Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Astroglial Connexins in Neurological and Neuropsychological Disorders and Radiation Exposure

Author(s): Yuan Duo Liu, Ge Tang, Feng Qian, Lian Liu*, Jiang Rong Huang* and Feng Ru Tang*

Volume 28, Issue 10, 2021

Published on: 10 June, 2020

Page: [1970 - 1986] Pages: 17

DOI: 10.2174/0929867327666200610175037

Price: $65

Abstract

Radiotherapy is a common treatment for brain and spinal cord tumors and also a risk factor for neuropathological changes in the brain leading to different neurological and neuropsychological disorders. Astroglial connexins are involved in brain inflammation, development of Alzheimer’s Disease (AD), depressive, epilepsy, and amyotrophic lateral sclerosis, and are affected by radiation exposure. Therefore, it is speculated that radiation-induced changes of astroglial connexins may be related to the brain neuropathology and development of neurological and neuropsychological disorders. In this paper, we review the functional expression and regulation of astroglial connexins expressed between astrocytes and different types of brain cells (including oligodendrocytes, microglia, neurons and endothelial cells). The roles of these connexins in the development of AD, depressive, epilepsy, amyotrophic lateral sclerosis and brain inflammation have also been summarized. The radiation-induced astroglial connexins changes and development of different neurological and neuropsychological disorders are then discussed. Based on currently available data, we propose that radiation-induced astroglial connexins changes may be involved in the genesis of different neurological and neuropsychological disorders which depends on the age, brain regions, and radiation doses/dose rates. The abnormal astroglial connexins may be novel therapeutic targets for the prevention of radiation-induced cognitive impairment, neurological and neuropsychological disorders.

Keywords: Alzheimer's Disease (AD), astroglial connexins, brain cells, neurological disorders, neuropsychological disorders, radiation exposure.

« Previous Next »
[1]
Poon, R.; Badawy, M.K. Radiation dose and risk to the lens of the eye during CT examinations of the brain. J. Med. Imaging Radiat. Oncol., 2019, 63(6), 786-794.
[http://dx.doi.org/10.1111/1754-9485.12950] [PMID: 31520467]
[2]
Lehrer, S.; Rheinstein, P.H.; Rosenzweig, K.E. Association of radon background and total background ionizing radiation with Alzheimer’s disease deaths in U.S. States. J. Alzheimers Dis., 2017, 59(2), 737-741.
[http://dx.doi.org/10.3233/JAD-170308] [PMID: 28671130]
[3]
Schulte, P.A.; Burnett, C.A.; Boeniger, M.F.; Johnson, J. Neurodegenerative diseases: occupational occurrence and potential risk factors, 1982 through 1991. Am. J. Public Health, 1996, 86(9), 1281-1288.
[http://dx.doi.org/10.2105/AJPH.86.9.1281] [PMID: 8806381]
[4]
Loganovsky, K.N.; Vasilenko, Z.L. Depression and ionizing radiation. Probl. Radiac. Med. Radiobiol., 2013, (18), 200-219.
[PMID: 25191725]
[5]
Loganovsky, K.N.; Loganovskaja, T.K. Schizophrenia spectrum disorders in persons exposed to ionizing radiation as a result of the Chernobyl accident. Schizophr. Bull., 2000, 26(4), 751-773.
[http://dx.doi.org/10.1093/oxfordjournals.schbul.a033492] [PMID: 11087010]
[6]
Loganovskiĭ, K.N. Neurological and psychopathological syndromes in the follow-up period after exposure to ionizing radiation. Zh. Nevrol. Psikhiatr. Im. S. S. Korsakova, 2000, 100(4), 15-21.
[PMID: 10812665]
[7]
Rivera, A.D.; Butt, A.M. Astrocytes are direct cellular targets of lithium treatment: novel roles for lysyl oxidase and peroxisome-proliferator activated receptor-γ as astroglial targets of lithium. Transl. Psychiatry, 2019, 9(1), 211.
[http://dx.doi.org/10.1038/s41398-019-0542-2] [PMID: 31477687]
[8]
Rodríguez-Arellano, J.J.; Parpura, V.; Zorec, R.; Verkhratsky, A. Astrocytes in physiological aging and Alzheimer’s disease. Neuroscience, 2016, 323, 170-182.
[http://dx.doi.org/10.1016/j.neuroscience.2015.01.007] [PMID: 25595973]
[9]
Sun, L.; Min, L.; Zhou, H.; Li, M.; Shao, F.; Wang, W. Adolescent social isolation affects schizophrenia-like behavior and astrocyte biomarkers in the PFC of adult rats. Behav. Brain Res., 2017, 333, 258-266.
[http://dx.doi.org/10.1016/j.bbr.2017.07.011] [PMID: 28705472]
[10]
Nielsen, M.S.; Axelsen, L.N.; Sorgen, P.L.; Verma, V.; Delmar, M.; Holstein-Rathlou, N.-H. Gap junctions. Compr. Physiol., 2012, 2(3), 1981-2035.
[http://dx.doi.org/10.1002/cphy.c110051] [PMID: 23723031]
[11]
Wasseff, S.K.; Scherer, S.S. Cx32 and Cx47 mediate oligodendrocyte:astrocyte and oligodendrocyte: oligodendrocyte gap junction coupling. Neurobiol. Dis., 2011, 42(3), 506-513.
