1. Institute of Biomedical Chemistry, Moscow, Russia 2. Institute of Biomedical Chemistry, Moscow, Russia; Zakusov Institute of Pharmacology, Moscow, Russia
Isatin (indoldione-2,3) is an endogenous biological regulator found in the brain, peripheral tissues, and biological fluids of humans and animals. Its biological activity is realized via isatin-binding proteins, many of which were identified during proteomic profiling of the brain of mice and rats. A number of these proteins are related to the development of neurodegenerative diseases. Previously, using a model of experimental Parkinsonism induced by a seven-day course of rotenone injections, we have observed behavioral disturbances, as well as changes in the profile and relative content of brain isatin-binding proteins. In this study, we have investigated behavioral responses and the relative content of brain isatin-binding proteins in rats with rotenone-induced Parkinsonism 5 days after the last administration of this neurotoxin. Despite the elimination of rotenone, animals exhibited motor and coordination impairments. Proteomic profiling of isatin-binding proteins revealed changes in the relative content of 120 proteins (the relative content of 83 proteins increased and that of 37 proteins decreased). Comparison of isatin-binding proteins characterized by the changes in the relative content observed in the brain right after the last injection of rotenone (n=16) and 5 days later (n=11) revealed only two common proteins (glyceraldehyde-3-phosphate dehydrogenase and subunit B of V-type proton ATPase). However, most of these proteins are associated with neurodegeneration, including Parkinson's and Alzheimer's diseases.
Buneeva O.A., Kapitsa I.G., Kazieva L.Sh., 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.
Buneeva O.A. et al. The delayed effect of rotenone on the relative content of brain isatin-binding proteins of rats with experimental parkinsonism // Biomeditsinskaya Khimiya. - 2024. - V. 70. -N 1. - P. 25-32.
Buneeva O.A. et al., "The delayed effect of rotenone on the relative content of brain isatin-binding proteins of rats with experimental parkinsonism." Biomeditsinskaya Khimiya 70.1 (2024): 25-32.
Buneeva, O. A., Kapitsa, I. G., Kazieva, L. Sh., 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.
References
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. PMID: 19707325. 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
Medvedev A., Kopylov A., Buneeva O., Kurbatov L., Tikhonova O., Ivanov A., Zgoda V.A. (2020) 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
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
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. (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
Bradford M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254. CrossRef Scholar google search
Yu H., Xiong M., Liu C., Xia D., Meng L., Zhang Z. (2023) The γ-adducin 1-357 fragment promotes tau pathology. Front. Aging Neurosci., 15, 1241750. CrossRef Scholar google search
Gallardo G., Barowski J., Ravits J., Siddique T., Lingrel J.B., Robertson J., Steen H., Bonni A. (2014) An α2-Na/K ATPase/α-adducin complex in astrocytes triggers non-cell autonomous neurodegeneration. Nat. Neurosci., 17(12), 1710-1719. CrossRef Scholar google search
Oikonomou K.G., Zachou K., Dalekos G.N. (2011) Alpha-actinin: A multidisciplinary protein with important role in B-cell driven autoimmunity. Autoimmun. Rev., 10(7), 389-396. CrossRef Scholar google search
Foley K.S., Young P.W. (2014) The non-muscle functions of actinins: An update. Biochem. J., 459(1), 1-13. CrossRef Scholar google search
Jang B., Kim M.J., Lee Y.J., Ishigami A., Kim Y.S., Choi E.K. (2020) Vimentin citrullination probed by a novel monoclonal antibody serves as a specific indicator for reactive astrocytes in neurodegeneration. Neuropathol. Appl. Neurobiol., 46(7), 751-769. CrossRef Scholar google search
Pires G., McElligott S., Drusinsky S., Halliday G., Potier M.C., Wisniewski T., Drummond E. (2019) Secernin-1 is a novel phosphorylated tau binding protein that accumulates in Alzheimer's disease and not in other tauopathies. Acta Neuropathol. Commun., 7(1), 195. CrossRef Scholar google search
