Periodization of adaptation-compensatory remodeling of brain structures in incomplete permanent cerebral hypoperfusion in rats
- Authors: Gaivoronsky I.V.1,2, Chrishtop V.V.3, Nikonorova V.G.3, Semenov A.A.1,2, Khrustaleva Y.A.1
-
Affiliations:
- Military Medical Academy named after S.M. Kirov
- St Petersburg University
- State Scientific Research Test Institute of Military Medicine of the Ministry of Defence of Russia
- Issue: Vol 19, No 1 (2024)
- Pages: 5-20
- Section: Reviews
- URL: https://genescells.ru/2313-1829/article/view/492252
- DOI: https://doi.org/10.17816/gc492252
- ID: 492252
Cite item
Abstract
Bilateral one-stage ligation of the common carotid arteries in rats is the most common method of forming prolonged cerebral hypoxia with cognitive impairment. Pharmacological studies are most commonly performed at the early postoperative periods, up to 3 days. They are characterized by neuronal death, hypoenergetic state, and edema. In the acute period (3–8 days), changes are associated with the activation of astrocytes, which form intercellular cooperation between the neuron, hemocapillary, and respiratory burst of neutrophil granulocytes. Thus, the permeability of the blood–brain barrier increases, accompanied by the death of one part of the neurons and the improvement of the vitality of another part. The subacute period (from 8 days to 8 weeks) is accompanied by the death of neurons in a state of poor life support, microglial activation, myelin fiber damage, increased diameter of paravertebral arteries in the early period, and the development of astrocytosis and angiogenesis in the late period, which leads to increased lipid peroxidation, secondary damage, and neuronal death. In the late period, neurodystrophic changes appear, and minor neuronal apoptosis and increased permeability of the blood–brain barrier persist. Surviving neurons show metabolic activation and concentration of pericarions near the hemocapillaries.
Keywords
Full Text
About the authors
Ivan V. Gaivoronsky
Military Medical Academy named after S.M. Kirov; St Petersburg University
Email: i.v.gaivoronsky@mail.ru
ORCID iD: 0000-0002-7232-6419
SPIN-code: 1898-3355
MD, Dr. Sci. (Medicine), Professor
Russian Federation, Saint Petersburg; Saint PetersburgVladimir V. Chrishtop
State Scientific Research Test Institute of Military Medicine of the Ministry of Defence of Russia
Email: chrishtop@mail.ru
ORCID iD: 0000-0002-9267-5800
SPIN-code: 3734-5479
MD, Cand. Sci. (Medicine)
Russian Federation, Saint PetersburgVarvara G. Nikonorova
State Scientific Research Test Institute of Military Medicine of the Ministry of Defence of Russia
Email: bgnikon@gmail.com
ORCID iD: 0000-0001-9453-4262
SPIN-code: 2161-4838
Russian Federation, Saint Petersburg
Aleksei A. Semenov
Military Medical Academy named after S.M. Kirov; St Petersburg University
Author for correspondence.
Email: semfeodosia82@mail.ru
ORCID iD: 0000-0002-1977-7536
SPIN-code: 1147-3072
MD, Cand. Sci. (Medicine)
Russian Federation, Saint Petersburg; Saint PetersburgYulia A. Khrustaleva
Military Medical Academy named after S.M. Kirov
Email: khrustaleva-julia@yandex.ru
ORCID iD: 0000-0001-5282-7219
SPIN-code: 3622-5270
MD, Dr. Sci. (Medicine), Associate Professor
Russian Federation, Saint PetersburgReferences
- Levine S. Anoxic-ischemic encephalopathy in rats. Am J Pathol. 1960;36(1):1–17.