[http://dx.doi.org/10.1016/j.nbd.2011.03.003] [PMID: 21396451]
[12]
Lynn, B.D.; Tress, O.; May, D.; Willecke, K.; Nagy, J.I. Ablation of connexin30 in transgenic mice alters expression patterns of connexin26 and connexin32 in glial cells and leptomeninges. Eur. J. Neurosci., 2011, 34(11), 1783-1793.
[http://dx.doi.org/10.1111/j.1460-9568.2011.07900.x] [PMID: 22098503]
[13]
Retamal, M.A.; Alcayaga, J.; Verdugo, C.A.; Bultynck, G.; Leybaert, L.; Sáez, P.J.; Fernández, R.; León, L.E.; Sáez, J.C. Opening of pannexin- and connexin-based channels increases the excitability of nodose ganglion sensory neurons. Front. Cell. Neurosci., 2014, 8, 158.
[http://dx.doi.org/10.3389/fncel.2014.00158] [PMID: 24999316]
[14]
Nielsen, B.S.; Hansen, D.B.; Ransom, B.R.; Nielsen, M.S.; MacAulay, N. Connexin hemichannels in astrocytes: an assessment of controversies regarding their functional characteristics. Neurochem. Res., 2017, 42(9), 2537-2550.
[http://dx.doi.org/10.1007/s11064-017-2243-7] [PMID: 28434165]
[15]
Takeuchi, H.; Suzumura, A. Gap junctions and hemichannels composed of connexins: potential therapeutic targets for neurodegenerative diseases. Front. Cell. Neurosci., 2014, 8, 189.
[http://dx.doi.org/10.3389/fncel.2014.00189] [PMID: 25228858]
[16]
Huang, D.; Li, C.; Zhang, W.; Qin, J.; Jiang, W.; Hu, C. Dysfunction of astrocytic connexins 30 and 43 in the medial prefrontal cortex and hippocampus mediates depressive-like behaviours. Behav. Brain Res., 2019, 372, 111950.
[http://dx.doi.org/10.1016/j.bbr.2019.111950] [PMID: 31103752]
[17]
Fatemi, S.H.; Folsom, T.D.; Reutiman, T.J.; Pandian, T.; Braun, N.N.; Haug, K. Chronic psychotropic drug treatment causes differential expression of connexin 43 and GFAP in frontal cortex of rats. Schizophr. Res., 2008, 104(1-3), 127-134.
[http://dx.doi.org/10.1016/j.schres.2008.05.016] [PMID: 18585900]
[18]
Wu, X.L.; Ma, D.M.; Zhang, W.; Zhou, J.S.; Huo, Y.W.; Lu, M.; Tang, F.R. Cx36 in the mouse hippocampus during and after pilocarpine-induced status epilepticus. Epilepsy Res., 2018, 141, 64-72.
[http://dx.doi.org/10.1016/j.eplepsyres.2018.02.007] [PMID: 29476948]
[19]
Wu, X.L.; Tang, Y.C.; Lu, Q.Y.; Xiao, X.L.; Song, T.B.; Tang, F.R. Astrocytic Cx 43 and Cx 40 in the mouse hippocampus during and after pilocarpine-induced status epilepticus. Exp. Brain Res., 2015, 233(5), 1529-1539.
[http://dx.doi.org/10.1007/s00221-015-4226-8] [PMID: 25690864]
[20]
Yi, C.; Koulakoff, A.; Giaume, C. Astroglial connexins as a therapeutic target for Alzheimer’s disease. Curr. Pharm. Des., 2017, 23(33), 4958-4968.
[http://dx.doi.org/10.2174/1381612823666171004151215] [PMID: 28982320]
[21]
Xing, L.; Yang, T.; Cui, S.; Chen, G. Connexin hemichannels in astrocytes: role in CNS disorders. Front. Mol. Neurosci., 2019, 12, 23.
[http://dx.doi.org/10.3389/fnmol.2019.00023] [PMID: 30787868]
[22]
Wang, H.; Segaran, R.C.; Chan, L.Y.; Aladresi, A.A.M.; Chinnathambi, A.; Alharbi, S.A.; Sethi, G.; Tang, F.R. Gamma radiation-induced disruption of cellular junctions in HUVECs is mediated through affecting MAPK/NF-κB inflammatory pathways. Oxid. Med. Cell. Longev., 2019, 2019, 1486232.
[http://dx.doi.org/10.1155/2019/1486232] [PMID: 31467629]
[23]
Yang, X.; Xu, S.; Su, Y.; Chen, B.; Yuan, H.; Xu, A.; Wu, L. Autophagy-Src regulates connexin43-mediated gap junction intercellular communication in irradiated HepG2 cells. Radiat. Res., 2018, 190(5), 494-503.
[http://dx.doi.org/10.1667/RR15073.1] [PMID: 30095367]
[24]
Viczenczova, C.; Szeiffova Bacova, B.; Egan Benova, T.; Kura, B.; Yin, C.; Weismann, P.; Kukreja, R.; Slezak, J.; Tribulova, N. Myocardial connexin-43 and PKC signalling are involved in adaptation of the heart to irradiation-induced injury: implication of miR-1 and miR-21. Gen. Physiol. Biophys., 2016, 35(2), 215-222.
