1. Institute of Biomedical Chemistry, Moscow, Russia 2. Institute of Biomedical Chemistry, Moscow, Russia; Zakusov Institute of Pharmacology, Moscow, Russia
Parkinsonism in rats induced by the pesticide rotenone is one of the most adequate models of Parkinson's disease (PD). Isatin (indole-2,3-dione) is an endogenous regulator found in mammals and humans and exhibiting a wide range of biological activities mediated by numerous isatin-binding proteins, including those associated with neurodegenerative pathology. A course of rotenone administration to rats caused behavioral impairments and changes in the profile and relative content of isatin-binding proteins in the brain. In this study, we have investigated the delayed neuroprotective effect of isatin (5 days after completion of the course of rotenone administration) on behavioral reactions and the relative content of isatin-binding proteins in the brain of rats with rotenone-induced experimental parkinsonism. Although during this period the rats retained locomotor dysfunction, the proteomic analysis data (profile of isatin-binding proteins in the brain and changes in their relative content) differed from the results obtained immediately after completion of the course of rotenone administration. Moreover, all isatin-binding proteins with altered relative content changed during this period are associated to varying degrees with neurodegeneration (many with Parkinson's and Alzheimer's diseases).
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Keywords: isatin, isatin-binding proteins in the brain, parkinsonism, rotenone, neurodegeneration, neuroprotectors, proteomic profiling
Citation:
Buneeva O.A., Kapitsa I.G., Kazieva L.Sh., Vavilov N.E., Zgoda V.G., Medvedev A.E. (2024) The neuroprotective effect of isatin in the rotenone-induced model of parkinonism in rats: the study of delayed effects. Biomeditsinskaya Khimiya, 70(4), 231-239.
Buneeva O.A. et al. The neuroprotective effect of isatin in the rotenone-induced model of parkinonism in rats: the study of delayed effects // Biomeditsinskaya Khimiya. - 2024. - V. 70. -N 4. - P. 231-239.
Buneeva O.A. et al., "The neuroprotective effect of isatin in the rotenone-induced model of parkinonism in rats: the study of delayed effects." Biomeditsinskaya Khimiya 70.4 (2024): 231-239.
Buneeva, O. A., Kapitsa, I. G., Kazieva, L. Sh., Vavilov, N. E., Zgoda, V. G., Medvedev, A. E. (2024). The neuroprotective effect of isatin in the rotenone-induced model of parkinonism in rats: the study of delayed effects. Biomeditsinskaya Khimiya, 70(4), 231-239.
References
Duty S., Jenner P. (2011) Animal models of Parkinson's disease: A source of novel treatments and clues to the cause of the disease. Br. J. Pharmacol., 164(4), 1357–1391. CrossRef Scholar google search
Fleming S.M., Zhu C., Fernagut P.O., Mehta A., Dicarlo C.D., Seaman R.L., Chesselet M.F. (2004) Behavioral and immunohistochemical effects of chronic intravenous and subcutaneous infusions of varying doses of rotenone. Exp. Neurol., 187(2), 418–429. CrossRef Scholar google search
Fleming S.M., Salcedo J., Fernagut P.O., Rockenstein E., Masliah E., Levine M.S., Chesselet M.F. (2004) Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J. Neurosci., 24(42), 9434–9440. CrossRef Scholar google search
Cannon J.R., Tapias V.M., Na H.M., Honick A.S., Drolet R.E., Greenamyre J.T. (2009) A highly reproducible rotenone model of Parkinson’s disease. Neurobiol. Dis., 34(2), 279–290. CrossRef Scholar google search
Kapitsa I.G., Kazieva L.S., Vavilov N.E., Zgoda V.G., Kopylov A.T., Medvedev A.E., Buneeva O.A. (2023) Characteristics of behavioral reactions and the profile of brain isatin-binding proteins of rats with the rotenone-induced experimental parkinsonism. Biomeditsinskaya Khimiya, 69(1), 46–54. CrossRef Scholar google search