- Chrishtop V, Nikonorova V, Gutsalova A, et al. Systematic comparison of basic animal models of cerebral hypoperfusion. Tissue Cell. 2022;75:101715. doi: 10.1016/j.tice.2021.101715
- Ojo OB, Amoo ZA, Saliu IO, et al. Neurotherapeutic potential of kolaviron on neurotransmitter dysregulation, excitotoxicity, mitochondrial electron transport chain dysfunction and redox imbalance in 2-VO brain ischemia/reperfusion injury. Biomed Pharmacother. 2019;111:859–872. doi: 10.1016/j.biopha.2018.12.144
- Zong W, Zeng X, Che S, et al. Ginsenoside compound K attenuates cognitive deficits in vascular dementia rats by reducing the Aβ deposition. J Pharmacol Sci. 2019;139(3):223–230. doi: 10.1016/j.jphs.2019.01.013
- Wang DP, Yin H, Lin Q, et al. Andrographolide enhances hippocampal BDNF signaling and suppresses neuronal apoptosis, astroglial activation, neuroinflammation, and spatial memory deficits in a rat model of chronic cerebral hypoperfusion. Naunyn Schmiedebergs Arch Pharmacol. 2019;392(10):1277–1284. doi: 10.1007/s00210-019-01672-9
- Al Dera H, Alassiri M, Eleawa SM, et al. Melatonin improves memory deficits in rats with cerebral hypoperfusion, possibly, through decreasing the expression of small-conductance Ca 2+-activated K+ channels. Neurochem Res. 2019;44(8):1851–1868. doi: 10.1007/s11064-019-02820-6
- Chrishtop VV, Prilepskii AY, Nikonorova VG, Mironov VA. Nanosafety vs. nanotoxicology: adequate animal models for testing in vivo toxicity of nanoparticles. Toxicology. 2021;462:152952. doi: 10.1016/j.tox.2021.152952
- Fateev IV, Bykov VN, Chepur SV, et al. A model of cerebral circulation disorders created by staged ligation of the common carotid arteries. Bull Exp Biol Med. 2012;152(3):378–381. doi: 10.1007/s10517-012-1533-y
- Farkas E, Luiten PGM, Bari F. Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev. 2007;54(1):162–180. doi: 10.1016/j.brainresrev.2007.01.003
- Fujiwara S, Mori Y, de la Mora DM. Prediction of outcome in bilateral common carotid artery occlusion (BCCAO) rats by intravoxel incoherent motion (IVIM) analysis at 11.7 Tesla. Proceedings of the ISMRM 25th Annual Meeting & Exhibition; 2017 Apr 22–27; Honolulu, HI, USA.
- Muniz M, Fisher M. Visualization in the acute period of stroke. Stroke. Supplement to the Korsakov Journal of Neurology and Psychiatry. S.S. Korsakov. 2001;2(4):4–12. (In Russ).
- Zanin SA, Kade AKh, Trofimenko AI, Malysheva AV. Hystologic substantiation of efficiency of TES-therapy at the experimental ischemic stroke. Modern Problems of Science and Education. 2015;(1-1):1343.
- Ischemic stroke and transient ischemic attack in adults: clinical guidelines. 2022. 215 p. (In Russ).
- Lee MC, Jin CY, Kim HS, et al. Stem cell dynamics in an experimental model of stroke. Chonnam Med J. 2011;47(2):90–98. doi: 10.4068/cmj.2011.47.2.90
- Kitamura A, Fujita Y, Oishi N, et al. Selective white matter abnormalities in a novel rat model of vascular dementia. Neurobiol Aging. 2012;33(5):1012.e25–1012.e35. doi: 10.1016/j.neurobiolaging.2011.10.033
- Gopalakrishanan S, Babu MR, Thangarajan R, et al. Impact of seasonal variant temperatures and laboratory room ambient temperature on mortality of rats with ischemic brain injury. J Clin Diagn Res. 2016;10(4):CF01–CF5. doi: 10.7860/JCDR/2016/17372.7597
- Krishtop VV, Rumyantseva TA, Pakhrova OA. Influence of condition of higher nervous activity and sex on survival in modeling total cerebral hypoxia in rats. Modern Problems of Science and Education. 2015;(5):270.
- Kim SK, Cho KO, Kim SY. White matter damage and hippocampal neurodegeneration induced by permanent bilateral occlusion of common carotid artery in the rat: comparison between Wistar and Sprague-Dawley strain. Korean J Physiol Pharmacol. 2008;12(3):89–94. doi: 10.4196/kjpp.2008.12.3.89
- Gromova OA, Torshin IIu, Gogoleva IV, et al. Pharmacokinetic and pharmacodynamic synergism between neuropeptides and lithium in the neurotrophic and neuroprotective action of cerebrolysin. S.S. Korsakov Journal of Neurology and Psychiatry. 2015;115(3):65–72. doi: 10.17116/jnevro20151153165-72
- Mazina NV, Volotova EV, Kurkin DV. Neuroprotectivе action of new GABA derivative — RGPU-195 in cerebral ishemia. Fundamental Research. 2013;(6-6):1473–1476.
- Volotova EV, Kurkin DV, Tyurenkov IN, Litvinov AA. Cerebroprotective effects of derivatives of gaba in acute ischemia of rats brain. Journal of Volgograd State Medical University. 2011;(2):72–75.