[http://dx.doi.org/10.4149/gpb_2015038] [PMID: 26830133]
[25]
De Bock, M.; Wang, N.; Decrock, E.; Bol, M.; Gadicherla, A.K.; Culot, M.; Cecchelli, R.; Bultynck, G.; Leybaert, L. Endothelial calcium dynamics, connexin channels and blood-brain barrier function. Prog. Neurobiol., 2013, 108, 1-20.
[http://dx.doi.org/10.1016/j.pneurobio.2013.06.001] [PMID: 23851106]
[26]
De Bock, M.; Culot, M.; Wang, N.; Bol, M.; Decrock, E.; De Vuyst, E.; da Costa, A.; Dauwe, I.; Vinken, M.; Simon, A.M.; Rogiers, V.; De Ley, G.; Evans, W.H.; Bultynck, G.; Dupont, G.; Cecchelli, R.; Leybaert, L. Connexin channels provide a target to manipulate brain endothelial calcium dynamics and blood-brain barrier permeability. J. Cereb. Blood Flow Metab., 2011, 31(9), 1942-1957.
[http://dx.doi.org/10.1038/jcbfm.2011.86] [PMID: 21654699]
[27]
Belousov, A.B.; Fontes, J.D.; Freitas-Andrade, M.; Naus, C.C. Gap junctions and hemichannels: communicating cell death in neurodevelopment and disease. BMC Cell Biol., 2017, 18(Suppl. 1), 4.
[http://dx.doi.org/10.1186/s12860-016-0120-x] [PMID: 28124625]
[28]
Rash, J.E.; Yasumura, T.; Dudek, F.E.; Nagy, J.I. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci., 2001, 21(6), 1983-2000.
[http://dx.doi.org/10.1523/JNEUROSCI.21-06-01983.2001] [PMID: 11245683]
[29]
Niu, J.; Li, T.; Yi, C.; Huang, N.; Koulakoff, A.; Weng, C.; Li, C.; Zhao, C.J.; Giaume, C.; Xiao, L. Connexin-based channels contribute to metabolic pathways in the oligodendroglial lineage. J. Cell Sci., 2016, 129(9), 1902-1914.
[http://dx.doi.org/10.1242/jcs.178731] [PMID: 27006115]
[30]
Lapato, A.S.; Tiwari-Woodruff, S.K. Connexins and pannexins: at the junction of neuro-glial homeostasis and disease. J. Neurosci. Res., 2018, 96(1), 31-44.
[http://dx.doi.org/10.1002/jnr.24088] [PMID: 28580666]
[31]
Massa, P.T.; Mugnaini, E. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience, 1982, 7(2), 523-538.
[http://dx.doi.org/10.1016/0306-4522(82)90285-8] [PMID: 7078735]
[32]
Fasciani, I.; Pluta, P.; González-Nieto, D.; Martínez-Montero, P.; Molano, J.; Paíno, C.L.; Millet, O.; Barrio, L.C. Directional coupling of oligodendrocyte connexin-47 and astrocyte connexin-43 gap junctions. Glia, 2018, 66(11), 2340-2352.
[http://dx.doi.org/10.1002/glia.23471] [PMID: 30144323]
[33]
Tress, O.; Maglione, M.; May, D.; Pivneva, T.; Richter, N.; Seyfarth, J.; Binder, S.; Zlomuzica, A.; Seifert, G.; Theis, M.; Dere, E.; Kettenmann, H.; Willecke, K. Panglial gap junctional communication is essential for maintenance of myelin in the CNS. J. Neurosci., 2012, 32(22), 7499-7518.
[http://dx.doi.org/10.1523/JNEUROSCI.0392-12.2012] [PMID: 22649229]
[34]
Kamasawa, N.; Sik, A.; Morita, M.; Yasumura, T.; Davidson, K.G.; Nagy, J.I.; Rash, J.E. Connexin-47 and connexin-32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops and Schmidt-Lanterman incisures: implications for ionic homeostasis and potassium siphoning. Neuroscience, 2005, 136(1), 65-86.
[http://dx.doi.org/10.1016/j.neuroscience.2005.08.027] [PMID: 16203097]
[35]
Kleopa, K.A.; Orthmann, J.L.; Enriquez, A.; Paul, D.L.; Scherer, S.S. Unique distributions of the gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia, 2004, 47(4), 346-357.
[http://dx.doi.org/10.1002/glia.20043] [PMID: 15293232]
[36]
Orthmann-Murphy, J.L.; Abrams, C.K.; Scherer, S.S. Gap junctions couple astrocytes and oligodendrocytes. J. Mol. Neurosci., 2008, 35(1), 101-116.
[http://dx.doi.org/10.1007/s12031-007-9027-5] [PMID: 18236012]
[37]
Sargiannidou, I.; Vavlitou, N.; Aristodemou, S.; Hadjisavvas, A.; Kyriacou, K.; Scherer, S.S.; Kleopa, K.A. Connexin32 mutations cause loss of function in Schwann cells and oligodendrocytes leading to PNS and CNS myelination defects. J. Neurosci., 2009, 29(15), 4736-4749.
