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Expression of Cytoskeletal Proteins in Neurons of the Rat Sensorimotor Cortex upon Hypoperfusion of the Brain and Sensitization by Cerebral Antigen

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Neurophysiology Aims and scope

Relatively mild disturbances in the blood supply of the rat brain provided by ligation of one common carotid artery leading to relatively mild disturbances of the cerebral blood supply or sensitization of the animals by brain antigen induce noticeable disorganization of the cytoskeleton in neurons of the sensorimotor cortex (SMC). The most considerable shifts in the system of cytoskeleton proteins were decreased expressions of low molecular mass neurofilament proteins (NF-L), actin (Act), and β-tubulin (β-tub), and increased expression of tau-protein (tau-p) within an early period after induction of hypoperfusion or sensitization (days 1–10) with a tendency toward normalization within the 2nd to 3rd months. The nature of changes in the NF-L expression allows one to qualify the observed phenomena as results of terminal neurodegeneration with subsequent regeneration. Decreased expression of Act and β-tub in the neuropil elements may be related to the impairment of the synaptic function and plasticity, whereas such shifts in the neuronal somata probably reflect disorders of the synthesis of these proteins. An increase in the tau-p expression was a most significant change among the observed phenomena. Presensitization of the animals with cerebral antigen potentiated the effects of ligation of the carotid artery and slowed down the recovery processes.

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References

  1. G. C. Román, “Brain hypoperfusion: a critical factor in vascular dementia,” Neuro. Res., 26, No. 5, 454–458 (2004), https://doi.org/10.1179/016164104225017686.

    Article  Google Scholar 

  2. J. C. de la Torre, “Cardiovascular risk factors promote brain hypoperfusion leading to cognitive decline and dementia,” Cardiovasc. Psychiatry Neurol., 2012, Article ID 367516 (2012), https://doi.org/10.1155/2012/367516.

  3. D. Inzitari, G. Pracucci, A. Poggesi, et al., “Changes in white matter as determinant of global functional decline in older independent outpatients: three year follow-up of LADIS (leukoaraiosis and disability) study cohort,” BMJ, 339, b2477 (2009), https://doi.org/10.1136/bmj.b2477.

  4. R. Schmidt, A. Berghold, H. Jokinen, et al., “White matter lesion progression in LADIS: frequency, clinical effects, and sample size calculations,” Stroke, 43, No. 10, 2643–2647 (2012), https://doi.org/10.1161/STROKEAHA.112.662593.

    Article  PubMed  Google Scholar 

  5. F. Cechetti, A. S. Pagnussat, P. V. Worm, et al., “Chronic brain hypoperfusion causes early glial activation and neuronal death, and subsequent long-term memory impairment,” Brain Res. Bull., 87, No. 1, 109–116 (2012), https://doi.org/10.1016/j.brainresbull.2011.10.006.

    Article  CAS  PubMed  Google Scholar 

  6. H. Tomimoto, M. Ihara, H. Wakita, et al., “Chronic cerebral hypoperfusion induces white matter lesions and loss of oligodendroglia with DNA fragmentation in the rat,” Acta Neuropathol., 106, No. 6, 527–534 (2003), https://doi.org/10.1007/s00401-003-0749-3.

    Article  CAS  PubMed  Google Scholar 

  7. É. Vicente, D. Degerone, L. Bohn, et al., “Astroglial and cognitive effects of chronic cerebral hypoperfusion in the rat,” Brain Res., 1251, 204–212 (2009), https://doi.org/10.1016/j.brainres.2008.11.032.

    Article  CAS  PubMed  Google Scholar 

  8. A. Nishino, Y. Tajima, H. Takuwa, et al., “Long-term effects of cerebral hypoperfusion on neural density and function using misery perfusion animal model,” Sci. Rep., 6, 25072 (2016), https://doi.org/10.1038/srep25072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. A. K. Saxena, S. S. Abdul-Majeed, S. Gurtu, and W. M. Mohamed, “Investigation of redox status in chronic cerebral hypoperfusion-induced neurodegeneration in rats,” Appl. Transl. Genom., 5, 30–32 (2015), https://doi.org/10.1016/j.atg.2015.05.004.