- Li N, Gu Z, Li Y, et al. A modified bilateral carotid artery stenosis procedure to develop a chronic cerebral hypoperfusion rat model with an increased survival rate. J Neurosci Methods. 2015;255:115–121. doi: 10.1016/j.jneumeth.2015.08.002
- Titovich IA, Sysoev YI, Bolotova VC, Okovityi S.V. Neurotropic activity of a new aminoethanol derivative under conditions of experimental brain ischemia. Experimental and Clinical Pharmacology. 2017;80(5):3–6. doi: 10.30906/0869-2092-2017-80-5-3-6
- Kitamura A, Saito S, Maki T, et al. Gradual cerebral hypoperfusion in spontaneously hypertensive rats induces slowly evolving white matter abnormalities and impairs working memory. J Cereb Blood Flow Metab. 2016;36(9):1592–1602. doi: 10.1177/0271678X15606717
- Sultanov VS, Zarubina IV, Shabanov PD. Cerebroprotective and energy-stabilizing effects of the polyprenol drug ropren in cerebral ischemia in rats. Reviews on Clinical Pharmacology and Drug Therapy. 2010;8(3):31–47. (In Russ).
- Blinova EV, Maksimkin AI, Ambrosimov AV, et al. Promising approaches to pharmacological prophylaxis of acute ischemic cerebral attack in the experiment. The Journal of Scientific Articles Health and Education Millennium. 2016;18(11):123–125.
- Volotova EV. Pharmacological correction of cerebral circulation disorders in conditions of endothelial dysfunction (in experiment) [dissertation]. Volgograd, 2016. (In Russ).
- Lai TW, Zhang S, Wang YT. Excitotoxicity and stroke: identifying novel targets for neuroprotection. Prog Neurobiol. 2014;115:157–188. doi: 10.1016/j.pneurobio.2013.11.006
- Chepur SV, Bykov VN, Yudin MA, et al. Features of experimental modeling of somatic and neurological diseases to assess the effectiveness of drugs. Journal Biomed. 2012;(1):16–28. (In Russ).
- Fateev IV, Bykov VN, Chepur SV, et al. Model of cerebral circulation disorders with staged ligation of common carotid arteries. Byulleten’ eksperimental’noj biologii i mediciny. 2011;152(9);350–354. (In Russ).
- Danilova TG. Morphology of the frontal cortex of the large hemisphere in rats during common carotid artery clamping. Vestnik NOVSU. 2013;(71-1):101–105. (In Russ).
- Bon LI, Maksimovich NYe, Zimatkin SM, Valko NA. Morphological disturbances of the parietal cortex an hippocampus neurons in the dynamics of subtotal cerebral ischemia. Orenburg Medical Herald. 2019;7(2):36–41. (In Russ).
- Gallyas F, Pál J, Bukovics P. Supravital microwave experiments support that the formation of “dark” neurons is propelled by phase transition in an intracellular gel system. Brain Res. 2009;1270:152–156. doi: 10.1016/j.brainres.2009.03.020
- Panickar KS, Norenberg MD. Astrocytes in cerebralischemic injury: morphological and general considerations. Glia. 2005;50(4):287–298. doi: 10.1002/glia.20181
- Shavrin VA, Shulyatnikova TV. Ultrastructural features of synapses in critical zones of brain infarction in experiment. Pathologiya. 2011;8(3):090–093.
- Bon EI, Maksimovich NYe, Zimatkin SM, Valko NA. Morphological disturbances of the parietal cortex and hippocampus neurons in the dynamics of subtotal cerebral ischemia. Orenburgskij medicinskij vestnik. 2019;7(2):36–41.
- Shulyatnikova TV. Ultrastructure features of microcirculation in critical zones of brain ischemia in the experiment. Pathologiya. 2010;7(2):32–34.
- Markina LD, Shiryaeva EE, Markin VV. Morphofunctional features of the pial arteries adjacent areas of cerebral blood flow in acute circulatory hypoxia. Pacific Medical Journal. 2015;(1):40–42.
- Razvodovsky YuE, Smirnov VYu, Troyan EI, Maksimovich NE. Interhemispheric asymmetry of the cerebral amino acid pool in rat with subtotal cerebral ischaemia. Annals of Clinical and Experimental Neurology. 2019;13(2):41–46.
- Barber PA. Magnetic resonance imaging of ischemia viability thresholds and the neurovascular unit. Sensors (Basel). 2013;13(6):6981–7003. doi: 10.3390/s130606981
- Voronkov AV, Oganesjan JeT, Pozdnjakov DI, et al. Effect of flavonoids: hesperidin and patuletin on the vasodilatory function of the vascular endothelium of the brain of experimental animals against its focal ischemia. Nauchnye vedomosti Belgorodskogo gosudarstvennogo universiteta. Serija: Medicina. Farmacija. 2017;(19):186–194. (In Russ).