[http://dx.doi.org/10.1523/JNEUROSCI.0325-09.2009] [PMID: 19369543]
[38]
Kalsi, A.S.; Greenwood, K.; Wilkin, G.; Butt, A.M. Kir4.1 expression by astrocytes and oligodendrocytes in CNS white matter: a developmental study in the rat optic nerve. J. Anat., 2004, 204(6), 475-485.
[http://dx.doi.org/10.1111/j.0021-8782.2004.00288.x] [PMID: 15198689]
[39]
Djukic, B.; Casper, K.B.; Philpot, B.D.; Chin, L.S.; McCarthy, K.D. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J. Neurosci., 2007, 27(42), 11354-11365.
[http://dx.doi.org/10.1523/JNEUROSCI.0723-07.2007] [PMID: 17942730]
[40]
Olsen, M.L.; Higashimori, H.; Campbell, S.L.; Hablitz, J.J.; Sontheimer, H. Functional expression of Kir4.1 channels in spinal cord astrocytes. Glia, 2006, 53(5), 516-528.
[http://dx.doi.org/10.1002/glia.20312] [PMID: 16369934]
[41]
Wallraff, A.; Köhling, R.; Heinemann, U.; Theis, M.; Willecke, K.; Steinhäuser, C. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci., 2006, 26(20), 5438-5447.
[http://dx.doi.org/10.1523/JNEUROSCI.0037-06.2006] [PMID: 16707796]
[42]
Jiang, L.; Xu, D.; Zhang, W.J.; Tang, Y.; Peng, Y. Astrocytes induce proliferation of oligodendrocyte progenitor cells via connexin 47-mediated activation of Chi3l1 expression. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(7), 3012-3020.
[http://dx.doi.org/10.26355/eurrev_201904_17583] [PMID: 31002152]
[43]
Xu, D.; Liu, Z.; Wang, S.; Peng, Y.; Sun, X. Astrocytes regulate the expression of Sp1R3 on oligodendrocyte progenitor cells through Cx47 and promote their proliferation. Biochem. Biophys. Res. Commun., 2017, 490(3), 670-675.
[http://dx.doi.org/10.1016/j.bbrc.2017.06.099] [PMID: 28634078]
[44]
Liu, Z.; Xu, D.; Wang, S.; Chen, Y.; Li, Z.; Gao, X.; Jiang, L.; Tang, Y.; Peng, Y. Astrocytes induce proliferation of oligodendrocyte progenitor cells via connexin 47-mediated activation of the ERK/Id4 pathway. Cell Cycle, 2017, 16(7), 714-722.
[http://dx.doi.org/10.1080/15384101.2017.1295183] [PMID: 28278052]
[45]
Papaneophytou, C.P.; Georgiou, E.; Karaiskos, C.; Sargiannidou, I.; Markoullis, K.; Freidin, M.M.; Abrams, C.K.; Kleopa, K.A. Regulatory role of oligodendrocyte gap junctions in inflammatory demyelination. Glia, 2018, 66(12), 2589-2603.
[http://dx.doi.org/10.1002/glia.23513] [PMID: 30325069]
[46]
Markoullis, K.; Sargiannidou, I.; Gardner, C.; Hadjisavvas, A.; Reynolds, R.; Kleopa, K.A. Disruption of oligodendrocyte gap junctions in experimental autoimmune encephalomyelitis. Glia, 2012, 60(7), 1053-1066.
[http://dx.doi.org/10.1002/glia.22334] [PMID: 22461072]
[47]
May, D.; Tress, O.; Seifert, G.; Willecke, K. Connexin47 protein phosphorylation and stability in oligodendrocytes depend on expression of connexin43 protein in astrocytes. J. Neurosci., 2013, 33(18), 7985-7996.
[http://dx.doi.org/10.1523/JNEUROSCI.5874-12.2013] [PMID: 23637189]
[48]
Magnotti, L.M.; Goodenough, D.A.; Paul, D.L. Deletion of oligodendrocyte Cx32 and astrocyte Cx43 causes white matter vacuolation, astrocyte loss and early mortality. Glia, 2011, 59(7), 1064-1074.
[http://dx.doi.org/10.1002/glia.21179] [PMID: 21538560]
[49]
Richter, N.; Wendt, S.; Georgieva, P.B.; Hambardzumyan, D.; Nolte, C.; Kettenmann, H. Glioma-associated microglia and macrophages/monocytes display distinct electrophysiological properties and do not communicate via gap junctions. Neurosci. Lett., 2014, 583, 130-135.
[http://dx.doi.org/10.1016/j.neulet.2014.09.035] [PMID: 25261595]
[50]
Gajardo-Gómez, R.; Labra, V.C.; Orellana, J.A. Connexins and pannexins: new insights into microglial functions and dysfunctions. Front. Mol. Neurosci., 2016, 9, 86.
[http://dx.doi.org/10.3389/fnmol.2016.00086] [PMID: 27713688]
[51]
Takeuchi, H.; Jin, S.; Suzuki, H.; Doi, Y.; Liang, J.; Kawanokuchi, J.; Mizuno, T.; Sawada, M.; Suzumura, A. Blockade of microglial glutamate release protects against ischemic brain injury. Exp. Neurol., 2008, 214(1), 144-146.