Buneeva O.A., Kapitsa I.G., Kazieva L.S., Vavilov N.E., Zgoda V.G., Medvedev A.E. (2024) The delayed effect of rotenone on the relative content of brain isatin-binding proteins of rats with experimental parkinsonism. Biomeditsinskaya Khimiya, 70(1), 25–32. CrossRef Scholar google search
Medvedev A., Igosheva N., Crumeyrolle-Arias M., Glover V. (2005) Isatin: Role in stress and anxiety. Stress, 8(3), 175–183. CrossRef Scholar google search
Medvedev A., Buneeva O., Glover V. (2007) Biological targets for isatin and its analogues: Implications for therapy. Biologics, 1(2), 151–162. Scholar google search
Medvedev A., Buneeva O., Gnedenko O., Ershov P., Ivanov A. (2018) Isatin, an endogenous non-peptide biofactor: A review of its molecular targets, mechanisms of actions and their biomedical implications. Biofactors, 44, 95–108. CrossRef Scholar google search
Medvedev A., Buneeva O. (2022) Tryptophan metabolites as mediators of microbiota-gut-brain communication: Focus on isatin. Front. Behav. Neurosci., 16, 922274. CrossRef Scholar google search
Buneeva O., Gnedenko O., Zgoda V., Kopylov A., Glover V., Ivanov A., Medvedev A., Archakov A. (2010) Isatin binding proteins of rat and mouse brain: Proteomic identification and optical biosensor validation. Proteomics, 10, 23–37. CrossRef Scholar google search
Buneeva O., Kopylov A., Kapitsa I., Ivanova E., Zgoda V., Medvedev A. (2018) The effect of neurotoxin MPTP and neuroprotector isatin on the profile of ubiquitinated brain mitochondrial proteins. Cells, 7(8), 91. CrossRef Scholar google search
Buneeva O.A., Kapitsa I.G., Ivanova E.A., Kopylov A.T., Zgoda V.G., Medvedev A.E. (2019) The effect of a neuroprotective dose of isatin or deprenyl to mice on the profile of brain isatin-binding proteins. Biomeditsinskaya Khimiya, 65(5), 407–417. CrossRef Scholar google search
Buneeva O.A., Kapitsa I.G., Kazieva L.S., Vavilov N.E., Zgoda V.G., Medvedev A.E. (2023) Quantitative changes of brain isatin-binding proteins of rats with the rotenone-induced experimental parkinsonism. Biomeditsinskaya Khimiya, 69(3), 188–192. CrossRef Scholar google search
Voronina T.A., Seredenin S.B., Yarkova M.A., Voronin M.V. (2012) Rukovodstvo po provedeniyu doklinicheskih issledovanij lekarstvennyh sredstv, chast' pervaya (Mironov A.N. (ed.)), Grif i K, Moskva, 994 p. Scholar google search
Buneeva O.A., Kapitsa I.G., Zgoda V.G., Medvedev A.E. (2023) Neuroprotective effects of isatin and afobazole in rats with rotenone-induced parkinsonism are accompanied by increased brain levels of Triton X-100 soluble alpha-synuclein. Biomeditsinskaya Khimiya, 69(5), 290–299. CrossRef Scholar google search
Barinova K., Khomyakova E., Semenyuk P., Schmalhausen E., Muronetz V. (2018) Binding of alpha-synuclein to partially oxidized glyceraldehyde-3-phosphate dehydrogenase induces subsequent inactivation of the enzyme. Arch. Biochem. Biophys., 642, 10–22. CrossRef Scholar google search
Gerszon J., Rodacka A. (2018) Oxidatively modified glyceraldehyde-3-phosphate dehydrogenase in neurodegenerative processes and the role of low molecular weight compounds in counteracting its aggregation and nuclear translocation. Ageing Res. Rev., 48, 21–31. CrossRef Scholar google search
Zhao Y., Zhang M., Li H., Yang Y., Lu X., Yu J., Pan L. (2023) Aldo-keto reductase 1B: Much learned, much more to do. HLife, 2023, DOI: 10.1016/j.hlife.2023.12.002. CrossRef Scholar google search
Lewczuk P., Ermann N., Andreasson U., Schultheis C., Podhorna J., Spitzer P., Maler J.M., Kornhuber J., Blennow K., Zetterberg H. (2018) Plasma neurofilament light as a potential biomarker of neurodegeneration in Alzheimer's disease. Alzheimers Res. Ther., 10(1), 71. CrossRef Scholar google search
Song D.G., Kim Y.S., Jung B.C., Rhee K.J., Pan C.H. (2013) Parkin induces upregulation of 40S ribosomal protein SA and posttranslational modification of cytokeratins 8 and 18 in human cervical cancer cells. Appl. Biochem. Biotechnol., 171(7),1630–1638. CrossRef Scholar google search