    Article  PubMed  PubMed Central  Google Scholar 

  10. F. Gueniot, J. L. Morel, T. Couffinhal, and C. Duplàa, “Development of a mouse model for chronic cerebral hypoperfusion: Analysis of its impact on neurovascular unit and cognitive impairment,” Arch. Cardiovasc. Dis. Suppl., 10, No. 2, 225–226 (2018), https://doi.org/10.1016/j.acvdsp.2018.02.107.

    Article  Google Scholar 

  11. E. Sigfridsson, M. Marangoni, J. A. Johnson, et al., “Astrocyte-specific overexpression of Nrf2 protects against optic tract damage and behavioural alterations in a mouse model of cerebral hypoperfusion,” Sci. Rep., 8, No. 1, 12552 (2018), https://doi.org/10.1038/s41598-018-30675-4.

  12. Y. Manso, P. R. Holland, A. Kitamura, et al., “Minocycline reduces microgliosis and improves subcortical white matter function in a model of cerebral vascular disease,” Glia, 66, No. 1, 34–46 (2018), https://doi.org/10.1002/glia.23190.

    Article  PubMed  Google Scholar 

  13. K. Yoshizaki, K. Adachi, S. Kataoka, et al., “Chronic cerebral hypoperfusion induced by right unilateral common carotid artery occlusion causes delayed white matter lesions and cognitive impairment in adult mice,” Exp. Neurol., 210, No. 2, 585–591 (2008), https://doi.org/10.1016/j.expneurol.2007.12.005.

    Article  PubMed  Google Scholar 

  14. B. Diamond, G. Honig, S. Mader, et al., “Brain-reactive antibodies and disease,” Annu. Rev. Immunol., 31, 345–385 (2013), https://doi.org/10.1146/annurevimmunol-020711-075041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. S. Irani and B. Lang, “Autoantibody-mediated disorders of the central nervous system,” Autoimmunity, 41, No. 1, 55–65 (2008), https://doi.org/10.1080/08916930701619490.

    Article  CAS  PubMed  Google Scholar 

  16. A. N. Grabovoy and L. M. Jaremenko, “The condition of brain hemisphere cortex at circulation problems modulation and at the correction of accompanying changes in immune system in rats.” Nauk. Visn. Bogomolets Natl. Med. Univ. (Kyiv), No. 4, 28–33 (2009).

  17. A. Villa, E. Vegeto, A. Poletti, and A. Maggi, “Estrogens, neuroinflammation, and neurodegeneration,” Endocr. Rev., 37, No. 4, 372–402 (2016), https://doi.org/10.1210/er.2016-1007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. L. M. Yaremenko, O. M. Grabovy, and V. G. Bordonos, “The state of autoantibody titers to tissue antigens of the brain and circulating immune complexes in the modeling of blood supply disorders of the brain of varying severity and its correction,” Immunol. Allergol. (Kyiv), Nos. 2–3, 55–59 (2009).

  19. L. M. Yaremenko and A. N. Grabovoy, “Changes in the expression of neurofilament protein in the rat sensorimotor cortex induced by microembolization of blood vessels: effect of immunomodulation,” Neurophysiology, 48, No. 2, 111–116. (2016).

    Article  CAS  Google Scholar 

  20. Y. Fan, X. Tang, E. Vitriol, et al., “Actin capping protein is required for dendritic spine development and synapse formation,” J. Neurosci., 31, No. 28, 10228–10233 (2011), https://doi.org/10.1523/JNEUROSCI.0115-11.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. E. Schroeder, S. Vogelgesang, A. Popa-Wagner, and C. Kessler, “Neurofilament expression in the rat brain after cerebral infarction: effect of age,” Neurobiol. Aging, 24, No. 1, 135–145 (2003), https://doi.org/10.1016/s0197-4580(02)00063-5.

    Article  CAS  PubMed  Google Scholar 

  22. B. Mages, S. Aleithe, S. Altmann, et al., “Impaired neurofilament integrity and neuronal morphology in different models of focal cerebral ischemia and human stroke tissue?” Front. Cell. Neurosci., 12, 161 (2018), https://doi.org/10.3389/fncel.2018.00161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. H. Stefen, C. Chaichim, J. Power, and T. Fath, “Regulation of the postsynaptic compartment of excitatory synapses by the actin cytoskeleton in health and its disruption in disease,” Neural Plast., 2016, Article ID 2371970 (2016), https://doi.org/10.1155/2016/2371970.