[http://dx.doi.org/10.1016/j.expneurol.2008.08.001] [PMID: 18775425]
[52]
Shijie, J.; Takeuchi, H.; Yawata, I.; Harada, Y.; Sonobe, Y.; Doi, Y.; Liang, J.; Hua, L.; Yasuoka, S.; Zhou, Y.; Noda, M.; Kawanokuchi, J.; Mizuno, T.; Suzumura, A. Blockade of glutamate release from microglia attenuates experimental autoimmune encephalomyelitis in mice. Tohoku J. Exp. Med., 2009, 217(2), 87-92.
[http://dx.doi.org/10.1620/tjem.217.87] [PMID: 19212100]
[53]
Liu, W.; Tang, Y.; Feng, J. Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci., 2011, 89(5-6), 141-146.
[http://dx.doi.org/10.1016/j.lfs.2011.05.011] [PMID: 21684291]
[54]
Retamal, M.A.; Froger, N.; Palacios-Prado, N.; Ezan, P.; Sáez, P.J.; Sáez, J.C.; Giaume, C. Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J. Neurosci., 2007, 27(50), 13781-13792.
[http://dx.doi.org/10.1523/JNEUROSCI.2042-07.2007] [PMID: 18077690]
[55]
Abudara, V.; Roux, L.; Dallérac, G.; Matias, I.; Dulong, J.; Mothet, J.P.; Rouach, N.; Giaume, C. Activated microglia impairs neuroglial interaction by opening Cx43 hemichannels in hippocampal astrocytes. Glia, 2015, 63(5), 795-811.
[http://dx.doi.org/10.1002/glia.22785] [PMID: 25643695]
[56]
Chávez, C.E.; Oyarzún, J.E.; Avendaño, B.C.; Mellado, L.A.; Inostroza, C.A.; Alvear, T.F.; Orellana, J.A. The opening of connexin 43 hemichannels alters hippocampal astrocyte function and neuronal survival in prenatally LPS-exposed adult offspring. Front. Cell. Neurosci., 2019, 13, 460.
[http://dx.doi.org/10.3389/fncel.2019.00460] [PMID: 31680871]
[57]
Fang, M.; Yamasaki, R.; Li, G.; Masaki, K.; Yamaguchi, H.; Fujita, A.; Isobe, N.; Kira, J.I. Connexin 30 deficiency attenuates chronic but not acute phases of experimental autoimmune encephalomyelitis through induction of neuroprotective microglia. Front. Immunol., 2018, 9, 2588.
[http://dx.doi.org/10.3389/fimmu.2018.02588] [PMID: 30464764]
[58]
Suadicani, S.O.; Iglesias, R.; Wang, J.; Dahl, G.; Spray, D.C.; Scemes, E. ATP signaling is deficient in cultured pannexin1-null mouse astrocytes. Glia, 2012, 60(7), 1106-1116.
[http://dx.doi.org/10.1002/glia.22338] [PMID: 22499153]
[59]
Orellana, J.A.; Froger, N.; Ezan, P.; Jiang, J.X.; Bennett, M.V.; Naus, C.C.; Giaume, C.; Sáez, J.C. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J. Neurochem., 2011, 118(5), 826-840.
[http://dx.doi.org/10.1111/j.1471-4159.2011.07210.x] [PMID: 21294731]
[60]
Anderson, C.M.; Bergher, J.P.; Swanson, R.A. ATP-induced ATP release from astrocytes. J. Neurochem., 2004, 88(1), 246-256.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02204.x] [PMID: 14675168]
[61]
Schipke, C.G.; Boucsein, C.; Ohlemeyer, C.; Kirchhoff, F.; Kettenmann, H. Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices. FASEB J., 2002, 16(2), 255-257.
[http://dx.doi.org/10.1096/fj.01-0514fje] [PMID: 11772946]
[62]
Inoue, K. Microglial activation by purines and pyrimidines. Glia, 2002, 40(2), 156-163.
[http://dx.doi.org/10.1002/glia.10150] [PMID: 12379903]
[63]
Orellana, J.A.; Montero, T.D.; von Bernhardi, R. Astrocytes inhibit nitric oxide-dependent Ca(2+) dynamics in activated microglia: involvement of ATP released via pannexin 1 channels. Glia, 2013, 61(12), 2023-2037.
[http://dx.doi.org/10.1002/glia.22573] [PMID: 24123492]
[64]
Ma, Y.; Cao, W.; Wang, L.; Jiang, J.; Nie, H.; Wang, B.; Wei, X.; Ying, W. Basal CD38/cyclic ADP-ribose-dependent signaling mediates ATP release and survival of microglia by modulating connexin 43 hemichannels. Glia, 2014, 62(6), 943-955.
[http://dx.doi.org/10.1002/glia.22651] [PMID: 24578339]
[65]
De Bock, M.; Wang, N.; Bol, M.; Decrock, E.; Ponsaerts, R.; Bultynck, G.; Dupont, G.; Leybaert, L. Connexin 43 hemichannels contribute to cytoplasmic Ca2+ oscillations by providing a bimodal Ca2+-dependent Ca2+ entry pathway. J. Biol. Chem., 2012, 287(15), 12250-12266.
[http://dx.doi.org/10.1074/jbc.M111.299610] [PMID: 22351781]
[66]
Wang, N.; De Bock, M.; Antoons, G.; Gadicherla, A.K.; Bol, M.; Decrock, E.; Evans, W.H.; Sipido, K.R.; Bukauskas, F.F.; Leybaert, L. Connexin mimetic peptides inhibit Cx43 hemichannel opening triggered by voltage and intracellular Ca2+ elevation. Basic Res. Cardiol., 2012, 107(6), 304.