Weiner S., Sauer M., Brinkmalm G., Constantinescu J., Constantinescu R., Gomes B.F., Becker B., Nellgård B., Dalla K., Galasko D., Zetterberg H., Blennow K., Gobom J. (2023) SCRN1: A cerebrospinal fluid biomarker correlating with tau in Alzheimer's disease. Alzheimers Dement., 19(10), 4609-4618. CrossRef Scholar google search
Sharma A., Liu H., Tobar-Tosse F., Chand Dakal T., Ludwig M., Holz F.G., Loeffler K.U., Wüllner U., Herwig-Carl M.C. (2020) Ubiquitin carboxyl-terminal hydrolases (UCHs): Potential mediators for cancer and neurodegeneration. Int. J. Mol. Sci., 21(11), 3910. CrossRef Scholar google search
Buneeva O., Medvedev A. (2024) Ubiquitin carboxyl-terminal hydrolase L1 and its role in Parkinson's disease. Int. J. Mol. Sci., 25(2), 1303. CrossRef Scholar google search
Mor F., Izak M., Cohen I.R. (2005) Identification of aldolase as a target antigen in Alzheimer's disease. J. Immunol., 175(5), 3439-3445. CrossRef Scholar google search
Dukes A.A., van Laar V.S., Cascio M., Hastings T.G. (2008) Changes in endoplasmic reticulum stress proteins and aldolase A in cells exposed to dopamine. J. Neurochem., 106(1), 333-346. 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
Fu Y., Zhou L., Li H., Hsiao J.T., Li B., Tanglay O., Auwyang A.D., Wang E., Feng J., Kim W.S., Liu J., Halliday G.M. (2022) Adaptive structural changes in the motor cortex and white matter in Parkinson's disease. Acta Neuropathol., 144(5), 861-879. CrossRef Scholar google search
Mazzetti S., Calogero A.M., Pezzoli G., Cappelletti G. (2023) Cross-talk between α-synuclein and the microtubule cytoskeleton in neurodegeneration. Exp. Neurol., 359, 114251. CrossRef Scholar google search
Mazzetti S., Giampietro F., Calogero A.M., Isilgan H.B., Gagliardi G., Rolando C., Cantele F., Ascagni M., Bramerio M., Giaccone G., Isaias I.U., Pezzoli G., Cappelletti G. (2024) Linking acetylated α-tubulin redistribution to α-synuclein pathology in brain of Parkinson's disease patients. NPJ Parkinsons Dis., 10(1), 2. CrossRef Scholar google search
Amadeo A., Pizzi S., Comincini A., Modena D., Calogero A.M., Madaschi L., Faustini G., Rolando C., Bellucci A., Pezzoli G., Mazzetti S., Cappelletti G. (2021) The association between α-synuclein and α-tubulin in brain synapses. Int. J. Mol. Sci., 22(17), 9153. CrossRef Scholar google search
Pellegrini L., Wetzel A., Grannó S., Heaton G., Harvey K. (2017) Back to the tubule: Microtubule dynamics in Parkinson's disease. Cell Mol. Life Sci., 74(3), 409-434. CrossRef Scholar google search
Ren Y., Zhao J., Feng J. (2003) Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation. J. Neurosci., 23(8), 3316-3324. 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
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
Orosz F., Oláh J., Ovádi J. (2006) Triosephosphate isomerase deficiency: Facts and doubts. IUBMB Life, 58(12), 703-715. 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
He T., Lin X., Su A., Zhang Y., Xing Z., Mi L., Wei T., Li Z., Wu W. (2023) Mitochondrial dysfunction-targeting therapeutics of natural products in Parkinson's disease. Front. Pharmacol., 14, 1117337. CrossRef Scholar google search
Brotchie J.M. (2003) CB1cannabinoid receptor signalling in Parkinson's disease. Curr. Opin. Pharmacol., 3(1), 54-61. CrossRef Scholar google search
Lastres-Becker I., Cebeira M., de Ceballos M.L., Zeng B.Y., Jenner P., Ramos J.A., Fernández-Ruiz J.J. (2001) Increased cannabinoid CB1 receptor binding and activation of GTP-binding proteins in the basal ganglia of patients with Parkinson's syndrome and of MPTP-treated marmosets. Eur. J. Neurosci., 14(11), 1827-1832. CrossRef Scholar google search
Oliver E.E., Hughes E.K., Puckett M.K., Chen R., Lowther W.T., Howlett A.C. (2020) Cannabinoid receptor interacting protein 1a (CRIP1a) in health and disease. Biomolecules, 10(12), 1609. CrossRef Scholar google search
Smith T.H., Sim-Selley L.J., Selley D.E. (2010) Cannabinoid CB1 receptor-interacting proteins: Novel targets for central nervous system drug discovery? Br. J. Pharmacol., 160(3), 454-466. 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
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
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., 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
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
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
