morphoМорфологические ведомостиMorphological newsletter1812-31712686-8741Private Medical University REAVIZ10.20340/mv-mn.2020.28(3):35-50morpho-471Research ArticleОРИГИНАЛЬНЫЕ ИССЛЕДОВАНИЯRESEARCH ARTICLESНЕЙРОНАЛЬНО-ГЛИАЛЬНЫЕ МЕМБРАННЫЕ КОНТАКТЫ ПРИ ПЕССИМАЛЬНОЙ ЭЛЕКТРОСТИМУЛЯЦИИNEURONAL-GLIAL MEMBRANE CONTACTS DURING PESSIMAL ELECTRICAL STIMULATIONhttps://orcid.org/0000-0001-6065-3757СотниковОлег СеменовичSotnikovOleg S.

доктор биологических наук, профессор, заслуженный деятель науки Российской Федерации, главный научный сотрудник

Doctor of Biological Sciences, Professor, Honored Scientist of the Russian Federation, Chief Researcher

ossotnikov@mail.ruСергееваСветлана СергеевнаSergeevaSvetlana S.

кандидат биологических наук, руководитель группы функциональной морфологии и физиологии нейрона

Candidate of Biological Sciences, Head of the Group of Functional Morphology and Physiology of the Neuron

sveta_serga@yandex.ruВасягинаТатьяна ИвановнаVasyaginaTat'yana I.

кандидат биологических наук, научный сотрудник

Candidate of Biological Sciences, Researcher

tvasyagina@yandex.ruИнститут физиологии имени И.П. Павлова Российской академии наук, Санкт-ПетербургРоссияPavlov Research Institute of Russian Academy of Sciences, Saint-PetersburgRussian FederationПриволжский исследовательский медицинский университет Минздрава России, Нижний НовгородРоссияPrivolzhsky Research Medical University of the Ministry of Health of Russia, Nizhny NovgorodRussian Federation2020281120202833550Copyright © Сотников О.С., Сергеева С.С., Васягина Т.И., 20202020Сотников О.С., Сергеева С.С., Васягина Т.И.Sotnikov O.S., Sergeeva S.S., Vasyagina T.I.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.morpholetter.com/jour/article/view/471

После создания способа получения межнейронных щелевых контактов в нервной системе, лишенной глии, целесообразным является воспроизведение щелевых нейронально-глиальные контактов на модели, содержащей также гибридные нейронально-глиальные щелевые контакты, которые, как известно, функционально принципиально отличаются от межнейронных контактов. Эксперименты проведены на ганглиях truncus sympathicus лабораторных крыс с помощью пессимальной электростимуляции и трансмиссионной электронной микроскопии. При электрической активации ганглиев с частотой до 100 Гц обнаружены местные и распространенные варианты разнообразных нейронально-глиальных связей (контактов, мостиков), покрытых бахромой околомембранных филаментозных белков. Они имели размытую форму пелены, маскирующую двухслойные нейромембраны. Часть контактов напоминала щелевые или плотные 5-слойные структуры без видимой межнейронной щели, но с предельным уменьшением толщины щели контактов. Главным результатом экспериментов оказалось образование, помимо щелевых, множественных септированных (лестничных) контактов. Относительно самостоятельные агрегаты электронно-плотного вещества септ располагались внутри межклеточных щелей, пересекая обе смежные мембраны, и, возможно, прободая их. Формировались и примембранные слабо очерченные пирамидо-подобные белковые конусы, связанные с обеими клеточными оболочками. Такие мембраны казались пунктирно-штриховидными, то есть не сплошными. Значительное количество септированных контактных мембран имело эндоцитозные впячивания (инвагинации), обращенные в сторону нейроплазмы с пирамидо-подобными краевыми выступами. Все реактивные измененные структуры, возникшие de novo, рассматриваются авторами как развившиеся под воздействием частотной электростимуляции денатурации и агрегации собственных и околомембранных белков.

After the creation of a method for obtaining inter-neuronal gap junctions in a nervous system devoid of glia, it is expedient to reproduce gap neuronal-glial contacts on a model that also contains hybrid neuronal-glial gap junctions, which, as you know, are functionally fundamentally different from inter-neuronal contacts. The experiments were carried out on the truncus sympathicus ganglia of laboratory rats using pessimal electrical stimulation and transmission electron microscopy. Electrical activation of ganglia with a frequency of up to 100 Hz revealed local and widespread variants of various neuronal-glial connections (contacts, bridges), fringed with peri-membrane filamentous proteins. They had a blurred veil that masked two-layer neuro-membranes. Some of the contacts resembled slit or dense 5-layer structures without a visible inter-neuronal slit, but with an extreme decrease in the thickness of the contact slit. The main result of the experiments was the formation, in addition to slotted, multiple septate (ladder) contacts. Relatively independent aggregates of the electron-dense substance of the septa were located inside the intercellular gaps, crossing both adjacent membranes, and, possibly, permeate of them. Near-membrane, poorly outlined pyramid-like protein cones associated with both cell membranes were also formed. Such membranes appeared to be dotted-dashed, that is, not continuous. A significant number of septic contact membranes had endocytic invaginations (invaginations) facing neuroplasm with pyramid-like marginal projections. All reactive altered structures that have arisen de novo are considered by the authors as developed under the influence of frequency electrical stimulation of denaturation and aggregation of intrinsic and perimembrane proteins.