[http://dx.doi.org/10.1007/s00395-012-0304-2] [PMID: 23095853]
[67]
Bezzi, P.; Volterra, A. A neuron-glia signalling network in the active brain. Curr. Opin. Neurobiol., 2001, 11(3), 387-394.
[http://dx.doi.org/10.1016/S0959-4388(00)00223-3] [PMID: 11399439]
[68]
Gow, A.; Devaux, J. A model of tight junction function in central nervous system myelinated axons. Neuron Glia Biol., 2008, 4(4), 307-317.
[http://dx.doi.org/10.1017/S1740925X09990391] [PMID: 20102674]
[69]
Devaux, J.; Gow, A. Tight junctions potentiate the insulative properties of small CNS myelinated axons. J. Cell Biol., 2008, 183(5), 909-921.
[http://dx.doi.org/10.1083/jcb.200808034] [PMID: 19047465]
[70]
Alvarez-Maubecin, V.; Garcia-Hernandez, F.; Williams, J.T.; Van Bockstaele, E.J. Functional coupling between neurons and glia. J. Neurosci., 2000, 20(11), 4091-4098.
[http://dx.doi.org/10.1523/JNEUROSCI.20-11-04091.2000] [PMID: 10818144]
[71]
Rash, J.E.; Olson, C.O.; Davidson, K.G.; Yasumura, T.; Kamasawa, N.; Nagy, J.I. Identification of connexin36 in gap junctions between neurons in rodent locus coeruleus. Neuroscience, 2007, 147(4), 938-956.
[http://dx.doi.org/10.1016/j.neuroscience.2007.04.061] [PMID: 17601673]
[72]
Rozental, R.; Giaume, C.; Spray, D.C. Gap junctions in the nervous system. Brain Res. Brain Res. Rev., 2000, 32(1), 11-15.
[http://dx.doi.org/10.1016/S0165-0173(99)00095-8] [PMID: 10928802]
[73]
Murphy, T.H.; Blatter, L.A.; Wier, W.G.; Baraban, J.M. Rapid communication between neurons and astrocytes in primary cortical cultures. J. Neurosci., 1993, 13(6), 2672-2679.
[http://dx.doi.org/10.1523/JNEUROSCI.13-06-02672.1993] [PMID: 8501531]
[74]
Fróes, M.M.; Correia, A.H.; Garcia-Abreu, J.; Spray, D.C.; de Carvalho, A.C.C.; Neto, M.V. Gap-junctional coupling between neurons and astrocytes in primary central nervous system cultures. Proc. Natl. Acad. Sci. USA, 1999, 96(13), 7541-7546.
[http://dx.doi.org/10.1073/pnas.96.13.7541] [PMID: 10377451]
[75]
Wiencken-Barger, A.E.; Djukic, B.; Casper, K.B.; McCarthy, K.D. A role for connexin43 during neurodevelopment. Glia, 2007, 55(7), 675-686.
[http://dx.doi.org/10.1002/glia.20484] [PMID: 17311295]
[76]
Pannasch, U.; Rouach, N. Emerging role for astroglial networks in information processing: from synapse to behavior. Trends Neurosci., 2013, 36(7), 405-417.
[http://dx.doi.org/10.1016/j.tins.2013.04.004] [PMID: 23659852]
[77]
Rouach, N.; Koulakoff, A.; Abudara, V.; Willecke, K.; Giaume, C. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science, 2008, 322(5907), 1551-1555.
[http://dx.doi.org/10.1126/science.1164022] [PMID: 19056987]
[78]
Clasadonte, J.; Scemes, E.; Wang, Z.; Boison, D.; Haydon, P.G. Connexin 43-mediated astroglial metabolic networks contribute to the regulation of the sleep-wake cycle. Neuron, 2017, 95(6), 1365-1380.
[http://dx.doi.org/10.1016/j.neuron.2017.08.022] [PMID: 28867552]
[79]
Almad, A.A.; Doreswamy, A.; Gross, S.K.; Richard, J.P.; Huo, Y.; Haughey, N.; Maragakis, N.J. Connexin 43 in astrocytes contributes to motor neuron toxicity in amyotrophic lateral sclerosis. Glia, 2016, 64(7), 1154-1169.
[http://dx.doi.org/10.1002/glia.22989] [PMID: 27083773]
[80]
Charvériat, M.; Naus, C.C.; Leybaert, L.; Sáez, J.C.; Giaume, C. Connexin-dependent neuroglial networking as a new therapeutic target. Front. Cell. Neurosci., 2017, 11, 174.
[http://dx.doi.org/10.3389/fncel.2017.00174] [PMID: 28694772]
[81]
Koulakoff, A.; Ezan, P.; Giaume, C. Neurons control the expression of connexin 30 and connexin 43 in mouse cortical astrocytes. Glia, 2008, 56(12), 1299-1311.
[http://dx.doi.org/10.1002/glia.20698] [PMID: 18512249]
[82]
Roux, L.; Benchenane, K.; Rothstein, J.D.; Bonvento, G.; Giaume, C. Plasticity of astroglial networks in olfactory glomeruli. Proc. Natl. Acad. Sci. USA, 2011, 108(45), 18442-18446.