Martinez V.J., Asico L.D., Jose P.A., Tiu A.C. (2020) Lipid rafts and dopamine receptor signaling. Int. J. Mol. Sci., 21(23), 8909. CrossRef Scholar google search
Zhang X., Zhou J.Y., Chin M.H., Schepmoes A.A., Petyuk V.A., Weitz K.K., Petritis B.O., Monroe M.E., Camp D.G., Wood S.A., Melega W.P., Bigelow D.J., Smith D.J., Qian W.J., Smith R.D. (2010) Region-specific protein abundance changes in the brain of MPTP-induced Parkinson's disease mouse model. J. Proteome Res., 9(3), 1496–1509. CrossRef Scholar google search
Song Q., Meng B., Xu H., Mao Z. (2020) The emerging roles of vacuolar-type ATPase-dependent lysosomal acidification in neurodegenerative diseases. Transl. Neurodegener., 9(1), 17. CrossRef Scholar google search
Chatterjee M., van Steenoven I., Huisman E., Oosterveld L., Berendse H., van der Flier W.M., del Campo M., Lemstra A.W., van de Berg W.D.J., Teunissen C.E. (2020) Contactin-1 is reduced in cerebrospinal fluid of Parkinson's disease patients and is present within Lewy bodies. Biomolecules, 10(8), 1177. CrossRef Scholar google search
Wang H., Sun C., Liang Y., Zhang H., Tan Y. (2013) Identification of regulatory relationships in Parkinson's disease. J. Mol. Neurosci., 51(1), 9–12. CrossRef Scholar google search
Stocker A.M., Chenn A. (2015) The role of adherens junctions in the developing neocortex. Cell Adh. Migr., 9(3), 167–174. CrossRef Scholar google search
Tretter L., Adam-Vizi V. (2000) Inhibition of Krebs cycle enzymes by hydrogen peroxide: A key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J. Neurosci., 20(24), 8972–8979. CrossRef Scholar google search
Gibson G.E., Xu H., Chen H.L., Chen W., Denton T.T., Zhang S. (2015) Alpha-ketoglutarate dehydrogenase complex-dependent succinylation of proteins in neurons and neuronal cell lines. J. Neurochem., 134(1), 86–96. CrossRef Scholar google search
Hansen G.E., Gibson G.E. (2022) The α-ketoglutarate dehydrogenase complex as a hub of plasticity in neurodegeneration and regeneration. Int. J. Mol. Sci., 23(20), 12403. CrossRef Scholar google search
Gibson G.E., Park L.C., Sheu K.F., Blass J.P., Calingasan N.Y. (2000) The alpha-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem. Int., 36(2), 97–112. CrossRef Scholar google search
Chung D., Shum A., Caraveo G. (2020) GAP-43 and BASP1 in axon regeneration: implications for the treatment of neurodegenerative diseases. Front. Cell Dev. Biol., 8, 567537. CrossRef Scholar google search
Lim Y.W., James D., Huang J., Lee M. (2020) The emerging role of the RNA-binding protein SFPQ in neuronal function and neurodegeneration. Int. J. Mol. Sci., 21(19), 7151. CrossRef Scholar google search
Hogan A.L., Grima N., Fifita J.A., McCann E.P., Heng B., Fat S.C.M., Wu S., Maharjan R., Cain A.K., Henden L., Rayner S., Tarr I., Zhang K.Y., Zhao Q., Zhang Z.H., Wright A., Lee A., Morsch M., Yang S., Williams K.L., Blair I.P. (2021) Splicing factor proline and glutamine rich intron retention, reduced expression and aggregate formation are pathological features of amyotrophic lateral sclerosis. Neuropathol. Appl. Neurobiol., 47(7), 990–1003. CrossRef Scholar google search
Kobayashi T., Matsumine H., Matuda S., Mizuno Y. (1998) Association between the gene encoding the E2 subunit of the alpha-ketoglutarate dehydrogenase complex and Parkinson's disease. Ann. Neurol., 43(1), 120–123. CrossRef Scholar google search
Collins M.P., Forgac M. (2020) Regulation and function of V-ATPases in physiology and disease. Biochim. Biophys. Acta Biomembr., 1862(12), 183341. CrossRef Scholar google search
Buneeva O., Medvedev A. (2022) Atypical ubiquitination and Parkinson's disease. Int. J. Mol. Sci., 23(7), 3705. CrossRef Scholar google search
Morrow J.S., Stankewich M.C. (2021) The spread of spectrin in ataxia and neurodegenerative disease. J. Exp. Neurol., 2(3), 131–139. CrossRef Scholar google search
Maor G., Dubreuil R.R., Feany M.B. (2023) α-Synuclein promotes neuronal dysfunction and death by disrupting the binding of ankyrin to β-spectrin. J. Neurosci., 43(9), 1614–1626. CrossRef Scholar google search