нейронально-глиальные контактыпессимальная электростимуляциясептированные контактыщелевые контактыэндоцитозneuronal-glial contactspessimal electrical stimulationseptic contactsgap junctionsendocytosisReferencesSotnikov OS. Ob’edinyonnaya nejronno - retikulyarnaya teoriya. SPb: Nauka. 2019. 239s.Sotnikov OS. Ob’edinyonnaya nejronno - retikulyarnaya teoriya. SPb: Nauka. 2019. 239s.Nekhendzy V, Davies MF, Lemmens HJ, Maze M. The role of the craniospinal nerves in mediating the antinociceptive effect of transcranial electrostimulation in the rat. Anesth Analg. 2006;102(6):1775–1780. DOI: 10.1213/01.ANE.0000219588.25375.36.Nekhendzy V, Davies MF, Lemmens HJ, Maze M. The role of the craniospinal nerves in mediating the antinociceptive effect of transcranial electrostimulation in the rat. Anesth Analg. 2006;102(6):1775–1780. DOI: 10.1213/01.ANE.0000219588.25375.36.Jiang F, Yin H, Qin X. Fastigial nucleus electrostimulation reduces the expression of repulsive guidance molecule, improves axonal growth following focal cerebral ischemia. Neurochem Res. 2012;7(9):1906–1914. DOI: 10.1007/s11064-012-0809-y.Jiang F, Yin H, Qin X. Fastigial nucleus electrostimulation reduces the expression of repulsive guidance molecule, improves axonal growth following focal cerebral ischemia. Neurochem Res. 2012;7(9):1906–1914. DOI: 10.1007/s11064-012-0809-y.Schucht P, Moritz-Gasser S, Herbet G, Raabe A, Duffau H. Subcortical electrostimulation to identify network subserving motor control. Hum Brain Mapp. 2013;34(11):3023–3030. DOI: 10.1002/hbm.22122.Schucht P, Moritz-Gasser S, Herbet G, Raabe A, Duffau H. Subcortical electrostimulation to identify network subserving motor control. Hum Brain Mapp. 2013;34(11):3023–3030. DOI: 10.1002/hbm.22122.Shchudlo NA, Borisova IV, Shchudlo MM. Morphometric evaluation of the effectiveness of post-traumatic peripheral nerve regeneration after a single and repeated courses of electrostimulation. Morfologiia. 2012;142(6):30–35.Shchudlo NA, Borisova IV, Shchudlo MM. Morphometric evaluation of the effectiveness of post-traumatic peripheral nerve regeneration after a single and repeated courses of electrostimulation. Morfologiia. 2012;142(6):30–35.Cavalcante Miranda de Assis D, Martins Lima Ê, Teixeira Goes B. The parameters of transcutaneous electrical nerve stimulation are critical to its regenerative effects when applied just after a sciatic crush lesion in mice. Biomed Res Int. 2014; Article ID 2014:572949. DOI:10.1155/2014/572949.Cavalcante Miranda de Assis D, Martins Lima Ê, Teixeira Goes B. The parameters of transcutaneous electrical nerve stimulation are critical to its regenerative effects when applied just after a sciatic crush lesion in mice. Biomed Res Int. 2014; Article ID 2014:572949. DOI:10.1155/2014/572949.Xu Z, Wang Y, Chen B, Xu C, Wu X, Wang Y, Zhang S, Hu W, Wang S, Guo Y, Zhang X, Luo J, Duan S, Chen Z. Entorhinal principal neurons mediate brain-stimulation treatments for epilepsy. EBioMedicine. 2016;14():148–160. DOI:10.1016/j.ebiom.2016.11.027.Xu Z, Wang Y, Chen B, Xu C, Wu X, Wang Y, Zhang S, Hu W, Wang S, Guo Y, Zhang X, Luo J, Duan S, Chen Z. Entorhinal principal neurons mediate brain-stimulation treatments for epilepsy. EBioMedicine. 2016;14():148–160. DOI:10.1016/j.ebiom.2016.11.027.Cota VR, Drabowski BM, de Oliveira JC. The epileptic amygdala: Toward the development of a neural prosthesis by temporally coded electrical stimulation. J Neurosci Res. 2016;94(6):463–485. DOI: 10.1002/jnr.23741.Cota VR, Drabowski BM, de Oliveira JC. The epileptic amygdala: Toward the development of a neural prosthesis by temporally coded electrical stimulation. J Neurosci Res. 2016;94(6):463–485. DOI: 10.1002/jnr.23741.Inman CS, Manns JR, Bijanki KR. Direct electrical stimulation of the amygdala enhances declarative memory in humans. Proc Natl Acad Sci USA. 2018;115(1):98–103. DOI: 10.1073/pnas.1714058114.Inman CS, Manns JR, Bijanki KR. Direct electrical stimulation of the amygdala enhances declarative memory in humans. Proc Natl Acad Sci USA. 2018;115(1):98–103. DOI: 10.1073/pnas.1714058114.Mardani P, Oryan S, Sarihi A, Alireza K, Amir S, Dehghan S, Mirnajafi-Zadeh J. ERK