[http://dx.doi.org/10.1073/pnas.1107386108] [PMID: 21997206]
[83]
De Pina-Benabou, M.H.; Srinivas, M.; Spray, D.C.; Scemes, E. Calmodulin kinase pathway mediates the K+-induced increase in Gap junctional communication between mouse spinal cord astrocytes. J. Neurosci., 2001, 21(17), 6635-6643.
[http://dx.doi.org/10.1523/JNEUROSCI.21-17-06635.2001] [PMID: 11517253]
[84]
Liebner, S.; Czupalla, C.J.; Wolburg, H. Current concepts of blood-brain barrier development. Int. J. Dev. Biol., 2011, 55(4-5), 467-476.
[http://dx.doi.org/10.1387/ijdb.103224sl] [PMID: 21769778]
[85]
Mathiisen, T.M.; Lehre, K.P.; Danbolt, N.C.; Ottersen, O.P. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia, 2010, 58(9), 1094-1103.
[http://dx.doi.org/10.1002/glia.20990] [PMID: 20468051]
[86]
Ezan, P.; André, P.; Cisternino, S.; Saubaméa, B.; Boulay, A.C.; Doutremer, S.; Thomas, M.A.; Quenech’du, N.; Giaume, C.; Cohen-Salmon, M. Deletion of astroglial connexins weakens the blood-brain barrier. J. Cereb. Blood Flow Metab., 2012, 32(8), 1457-1467.
[http://dx.doi.org/10.1038/jcbfm.2012.45] [PMID: 22472609]
[87]
Boulay, A.C.; Mazeraud, A.; Cisternino, S.; Saubaméa, B.; Mailly, P.; Jourdren, L.; Blugeon, C.; Mignon, V.; Smirnova, M.; Cavallo, A.; Ezan, P.; Avé, P.; Dingli, F.; Loew, D.; Vieira, P.; Chrétien, F.; Cohen-Salmon, M. Immune quiescence of the brain is set by astroglial connexin 43. J. Neurosci., 2015, 35(10), 4427-4439.
[http://dx.doi.org/10.1523/JNEUROSCI.2575-14.2015] [PMID: 25762685]
[88]
Mazaré, N.; Gilbert, A.; Boulay, A.C.; Rouach, N.; Cohen-Salmon, M. Connexin 30 is expressed in a subtype of mouse brain pericytes. Brain Struct. Funct., 2018, 223(2), 1017-1024.
[http://dx.doi.org/10.1007/s00429-017-1562-4] [PMID: 29143947]
[89]
Koulakoff, A.; Mei, X.; Orellana, J.A.; Sáez, J.C.; Giaume, C. Glial connexin expression and function in the context of Alzheimer’s disease. Biochim. Biophys. Acta, 2012, 1818(8), 2048-2057.
[http://dx.doi.org/10.1016/j.bbamem.2011.10.001] [PMID: 22008509]
[90]
Mei, X.; Ezan, P.; Giaume, C.; Koulakoff, A. Astroglial connexin immunoreactivity is specifically altered at β-amyloid plaques in β-amyloid precursor protein/presenilin1 mice. Neuroscience, 2010, 171(1), 92-105.
[http://dx.doi.org/10.1016/j.neuroscience.2010.08.001] [PMID: 20813165]
[91]
Nagy, J.I.; Li, W.; Hertzberg, E.L.; Marotta, C.A. Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer’s disease. Brain Res., 1996, 717(1-2), 173-178.
[http://dx.doi.org/10.1016/0006-8993(95)01526-4] [PMID: 8738268]
[92]
Kunzelmann, P.; Schröder, W.; Traub, O.; Steinhäuser, C.; Dermietzel, R.; Willecke, K. Late onset and increasing expression of the gap junction protein connexin30 in adult murine brain and long-term cultured astrocytes. Glia, 1999, 25(2), 111-119.
[http://dx.doi.org/10.1002/(SICI)1098-1136(19990115)25: 2<111:::AID-GLIA2>3.0.CO;2-I] [PMID: 9890626]
[93]
Yi, C.; Mei, X.; Ezan, P.; Mato, S.; Matias, I.; Giaume, C.; Koulakoff, A. Astroglial connexin43 contributes to neuronal suffering in a mouse model of Alzheimer’s disease. Cell Death Differ., 2016, 23(10), 1691-1701.
[http://dx.doi.org/10.1038/cdd.2016.63] [PMID: 27391799]
[94]
Davidson, J.O.; Green, C.R.; Bennet, L.; Gunn, A.J. Battle of the hemichannels-connexins and pannexins in ischemic brain injury. Int. J. Dev. Neurosci., 2015, 45, 66-74.
[http://dx.doi.org/10.1016/j.ijdevneu.2014.12.007] [PMID: 25546019]
[95]
Martineau, M.; Parpura, V.; Mothet, J.P. Cell-type specific mechanisms of D-serine uptake and release in the brain. Front. Synaptic Neurosci., 2014, 6, 12.
[http://dx.doi.org/10.3389/fnsyn.2014.00012] [PMID: 24910611]
[96]
Chakroborty, S.; Stutzmann, G.E. Calcium channelopathies and Alzheimer’s disease: insight into therapeutic success and failures. Eur. J. Pharmacol., 2014, 739, 83-95.
