and Moore, S. (1972) Determination of the tryptophan content of proteins by ion exchange chromatography of alkaline hydrolysates. J. Biol. Chem. 247, 2828-2834.

피인용 문헌

  1. Alpha-synuclein overexpression induced mitochondrial damage by the generation of endogenous neurotoxins in PC12 cells vol.547, 2013, https://doi.org/10.1016/j.neulet.2013.05.012
  2. Salsolinol, a catechol neurotoxin, induces oxidative modification of cytochrome c vol.46, pp.2, 2013, https://doi.org/10.5483/BMBRep.2013.46.2.220
  3. An Overview of Endogenous Catechol-Isoquinolines and Their Related Enzymes: Possible Biomarkers for Parkinson’s Disease vol.1, pp.2, 2012, https://doi.org/10.1007/s13670-012-0012-7
  4. Modification and inactivation of Cu,Zn-superoxide dismutase by the lipid peroxidation product, acrolein vol.46, pp.11, 2013, https://doi.org/10.5483/BMBRep.2013.46.11.138
  5. Salsolinol: an Unintelligible and Double-Faced Molecule—Lessons Learned from In Vivo and In Vitro Experiments vol.33, pp.2, 2018, https://doi.org/10.1007/s12640-017-9818-6
  6. Glycotoxins: Dietary and Metabolic Origins; Possible Amelioration of Neurotoxicity by Carnosine, with Special Reference to Parkinson’s Disease vol.34, pp.1, 2018, https://doi.org/10.1007/s12640-018-9867-5