activation is required for the antiepileptogenic effect of low frequency electrical stimulation in kindled rats. Rain Res Bull. 2018;14:132–139. DOI: 10.1016/j.brainresbull.2018.04.013.Mardani P, Oryan S, Sarihi A, Alireza K, Amir S, Dehghan S, Mirnajafi-Zadeh J. ERK activation is required for the antiepileptogenic effect of low frequency electrical stimulation in kindled rats. Rain Res Bull. 2018;14:132–139. DOI: 10.1016/j.brainresbull.2018.04.013.Finkelshtejn AV, Pticyn OB. Fizika belka: kurs lekcij s cvetnymi i stereoskopicheskimi illyustraciyami i zadachami. Moskva: KDU. 2012:456.Finkelshtejn AV, Pticyn OB. Fizika belka: kurs lekcij s cvetnymi i stereoskopicheskimi illyustraciyami i zadachami. Moskva: KDU. 2012:456.Brückner G, Szeöke S, Pavlica S, Grosche J, Kacza J. Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience. 2006;138(2):365–375.Brückner G, Szeöke S, Pavlica S, Grosche J, Kacza J. Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience. 2006;138(2):365–375.DOI: 10.1016/j.neuroscience.2005.11.068.DOI: 10.1016/j.neuroscience.2005.11.068.Ogawa Y, Rasband MN. The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol. 2008;18(3):307–313. DOI: 10.1016/j.conb.2008.08.008.Ogawa Y, Rasband MN. The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol. 2008;18(3):307–313. DOI: 10.1016/j.conb.2008.08.008.Bakkum DJ, Obien MEJ, Radivojevic M, Jäckel D, Frey U, Takahashi H, Hierlemann A. 2019. The Axon Initial Segment is the Dominant Contributor to the Neuron's Extracellular Electrical Potential Landscape. Adv Biosyst. 2019;3(2):pii:1800308. DOI: 10.1002/adbi.201800308.Bakkum DJ, Obien MEJ, Radivojevic M, Jäckel D, Frey U, Takahashi H, Hierlemann A. 2019. The Axon Initial Segment is the Dominant Contributor to the Neuron's Extracellular Electrical Potential Landscape. Adv Biosyst. 2019;3(2):pii:1800308. DOI: 10.1002/adbi.201800308.Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ. Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci. 2008;11(2):178–186. DOI: 10.1038/nn2040.Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ. Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci. 2008;11(2):178–186. DOI: 10.1038/nn2040.Sotelo C. Development of "Pinceaux" formations and dendritic translocation of climbing fibers during the acquisition of the balance between glutamatergic and gamma-aminobutyric acidergic inputs in developing Purkinje cells. J Comp Neurol. 2008;506(2):240–262. DOI: 10.1002/cne.21501.Sotelo C. Development of "Pinceaux" formations and dendritic translocation of climbing fibers during the acquisition of the balance between glutamatergic and gamma-aminobutyric acidergic inputs in developing Purkinje cells. J Comp Neurol. 2008;506(2):240–262. DOI: 10.1002/cne.21501.Kole MH, Stuart GJ. Signal processing in the axon initial segment. Neuron. 2012;73(2):235–247. DOI: 10.1016/j.neuron.2012.01.007.Kole MH, Stuart GJ. Signal processing in the axon initial segment. Neuron. 2012;73(2):235–247. DOI: 10.1016/j.neuron.2012.01.007.Hedstrom KL, Rasband MN. Intrinsic and extrinsic determinants of ion channel localization in neurons. J Neurochem. 2006;98(5):1345–1352.Hedstrom KL, Rasband MN. Intrinsic and extrinsic determinants of ion channel localization in neurons. J Neurochem. 2006;98(5):1345–1352.Pillai AM, Thaxton C, Pribisko AL, Cheng J, Dupree JL, Bhat MA. Spatiotemporal ablation of myelinating glia-specific neurofascin (Nfasc NF155) in mice reveals gradual loss of paranodal axoglial junctions and concomitant disorganization of axonal domains. J Neurosci Res. 2009;87(8):1773–1793. DOI: 10.1002/jnr.22015.Pillai AM, Thaxton C, Pribisko AL, Cheng J, Dupree JL, Bhat MA. Spatiotemporal ablation of myelinating glia-specific neurofascin (Nfasc NF155) in mice reveals gradual loss of paranodal axoglial junctions and concomitant disorganization of axonal domains. J Neurosci Res. 2009;87(8):1773–1793. DOI: 10.1002/jnr.22015.Iwakura A, Uchigashima M, Miyazaki T, Yamasaki M, Watanabe M. 2012. Lack of molecular-anatomical evidence for GABAergic influence on axon initial segment of cerebellar Purkinje cells by the pinceau formation. J Neurosci. 