Liu Y., Zhang Y., Zhu K., Chi S., Wang C., Xie A. (2020) Emerging role of sirtuin 2 in parkinson's disease. Front. Aging Neurosci., 11, 372. CrossRef Scholar google search
Wu Q.J., Zhang T.N., Chen H.H., Yu X.F., Lv J.L., Liu Y.Y., Liu Y.S., Zheng G., Zhao J.Q., Wei Y.F., Guo J.Y., Liu F.H., Chang Q., Zhang Y.X., Liu C.G., Zhao Y.H. (2022) The sirtuin family in health and disease. Signal Transduct. Target Ther., 7(1),402. CrossRef Scholar google search
Tang Y., Han L., Li S., Hu T., Xu Z., Fan Y., Liang X., Yu H., Wu J., Wang J. (2023) Plasma GFAP in Parkinson's disease with cognitive impairment and its potential to predict conversion to dementia. NPJ Parkinsons Dis., 9(1), 23. CrossRef Scholar google search
Bernstein B.W., Bamburg J.R. (2010) ADF/cofilin: A functional node in cell biology. Trends Cell Biol., 20(4), 187–195. CrossRef Scholar google search
Lapeña-Luzón T., Rodríguez L.R., Beltran-Beltran V., Benetó N., Pallardó F.V., Gonzalez-Cabo P. (2021) Cofilin and neurodegeneration: New functions for an old but gold protein. Brain Sci., 11(7), 954. CrossRef Scholar google search
Ben Zablah Y., Merovitch N., Jia Z. (2020) The role of ADF/cofilin in synaptic physiology and Alzheimer's disease. Front. Cell Dev. Biol., 8, 594998. CrossRef Scholar google search
Stefanizzi I., Cañete-Soler R. (2007) Coregulation of light neurofilament mRNA by poly(A)-binding protein and aldolase C: Implications for neurodegeneration. Brain Res., 1139, 15–28. CrossRef Scholar google search
Kingsbury A.E., Cooper M., Schapira A.H., Foster O.J. (2001) Metabolic enzyme expression in dopaminergic neurons in Parkinson's disease: An in situ hybridization study. Ann. Neurol., 50(2), 142–149. CrossRef Scholar google search
Vassilopoulos D., Jockers-Wretou E. (1987) Serum creatine kinase B levels in diseases of the central nervous system. Eur. Neurol., 27(2), 78–81. CrossRef Scholar google search
Xu J., Fu X., Pan M., Zhou X., Chen Z., Wang D., Zhang X., Chen Q., Li Y., Huang X., Liu G., Lu J., Liu Y., Hu Y., Pan S., Wang Q., Wang Q., Xu Y. (2019) Mitochondrial creatine kinase is decreased in the serum of idiopathic Parkinson's disease patients. Aging Dis., 10(3), 601–610. CrossRef Scholar google search
Katayama T., Sawada J., Takahashi K., Yahara O., Hasebe N. (2021) Meta-analysis of cerebrospinal fluid neuron-specific enolase levels in Alzheimer's disease, Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Alzheimers Res. Ther., 13(1), 163. CrossRef Scholar google search
Medvedev A.E., Buneeva O.A., Kopylov A.T., Tikhonova O.V., Medvedeva M.V., Nerobkova L.N., Kapitsa I.G., Zgoda V.G. (2017) Brain mitochondrial subproteome of Rpn10-binding proteins and its changes induced by the neurotoxin MPTP and the neuroprotector isatin. Biochemistry (Moscow), 82(3), 330–339. CrossRef Scholar google search
Buneeva O.A., Medvedev A.E. (2016) Atypical ubiquitination of proteins. Biomeditsinskaya Khimiya, 62(5), 496–509. CrossRef Scholar google search
Buneeva O.A., Kopylov A.T., Tikhonova O.V., Zgoda V.G., Medvedev A.E., Archakov A.I. (2012) Effect of affinity sorbent on proteomic profiling of isatin-binding proteins of mouse brain. Biochemistry (Moscow), 77(11), 1326–1338. CrossRef Scholar google search
Buneeva O.A., Kopylov A.T., Gnedenko O.V., Medvedeva M.V., Kapitsa I.G., Ivanova E.A., Ivanov A.S., Medvedev A.E. (2021) Changes in the mitochondrial subproteome of mouse brain Rpn13-binding proteins induced by the neurotoxin MPTP and the neuroprotector isatin. Biomeditsinskaya Khimiya, 67(1), 51–65. CrossRef Scholar google search
Medvedev A., Kopylov A., Buneeva O., Kurbatov L., Tikhonova O., Ivanov A., Zgoda V. (2020) A neuroprotective dose of isatin causes multilevel changes involving the brain proteome: Prospects for further research. Int. J. Mol. Sci., 21(11), 4187. CrossRef Scholar google search