  24. V. Sharma, T. W. Ling, S. S. Rewell, at al., “A novel population of α-smooth muscle actin-positive cells activated in a rat model of stroke: an analysis of the spatio-temporal distribution in response to ischemia,” J. Cereb. Blood Flow Metab., 32, No. 11, 2055–2065 (2012), https://doi.org/10.1038/jcbfm.2012.107.

  25. K. Xu, G. Zhong, and X. Zhuang, “Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons,” Science, 339, No. 6118, 452–456 (2013), https://doi.org/10.1126/science.1232251.

    Article  CAS  PubMed  Google Scholar 

  26. Y. Shen and L. C. Yu, “Potential protection of curcumin against hypoxia-induced decreases in beta-III tubulin content in rat prefrontal cortical neurons,” Neurochem. Res., 33, No. 10, 2112–2117 (2008), https://doi.org/10.1007/s11064-008-9720-y.

    Article  CAS  PubMed  Google Scholar 

  27. A. Latremoliere, L. Cheng,, M DeLisle, et al, “Neuronal-specific TUBB3 is not required for normal neuronal function but is essential for timely axon regeneration,” Cell Rep., 24, No. 7, 1865–1879 (2018), https://doi.org/10.1016/j.celrep.2018.07.029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. L. C. Kapitein and C. C. Hoogenraad, “Building the neuronal microtubule cytoskeleton,” Neuron, 87, No. 3, 492–506 (2015), doi: https://doi.org/10.1016/j.neuron.2015.05.046.

    Article  CAS  PubMed  Google Scholar 

  29. A. Akhmanova and C. C. Hoogenraad, “Microtubule minus-end-targeting proteins,” Curr. Biol., 25, No. 4, R162–R171 (2015), https://doi.org/10.1016/j.cub.2014.12.027.

    Article  CAS  PubMed  Google Scholar 

  30. P. R. Gordon-Weeks and A. E. Fournier, “Neuronal cytoskeleton in synaptic plasticity and regeneration,” J. Neurochem., 129, No. 2, 206–212 (2014), https://doi.org/10.1111/jnc.12502.

    Article  CAS  PubMed  Google Scholar 

  31. J. Bielewicz, J. Kurzepa, E. Czekajska-Chehab, et al., “Does serum Tau protein predict the outcome of patients with ischemic stroke?” J. Mol. Neurosci., 43, No. 3, 241–245 (2011), https://doi.org/10.1007/s12031-010-9403-4.

    Article  CAS  PubMed  Google Scholar 

  32. H. Kadavath, M. Jaremko, Ł. Jaremko et al., “Folding of the Tau protein on microtubules,” Angew. Chem. Int. Ed. Engl., 54, No. 35, 10347–10351 (2015), https://doi.org/10.1002/anie.201501714.

    Article  CAS  PubMed  Google Scholar 

  33. A. R. Nelson, M. D. Sweeney, A. P. Sagare, and B. V. Zlokovic, “Neurovascular dysfunction and neurodegeneration in dementia and Alzheimer’s disease,” Biochim. Biophys. Acta, 1862, No. 5, 887–900 (2016), https://doi.org/10.1016/j.bbadis.2015.12.016.

    Article  CAS  PubMed  Google Scholar 

  34. J. Eira, C. S. Silva, M. M Sousa and M. A. Liz, “The cytoskeleton as a novel therapeutic target for old neurodegenerative disorders,” Prog. Neurobiol., 141, 61–82 (2016), https://doi.org/10.1016/j.pneurobio.2016.04.007.

    Article  CAS  PubMed  Google Scholar 

  35. K. Kounakis and N. Tavernarakis, “The cytoskeleton as a modulator of aging and neurodegeneration,” Adv. Exp. Med. Biol., 1178, 227–245 (2019), https://doi.org/10.1007/978-3-030-25650-0_12.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Bogomolets National Medical University, Ministry of Public Health of Ukraine, Kyiv, Ukraine

    L. M. Yaremenko, A. N. Grabovoy & S. E. Shepelev

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  1. L. M. Yaremenko
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Correspondence to L. M. Yaremenko.

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Yaremenko, L.M., Grabovoy, A.N. & Shepelev, S.E. Expression of Cytoskeletal Proteins in Neurons of the Rat Sensorimotor Cortex upon Hypoperfusion of the Brain and Sensitization by Cerebral Antigen. Neurophysiology 53, 68–77 (2022). https://doi.org/10.1007/s11062-022-09917-9

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