2012;32(27):9438–9448. DOI: 10.1523/JNEUROSCI.1651-12.2012.Iwakura A, Uchigashima M, Miyazaki T, Yamasaki M, Watanabe M. 2012. Lack of molecular-anatomical evidence for GABAergic influence on axon initial segment of cerebellar Purkinje cells by the pinceau formation. J Neurosci. 2012;32(27):9438–9448. DOI: 10.1523/JNEUROSCI.1651-12.2012.Grubb MS, Burrone J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature. 2010;465(7301):1070–1074. DOI: 10.1038/nature09160.Grubb MS, Burrone J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature. 2010;465(7301):1070–1074. DOI: 10.1038/nature09160.Wefelmeyer W, Cattaert D, Burrone J. Activity-dependent mismatch between axo-axonic synapses and the axon initial segment controls neuronal output. Proc Natl Acad Sci USA. 2015;112(31):9757–9762. DOI: 10.1073/pnas.1502902112.Wefelmeyer W, Cattaert D, Burrone J. Activity-dependent mismatch between axo-axonic synapses and the axon initial segment controls neuronal output. Proc Natl Acad Sci USA. 2015;112(31):9757–9762. DOI: 10.1073/pnas.1502902112.Song I, Dityatev A. Crosstalk between glia, extracellular matrix and neurons. Brain Res Bull. 2018;136():101–108. DOI: 10.1016/j.brainresbull.2017.03.003.Song I, Dityatev A. Crosstalk between glia, extracellular matrix and neurons. Brain Res Bull. 2018;136():101–108. DOI: 10.1016/j.brainresbull.2017.03.003.Mikheeva IB, Shtanchaev RS, Pen'kova NA, Pavlik LL. Structure of Interneuronal Contacts in the Neuropil of the Oculomotor Nuclei in Mouse Brain under Conditions of Long-Term Microgravity. Bull Exp Biol Med. 2018;165(4):457–460. DOI: 10.1007/s10517-018-4193-8.Mikheeva IB, Shtanchaev RS, Pen'kova NA, Pavlik LL. Structure of Interneuronal Contacts in the Neuropil of the Oculomotor Nuclei in Mouse Brain under Conditions of Long-Term Microgravity. Bull Exp Biol Med. 2018;165(4):457–460. DOI: 10.1007/s10517-018-4193-8.Gormal R, Valmas N, Fath T, Meunier F. A role for tropomyosins in activity-dependent bulk endocytosis? Mol Cell Neurosci. 2017;84:112–118. DOI: 10.1016/j.mcn.2017.04.003.Gormal R, Valmas N, Fath T, Meunier F. A role for tropomyosins in activity-dependent bulk endocytosis? Mol Cell Neurosci. 2017;84:112–118. DOI: 10.1016/j.mcn.2017.04.003.Simard-Bisson C, Bidoggia J, Larouche D. A Role for DLK in Microtubule Reorganization to the Cell Periphery and in the Maintenance of Desmosomal and Tight Junction Integrity. J Invest Dermatol. 2017;137(1):132–141. DOI: 10.1016/j.jid.2016.07.035.Simard-Bisson C, Bidoggia J, Larouche D. A Role for DLK in Microtubule Reorganization to the Cell Periphery and in the Maintenance of Desmosomal and Tight Junction Integrity. J Invest Dermatol. 2017;137(1):132–141. DOI: 10.1016/j.jid.2016.07.035.Buck VU, Hodecker M, Eisner S, Leube RE, Krusche CA, Classen-Linke I. Ultrastructural changes in endometrial desmosomes of desmoglein 2 mutant mice. Cell Tissue Res. 2018;374(2):317–327. DOI: 10.1007/s00441-018-2869-z.Buck VU, Hodecker M, Eisner S, Leube RE, Krusche CA, Classen-Linke I. Ultrastructural changes in endometrial desmosomes of desmoglein 2 mutant mice. Cell Tissue Res. 2018;374(2):317–327. DOI: 10.1007/s00441-018-2869-z.Moshkov DA, Tiras NR, Pavlik LL, Dzeban DA, Mikheeva IB, Mukhtasimova NF. Structural differences between desmosome-like contacts in afferent chemical and mixed synapses of Mauthner neurons in the goldfish. Neurosci Behav Physiol. 2002;32(5):471–476. DOI: 10.1023/a:1019899320714.Moshkov DA, Tiras NR, Pavlik LL, Dzeban DA, Mikheeva IB, Mukhtasimova NF. Structural differences between desmosome-like contacts in afferent chemical and mixed synapses of Mauthner neurons in the goldfish. Neurosci Behav Physiol. 2002;32(5):471–476. DOI: 10.1023/a:1019899320714.Lewis JD, Caldara AL, Zimmer SE, Stahley SN, Seybold A, Strong NL, Frangakis AS, Levental I, Wahl JK 3rd, Mattheyses AL, Sasaki T, Nakabayashi K, Hata K, Matsubara Y, Ishida-Yamamoto A, Amagai M, Kubo A, Kowalczyk AP. The desmosome is a mesoscale lipid raft-like membrane domain. Mol Biol Cell. 2019;30(12):1390–1405. DOI: 10.1091/mbc.E18-10-0649.Lewis JD, Caldara AL, Zimmer SE, Stahley SN, Seybold A, Strong NL, Frangakis AS, Levental I, Wahl JK 3rd, Mattheyses AL, Sasaki T, Nakabayashi K, Hata K, Matsubara Y, Ishida-Yamamoto A, Amagai M, Kubo A, Kowalczyk AP. The desmosome is a mesoscale lipid raft-like membrane domain. Mol Biol Cell. 2019;30(12):1390–1405. DOI: 10.1091/mbc.E18-10-0649.Kitajima Y. Mechanisms of desmosome assembly and disassembly. Clin Exp Dermatol. 