- Voronkov AV, Shabanova NB, Voronkova MP. Assessment of influence of the pir-4 connection on brain edema at bilateral occlusion of the general carotids at rats. Journal of Volgograd State Medical University. 2018;(4):117–121. doi: 10.19163/1994-9480-2018-4(68)-117-121
- Rybalko AE, Kravchenko ES. Proceedings of the conference “New “targets” for pharmacological correction of cerebral edema in its damage of different genesis”. 2017 Apr 3; Kazan’. P. 197–201. (In Russ). Available from: https://www.elibrary.ru/item.asp?id=28895657
- Bon EI, Maksimovich NYe, Zimatkin SM. Cytochemical disturbances in the parietal cortex and hippocampus of rats after incomplete ischemia. Vitebsk Medical Journal. 2018;17(1):43–49. doi: 10.22263/2312-4156.2018.1.43
- Zimatkin SM, Bon EI, Maksimovich NYe. The role of neuroglobin in cerebral ischemia/hypoxia and other neuropathology. Journal of the Grodno State Medical University. 2018:16(6):643–647. doi: 10.25298/2221-8785-2018-16-6-643-647
- Litvinov AA. Cerebro-protective properties of salts of gamma-oxybutyric acid and some aspects of the mechanism of their action [dissertation]. Volgograd, 2015. Available from: https://www.dissercat.com/content/tserebroprotektornye-svoistva-solei-gamma-oksimaslyanoi-kisloty-i-nekotorye-aspekty-mekhaniz (In Russ).
- Droblenkov AV, Naumov NV, Monid MV, et al. Reactive changes of the rat brain cell elements due to circulatory hypoxia. Medical Academic Journal. 2013;13(4):19–28.
- Huang J, Li J, Feng C, et al. Blood-brain barrier damage as the starting point of leukoaraiosis caused by cerebral chronic hypoperfusion and its involved mechanisms: effect of Agrin and Aquaporin-4. Biomed Res Int. 2018;2018:2321797. doi: 10.1155/2018/2321797
- Naumov NG, Droblenkov AV. Reactive changes of neurons and astrocytes in the nucleus accumbens after blood flow restriction in rats. Vestnik NOVSU. 2016;(6):143–147.
- Lana D, Ugolini F, Melani A, et al. The neuron-astrocyte-microglia triad in CA3 after chronic cerebral hypoperfusion in the rat: protective effect of dipyridamole. Exp Gerontol. 2017;96:46–62. doi: 10.1016/j.exger.2017.06.006
- Cerbai F, Lana D, Nosi D, et al. The neuron-astrocyte-microglia triad in normal brain ageing and in a model of neuroinflammation in the rat hippocampus. PLoS One. 2012;7(9):45250. doi: 10.1371/journal.pone.0045250
- Galkin AA, Demidova VS. Neutrophils and systemic inflammatory response syndrome. Wounds and wound infections. The prof. B.M. Kostyuchenok journal. Rany i ranevye infekcii. 2015;2(2):25–31. doi: 10.17650/2408-9613-2015-2-2-25-31
- Jing Z, Shi C, Zhu L, et al. Chronic cerebral hypoperfusion induces vascular plasticity and hemodynamics but also neuronal degeneration and cognitive impairment. J Cereb Blood Flow Metab. 2015;35(8):1249–1259. doi: 10.1038/jcbfm.2015.55
- Krishtop VV, Nikonorova VG, Rumyantseva TA. Changes in the cellular composition of the cerebral cortex in rats with different levels of cognitive functions under cerebral hypoperfusion. Journal of Anatomy and Histopathology. 2019;8(4):22–29. doi: 10.18499/2225-7357-2019-8-4-22-29
- Chrishtop VV, Tomilova IK, Rumyantseva TA, et al. The effect of short-term physical activity on the oxidative stress in rats with different stress resistance profiles in cerebral hypoperfusion. Mol Neurobiol. 2020;57(7):3014–3026. doi: 10.1007/s12035-020-01930-5
- Chrishtop VV, Pakhrova OA, Kurchaninova MG, Rumyantseva TA. Blood leukocyte parameters in adaptation to acute experimental cerebral hypoxia depending on the level of stress resistance. Modern Problems of Science and Edication. 2016;(6):231. Available from: https://www.elibrary.ru/item.asp?id=27695040
- Stepanov AS, Akulinin VA, Mytsik AV, et al. Neuro-gliovascular complexes of the brain after acute ischemia. General Resuscitation. 2017;13(6):6–17.