2002;27(8): 684–690. DOI: 10.1046/j.1365-2230.2002.01116.x.Kitajima Y. Mechanisms of desmosome assembly and disassembly. Clin Exp Dermatol. 2002;27(8): 684–690. DOI: 10.1046/j.1365-2230.2002.01116.x.López-Leal R, Alvarez J, Court FA. Origin of axonal proteins: Is the axon-schwann cell unit a functional syncytium? Cytoskeleton (Hoboken). 2016;73(10):629–639. DOI: 10.1002/cm.21319.López-Leal R, Alvarez J, Court FA. Origin of axonal proteins: Is the axon-schwann cell unit a functional syncytium? Cytoskeleton (Hoboken). 2016;73(10):629–639. DOI: 10.1002/cm.21319.Villarreal S, Lee SH, Wu LG. Measuring Synaptic Vesicle Endocytosis in Cultured Hippocampal Neurons. J Vis Exp. 2017;127:55862. DOI: 10.3791/55862.Villarreal S, Lee SH, Wu LG. Measuring Synaptic Vesicle Endocytosis in Cultured Hippocampal Neurons. J Vis Exp. 2017;127:55862. DOI: 10.3791/55862.Smurova K, Podbilewicz B. Endocytosis regulates membrane localization and function of the fusogen EFF-1. Small GTPases. 2017;8(3):177–180. DOI: 10.1080/21541248.2016.1211399.Smurova K, Podbilewicz B. Endocytosis regulates membrane localization and function of the fusogen EFF-1. Small GTPases. 2017;8(3):177–180. DOI: 10.1080/21541248.2016.1211399.Maritzen T, Haucke V. Coupling of exocytosis and endocytosis at the presynaptic active zone. Neurosci Res. 2018;127:45–52. DOI: 10.1016/j.neures.2017.09.013.Maritzen T, Haucke V. Coupling of exocytosis and endocytosis at the presynaptic active zone. Neurosci Res. 2018;127:45–52. DOI: 10.1016/j.neures.2017.09.013.Kolosov D, Jonusaite S, Donini A, Kelly SP, O'Donnell MJ. Septate junction in the distal ileac plexus of larval lepidopteran Trichoplusia ni: alterations in paracellular permeability during ion transport reversal. Exp Biol. 2019;222(11):pii: jeb204750. DOI: 10.1242/jeb.204750.Kolosov D, Jonusaite S, Donini A, Kelly SP, O'Donnell MJ. Septate junction in the distal ileac plexus of larval lepidopteran Trichoplusia ni: alterations in paracellular permeability during ion transport reversal. Exp Biol. 2019;222(11):pii: jeb204750. DOI: 10.1242/jeb.204750.Li J. Molecular regulators of nerve conduction – Lessons from inherited neuropathies and rodent genetic models. Exp Neurol. 2015;267:209–218. DOI: 10.1016/j.expneurol.2015.03.009Li J. Molecular regulators of nerve conduction – Lessons from inherited neuropathies and rodent genetic models. Exp Neurol. 2015;267:209–218. DOI: 10.1016/j.expneurol.2015.03.009Rosenbluth J. Multiple functions of the paranodal junction of myelinated nerve fibers. J Neurosci Res. 2009;87(15):3250–3258. DOI: 10.1002/jnr.22013.Rosenbluth J. Multiple functions of the paranodal junction of myelinated nerve fibers. J Neurosci Res. 2009;87(15):3250–3258. DOI: 10.1002/jnr.22013.Revenko SV, Sotnikov OS, Hodorov BI. Sravnitel'nyj analiz morfologicheskih i fiziologicheskih harakteristik perekhvata Ranv'e. Nejrofiziologiya. 1978;10(4):400–405.Revenko SV, Sotnikov OS, Hodorov BI. Sravnitel'nyj analiz morfologicheskih i fiziologicheskih harakteristik perekhvata Ranv'e. Nejrofiziologiya. 1978;10(4):400–405.De Mello UK. Mezhkletochnye vzaimodejstviya v serdechnoj myshce. V kn.: Mezhkletochnye vzaimodejstviya, Moskva: Medicina; 1980:95–131.De Mello UK. Mezhkletochnye vzaimodejstviya v serdechnoj myshce. V kn.: Mezhkletochnye vzaimodejstviya, Moskva: Medicina; 1980:95–131.Sotnikov OS, Laktionova AA. Membrane fusion and syncytial neuronal cytoplasmic connection. Switzerland: Trans Tech Publications, Ltd; 2016. 159s.Sotnikov OS, Laktionova AA. Membrane fusion and syncytial neuronal cytoplasmic connection. Switzerland: Trans Tech Publications, Ltd; 2016. 159s.Lim HY, Bao H, Liu Y, Wang W. Select Septate Junction Proteins Direct ROS-Mediated Paracrine Regulation of Drosophila Cardiac Function. Cell Rep. 2019;28(6):1455–1470.e4.Lim HY, Bao H, Liu Y, Wang W. Select Septate Junction Proteins Direct ROS-Mediated Paracrine Regulation of Drosophila Cardiac Function. Cell Rep. 2019;28(6):1455–1470.e4.DOI: 10.1016/j.celrep.2019.07.004.DOI: 10.1016/j.celrep.2019.07.004.Khadilkar RJ, Tanentzapf G.Septate junction components control Drosophila hematopoiesis through the Hippo pathway. Development. 2019;146(7):pii: dev166819. DOI: 10.1242/dev.166819.Khadilkar RJ, Tanentzapf G.Septate junction components control Drosophila hematopoiesis through the Hippo pathway. Development. 2019;146(7):pii: dev166819. DOI: 10.1242/dev.166819.Ganot P, Zoccola D, Tambutté E, Voolstra CR, Aranda M, Allemand D, Tambutté S. Structural molecular components of septate junctions in cnidarians point to the origin of epithelial junctions in eukaryotes. Mol Biol Evol. 2015;32(1):44–62.DOI: 10.1093/molbev/msu265.Ganot P, Zoccola D, Tambutté E, Voolstra CR, Aranda M, Allemand D, Tambutté S. Structural molecular components of septate junctions in cnidarians point to the origin of epithelial junctions in eukaryotes. Mol Biol Evol. 2015;32(1):44–62.DOI: 10.1093/molbev/msu265.Izumi Y, Furuse K, Furuse M. Septate junctions regulate gut homeostasis through regulation of stem cell proliferation and enterocyte behavior in Drosophila. J Cell Sci. 2019;132(18):pii: jcs232108. DOI: 10.1242/jcs.232108.Izumi Y, Furuse K, Furuse M. Septate junctions regulate gut homeostasis through regulation of stem cell proliferation and enterocyte behavior in Drosophila. J Cell Sci. 2019;132(18):pii: jcs232108. DOI: 10.1242/jcs.232108.Komada M, Soriano P. [Beta] IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol. 2002;156(2):337–348. DOI: 10.1083/jcb.200110003.Komada M, Soriano P. [Beta] IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol. 2002;156(2):337–348. DOI: 10.1083/jcb.200110003.Lacas-Gervais S, Guo J, Strenzke N, Scarfone E, Kolpe M, Jahkel M, De Camilli P, Moser T, Rasband MN, Solimena M. BetaIVSigma1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J Cell Biol. 2004;166(7):983–990. DOI: 10.1083/jcb.200408007.Lacas-Gervais S, Guo J, Strenzke N, Scarfone E, Kolpe M, Jahkel M, De Camilli P, Moser T, Rasband MN, Solimena M. BetaIVSigma1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J Cell Biol. 2004;166(7):983–990. DOI: 10.1083/jcb.200408007.Politov AL. Belkovaya poluprovodimost: alternativnoe tolkovanie elektricheskogo soedineniya. V kn.: Mezhkletochnye vzaimodejstviya. Moskva: Medicina; 1980:132–147.Politov AL. Belkovaya poluprovodimost: alternativnoe tolkovanie elektricheskogo soedineniya. V kn.: Mezhkletochnye vzaimodejstviya. Moskva: Medicina; 1980:132–147.Hodorov BI. Obshchaya fiziologiya vozbudimyh membran. Rukovodstvo po fiziologii. Moskva: Nauka; 1975. 406s.Hodorov BI. Obshchaya fiziologiya vozbudimyh membran. Rukovodstvo po fiziologii. Moskva: Nauka; 1975. 406s.Levin SV. Strukturnye izmeneniya kletochnyh membran. Leningrad: Nauka; 1976. 224s.Levin SV. Strukturnye izmeneniya kletochnyh membran. Leningrad: Nauka; 1976. 224s.Braun G, Uolker Dzh. Zhidkie kristally i biologicheskie struktury. Moskva: Mir; 1982. 198s.Braun G, Uolker Dzh. Zhidkie kristally i biologicheskie struktury. Moskva: Mir; 1982. 198s.Vvedenskij NE. Vozbuzhdenie, tormozhenie, narkoz. V kn.: Izbrannye proizvedeniya. Moskva: Medgiz; 1952:291–395.Vvedenskij NE. Vozbuzhdenie, tormozhenie, narkoz. V kn.: Izbrannye proizvedeniya. Moskva: Medgiz; 1952:291–395.Mironov AA, Komissarchik YAYU, Mironov VA. Metody elektronnoj mikroskopii v biologii i medicine. SPb: Nauka; 1994. 400s.Mironov AA, Komissarchik YAYU, Mironov VA. Metody elektronnoj mikroskopii v biologii i medicine. SPb: Nauka; 1994. 400s.Conese M, Carbone A, Beccia E, Angiolillo A. 2017. The Fountain of Youth: A Tale of Parabiosis, Stem Cells, and Rejuvenation. Open Med (Wars). 2017;12():376–383. DOI: 10.1515/med-2017-0053.Conese M, Carbone A, Beccia E, Angiolillo A. 2017. The Fountain of Youth: A Tale of Parabiosis, Stem Cells, and Rejuvenation. Open Med (Wars). 2017;12():376–383. DOI: 10.1515/med-2017-0053.Nasonov DN, Aleksandrov VYA. Reakciya zhivogo veshchestva na vneshnie vozdejstviya. Moskva-Leningrad: Izdatelstvo AN SSSR; 1940. 252s.Nasonov DN, Aleksandrov VYA. Reakciya zhivogo veshchestva na vneshnie vozdejstviya. Moskva-Leningrad: Izdatelstvo AN SSSR; 1940. 