- Dosina MO, Loiko DO, Tokalchik YP. Assessment of the decrease in the duration of rehabilitation period after ischemic stroke on the model of ligation of common carotid arteries and intranasal administration of stem cells in rats. Proceedings of the conference “Health and environment”; 2018 Nov 15–16; Minsk. Available from: https://www.elibrary.ru/item.asp?id=36830687 (In Russ).
- Norenberg M.D. The reactive astrocyte. In: Aschner M., Costa L.G., editors. The role of glia in neurotoxicity. 2th edition. London, New York, Washington: CRC Press; 2004. P. 73–92.
- Petito CK, Morgello S, Felix JC, Lesser ML. The two patterns of reactive astrocytosis in postischemic rat brain. J Cereb Blood Flow Metab. 1990;10(6):850–859. doi: 10.1038/jcbfm.1990.141
- Petito CK, Morgello S, Felix JC, Lesser ML. The two patterns of reactive astrocytosis in postischemic rat brain. J Cereb Blood Flow Metab. 1990;10(6):850–859. doi: 10.1038/jcbfm.1990.141
- Chida Y, Kokubo Y, Sato S, et al. The alterations of oligodendrocyte, myelin in corpus callosum, and cognitive dysfunction following chronic cerebral ischemia in rats. Brain Res. 2011;1414:22–31. doi: 10.1016/j.brainres.2011.07.026
- Yang Q, Wang X, Cui J, et al. Bidirectional regulation ofangiogenesis and miR-18a expression by PNS in the mouse model oftumor complicated by myocardial ischemia. BMC Complement Altern Med. 2014;14:183. doi: 10.1186/1472-6882-14-183
- Zhang T, Gu J, Wu L, et al. Neuroprotective and axonal outgrowth-promoting effects of tetramethylpyrazine nitrone in chronic cerebral hypoperfusion rats and primary hippocampal neurons exposed to hypoxia. Neuropharmacology. 2017;118:137–147. doi: 10.1016/j.neuropharm.2017.03.022
- Xu Y, McArthur DL, Alger JR, et al. Early nonischemic oxidative metabolic dysfunction leads to chronic brain atrophy in traumatic brain injury. J Cereb Blood Flow Metab. 2010;30(4):883–894. doi: 10.1038/jcbfm.2009.263
- Monid MV, Droblenkov AV, Sosin DV, Shabanov PD. Reactive morphological changes of the rat brain anterior cingulate cortex after acute hypoxia. Vestnik of the Smolensk State Medical Academy. 2013;12(4):31–34.
- Stepanov AS, Akulinin VA, Stepanov SS, et al. Neurons communication in the hippocampus of field ca3 of the white rat brain after acute ischemia. General Reanimatology. 2018;14(5):38–49. doi: 10.15360/1813-9779-2018-5-38-49
- Harukuni I, Bhardwaj A. Mechanisms of brain injury after global cerebral ischemia. Neurol Clin. 2006;24(1):1–21. doi: 10.1016/j.ncl.2005.10.004
- Briede J, Duburs G. Protective effect of cerebrocrast on rat brain ischaemia induced by occlusion of both common carotid arteries. Cell Biochem Funct. 2007;25(2):203–210. doi: 10.1002/cbf.1318
- Akulinin VA, Sergeev AV, Stepanov SS, et al. Cytoarchitectonic of different shares of the human cerebral cortex in chronic ischemia. Omsk Scientific Bulletin. 2015;(2):5–9.
- Bak LK, Schousboe A, Waagepetersen HS. The glutamate GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem. 2006;98(3):641–653. doi: 10.1111/j.1471-4159.2006.03913.x
- Sukhorukova YeG, Guselnikova VV, Korzhevskiy DE. Glutamine synthetase in rat brain cells. Morphology. 2017;152(6):7–11.
- Qu C, Xu L, Shen J, et al. Protection of blood-brain barrier as a potential mechanism for enriched environments to improve cognitive impairment caused by chronic cerebral hypoperfusion. Behav Brain Res. 2020;379:112385. doi: 10.1016/j.bbr.2019.112385
- Chrishtop VV, Rumyantseva TA, Pozhilov DA. Exppression of GFAP in the large hemisphere cortex during development of cerebral hypoxia in rats with different outcomes in Morris maze. Biomedicine. 2020;16(10):89–98. doi: 10.33647/2074-5982-16-1-89-98