252s.Nasonov DN. Mestnaya reakciya protoplazmy i rasprostranyayushcheesya vozbuzhdenie. Moskva-Leningrad. Izdatel'stvo AN SSSR; 1962. 437s.Nasonov DN. Mestnaya reakciya protoplazmy i rasprostranyayushcheesya vozbuzhdenie. Moskva-Leningrad. Izdatel'stvo AN SSSR; 1962. 437s.Ling G. Fizicheskaya teoriya zhivoj kletki. SPb: Nauka; 2008. 375s.Ling G. Fizicheskaya teoriya zhivoj kletki. SPb: Nauka; 2008. 375s.Perez-Puyana V, Ostos FJ, Lópes-Cornejo F, Romero A, Guerrero A. Assessment of the denaturation of collagen protein concentrates using different techniques. Biol Chem. 2019;400(12):1583–1591. DOI: 10.1515/hsz-2019-0206.Perez-Puyana V, Ostos FJ, Lópes-Cornejo F, Romero A, Guerrero A. Assessment of the denaturation of collagen protein concentrates using different techniques. Biol Chem. 2019;400(12):1583–1591. DOI: 10.1515/hsz-2019-0206.Poghosyan AH, Schafer NP, Lyngsø J, Shahinyan AA, Pedersen JS, Otzen DE. Molecular dynamics study of ACBP denaturation in alkyl sulfates demonstrates possible pathways of unfolding through fused surfactant clusters. Protein Eng Des Sel. 2019;32(4):175–190. DOI: 10.1093/protein/gzz037.Poghosyan AH, Schafer NP, Lyngsø J, Shahinyan AA, Pedersen JS, Otzen DE. Molecular dynamics study of ACBP denaturation in alkyl sulfates demonstrates possible pathways of unfolding through fused surfactant clusters. Protein Eng Des Sel. 2019;32(4):175–190. DOI: 10.1093/protein/gzz037.Srivastava R, Alam MS. Influence of micelles on protein's denaturation. Int J Biol Macromol. 2020; 145:252–261. DOI: 10.1016/j.ijbiomac.2019.12.154.Srivastava R, Alam MS. Influence of micelles on protein's denaturation. Int J Biol Macromol. 2020; 145:252–261. DOI: 10.1016/j.ijbiomac.2019.12.154.Slivko-Koltchik GA, Kuznetsov VP, Panchin YV. Are there gap junctions without connexins or pannexins? BMC Evol Biol. 2019;19(1):46. DOI: 10.1186/s12862-019-1369-4.Slivko-Koltchik GA, Kuznetsov VP, Panchin YV. Are there gap junctions without connexins or pannexins? BMC Evol Biol. 2019;19(1):46. DOI: 10.1186/s12862-019-1369-4.Mueller P, Rudin DO. Action potentials induced in biomolecular lipid membranes. Nature. 1968;217(5130):713–719. DOI: 10.1038/217713a0.Mueller P, Rudin DO. Action potentials induced in biomolecular lipid membranes. Nature. 1968;217(5130):713–719. DOI: 10.1038/217713a0.Rosenberg B, Postow E. Semiconductivity in proteins and nucleic acids. In book: Experimental Methods in Biophysical Chemistry (C. Nicolau), New York: Wiley; 1973. 315s.Rosenberg B, Postow E. Semiconductivity in proteins and nucleic acids. In book: Experimental Methods in Biophysical Chemistry (C. Nicolau), New York: Wiley; 1973. 315s.Belousov AB, Wang Y, Song JH, Denisova JV, Berman NE, Fontes JD. Neuronal gap junctions play a role in the secondary neuronal death following controlled cortical impact. Neurosci. Lett. 2012;524(1):16–19. DOI: 10.1016/j.neulet.2012.06.065.Belousov AB, Wang Y, Song JH, Denisova JV, Berman NE, Fontes JD. Neuronal gap junctions play a role in the secondary neuronal death following controlled cortical impact. Neurosci. Lett. 2012;524(1):16–19. DOI: 10.1016/j.neulet.2012.06.065.Belousov AB, Fontes JD. Neuronal gap junctions: making and breaking connections during development and injury. Trends Neurosci. 2013; 36(4):227–236. DOI: 10.1016/j.tins.2012.11.001.Belousov AB, Fontes JD. Neuronal gap junctions: making and breaking connections during development and injury. Trends Neurosci. 2013; 36(4):227–236. DOI: 10.1016/j.tins.2012.11.001.Battefeld A, Klooster J, Kole MH. Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity. Nat Commun. 2016;7():11298. DOI: 10.1038/ncomms11298.Battefeld A, Klooster J, Kole MH. Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity. Nat Commun. 2016;7():11298. DOI: 10.1038/ncomms11298.Ma D, Feng L, Cheng Y, Xin M, You J, Yin X, Hao Y, Cui L, Feng J. Astrocytic gap junction inhibition by carbenoxolone enhances the protective effects of ischemic preconditioning following cerebral ischemia. J Neuroinflammation. 2018;15(1):198. DOI: 10.1186/s12974-018-1230-5.Ma D, Feng L, Cheng Y, Xin M, You J, Yin X, Hao Y, Cui L, Feng J. Astrocytic gap junction inhibition by carbenoxolone enhances the protective effects of ischemic preconditioning following cerebral ischemia. J Neuroinflammation. 2018;15(1):198. DOI: 10.1186/s12974-018-1230-5.Menichella DM., Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci. 2006;26(43):10984–10991. DOI: 10.1523/JNEUROSCI.0304-06.2006.Menichella DM., Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci. 2006;26(43):10984–10991. DOI: 10.1523/JNEUROSCI.0304-06.2006.Pannasch U, Derangeon M, Chever O, Rouach N. Astroglial gap junctions shape neuronal network activity. Commun Integr Biol. 2012;5(3):248–254. DOI: 10.4161/cib.19410.Pannasch U, Derangeon M, Chever O, Rouach N. Astroglial gap junctions shape neuronal network activity. Commun Integr Biol. 2012;5(3):248–254. DOI: 10.4161/cib.19410.Ioannou MS, Liu Z, Lippincott-Schwartz J. A Neuron-Glia Co-culture System for Studying Intercellular Lipid Transport. Curr Protoc Cell Biol. 2019;84(1):e95. DOI: 10.1002/cpcb.95.Ioannou MS, Liu Z, Lippincott-Schwartz J. A Neuron-Glia Co-culture System for Studying Intercellular Lipid Transport. Curr Protoc Cell Biol. 2019;84(1):e95. DOI: 10.1002/cpcb.95.Sun EW, Guillen-Samander A, Bian X, Wu Y, Cai Y, Messa M, De Camilli P. Lipid transporter TMEM24/C2CD2L is a Ca2+-regulated component of ER-plasma membrane contacts in mammalian neurons. Proc Natl Acad Sci USA. 2019;116(12):5775–5784. DOI: 10.1073/pnas.1820156116.Sun EW, Guillen-Samander A, Bian X, Wu Y, Cai Y, Messa M, De Camilli P. Lipid transporter TMEM24/C2CD2L is a Ca2+-regulated component of ER-plasma membrane contacts in mammalian neurons. Proc Natl Acad Sci USA. 2019;116(12):5775–5784. DOI: 10.1073/pnas.1820156116.Buzsáki G. Electrical wiring of the oscillating brain. Neuron. 2001;31(3):342–344.Buzsáki G. Electrical wiring of the oscillating brain. Neuron. 2001;31(3):342–344.Draguhn A, Traub RD, Bibbig A, Schmitz D. Ripple (approximately 200-Hz) oscillations in temporal structures. J. Clin. Neurophysiol. 2000;17(4):361–376. DOI: 10.1097/00004691-200007000-00003.Draguhn A, Traub RD, Bibbig A, Schmitz D. Ripple (approximately 200-Hz) oscillations in temporal structures. J. Clin. Neurophysiol. 2000;17(4):361–376. DOI: 10.1097/00004691-200007000-00003.Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron. 2001;31():477–485. DOI: 10.1016/s0896-6273(01)00373-7.Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron. 2001;31():477–485. DOI: 10.1016/s0896-6273(01)00373-7.Traub RD, Pais I, Bibbig A, Le Beau FEN, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA. 2003. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc. Natl. Acad. Sci. USA. 2003;100(3):1370–1374. DOI: 10.1073/pnas.0337529100.Traub RD, Pais I, Bibbig A, Le Beau FEN, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA. 2003. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc. Natl. Acad. Sci. USA. 2003;100(3):1370–1374. DOI: 10.1073/pnas.0337529100.Berkinblit MB, Bozhkova VN, Bojcova LYU. Vysokopronicaemye kontaktnye membrany i ih rol v mezhkletochnyh vzaimodejstviyah. Moskva: Nauka; 1981. 464s.Berkinblit MB, Bozhkova VN, Bojcova LYU. Vysokopronicaemye kontaktnye membrany i ih rol v mezhkletochnyh vzaimodejstviyah. Moskva: Nauka; 1981. 464s.Ben-Yaakov K, Dagan SY, Segal-Ruder Y, Shalem O, Vuppalanchi D, Willis DE, Yudin D, Rishal I, Rother F, Bader M, Blesch A, Pilpel Y, Twiss JL, Fainzilber M. 2012. Axonal transcription factors signal retrogradely in lesioned peripheral nerve. EMBO J. 2012;31(6):1350–1363. DOI: 10.1038/emboj.2011.494.Ben-Yaakov K, Dagan SY, Segal-Ruder Y, Shalem O, Vuppalanchi D, Willis DE, Yudin D, Rishal I, Rother F, Bader M, Blesch A, Pilpel Y, Twiss JL, Fainzilber M. 2012. Axonal transcription factors signal retrogradely in lesioned peripheral nerve. EMBO J. 2012;31(6):1350–1363. DOI: 10.1038/emboj.2011.494.Lopez-Verrilli MA, Picou F, Court FA. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia. 2013;61(11):1795–1806. DOI: 10.1002/glia.22558.Lopez-Verrilli MA, Picou F, Court FA. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia. 2013;61(11):1795–1806. DOI: 10.1002/glia.22558.

The authors declare that there are no conflicts of interest present.