[http://dx.doi.org/10.1016/j.ejphar.2013.11.012] [PMID: 24316360]
[97]
Demuro, A.; Parker, I.; Stutzmann, G.E. Calcium signaling and amyloid toxicity in Alzheimer disease. J. Biol. Chem., 2010, 285(17), 12463-12468.
[http://dx.doi.org/10.1074/jbc.R109.080895] [PMID: 20212036]
[98]
Kuchibhotla, K.V.; Goldman, S.T.; Lattarulo, C.R.; Wu, H.Y.; Hyman, B.T.; Bacskai, B.J. Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron, 2008, 59(2), 214-225.
[http://dx.doi.org/10.1016/j.neuron.2008.06.008] [PMID: 18667150]
[99]
Kuchibhotla, K.V.; Lattarulo, C.R.; Hyman, B.T.; Bacskai, B.J. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science, 2009, 323(5918), 1211-1215.
[http://dx.doi.org/10.1126/science.1169096] [PMID: 19251629]
[100]
Wang, Q.; Jie, W.; Liu, J.H.; Yang, J.M.; Gao, T.M. An astroglial basis of major depressive disorder? An overview. Glia, 2017, 65(8), 1227-1250.
[http://dx.doi.org/10.1002/glia.23143] [PMID: 28317185]
[101]
Lutz, S.E.; Zhao, Y.; Gulinello, M.; Lee, S.C.; Raine, C.S.; Brosnan, C.F. Deletion of astrocyte connexins 43 and 30 leads to a dysmyelinating phenotype and hippocampal CA1 vacuolation. J. Neurosci., 2009, 29(24), 7743-7752.
[http://dx.doi.org/10.1523/JNEUROSCI.0341-09.2009] [PMID: 19535586]
[102]
Rajkowska, G.; Stockmeier, C.A. Astrocyte pathology in major depressive disorder: insights from human postmortem brain tissue. Curr. Drug Targets, 2013, 14(11), 1225-1236.
[http://dx.doi.org/10.2174/13894501113149990156] [PMID: 23469922]
[103]
Quesseveur, G.; Portal, B.; Basile, J.A.; Ezan, P.; Mathou, A.; Halley, H.; Leloup, C.; Fioramonti, X.; Déglon, N.; Giaume, C.; Rampon, C.; Guiard, B.P. Attenuated levels of hippocampal connexin 43 and its phosphorylation correlate with antidepressant- and anxiolytic-like activities in mice. Front. Cell. Neurosci., 2015, 9, 490.
[http://dx.doi.org/10.3389/fncel.2015.00490] [PMID: 26733815]
[104]
Sun, J.D.; Liu, Y.; Yuan, Y.H.; Li, J.; Chen, N.H. Gap junction dysfunction in the prefrontal cortex induces depressive-like behaviors in rats. Neuropsychopharmacology, 2012, 37(5), 1305-1320.
[http://dx.doi.org/10.1038/npp.2011.319] [PMID: 22189291]
[105]
Jeanson, T.; Pondaven, A.; Ezan, P.; Mouthon, F.; Charvériat, M.; Giaume, C. Antidepressants impact connexin 43 channel functions in astrocytes. Front. Cell. Neurosci., 2016, 9, 495.
[http://dx.doi.org/10.3389/fncel.2015.00495] [PMID: 26778961]
[106]
Shen, F.; Huang, W.L.; Xing, B.P.; Fang, X.; Feng, M.; Jiang, C.M. Genistein improves the major depression through suppressing the expression of miR-221/222 by targeting connexin 43. Psychiatry Investig., 2018, 15(10), 919-925.
[http://dx.doi.org/10.30773/pi.2018.06.29] [PMID: 30205672]
[107]
Quesseveur, G.; David, D.J.; Gaillard, M.C.; Pla, P.; Wu, M.V.; Nguyen, H.T.; Nicolas, V.; Auregan, G.; David, I.; Dranovsky, A.; Hantraye, P.; Hen, R.; Gardier, A.M.; Déglon, N.; Guiard, B.P. BDNF overexpression in mouse hippocampal astrocytes promotes local neurogenesis and elicits anxiolytic-like activities. Transl. Psychiatry, 2013, 3, e253.
[http://dx.doi.org/10.1038/tp.2013.30] [PMID: 23632457]
[108]
Zafra, F.; Lindholm, D.; Castrén, E.; Hartikka, J.; Thoenen, H. Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes. J. Neurosci., 1992, 12(12), 4793-4799.
[http://dx.doi.org/10.1523/JNEUROSCI.12-12-04793.1992] [PMID: 1281495]
[109]
Jean, Y.Y.; Lercher, L.D.; Dreyfus, C.F. Glutamate elicits release of BDNF from basal forebrain astrocytes in a process dependent on metabotropic receptors and the PLC pathway. Neuron Glia Biol., 2008, 4(1), 35-42.
[http://dx.doi.org/10.1017/S1740925X09000052] [PMID: 19267952]
[110]
Araque, A.; Sanzgiri, R.P.; Parpura, V.; Haydon, P.G. Astrocyte-induced modulation of synaptic transmission. Can. J. Physiol. Pharmacol., 1999, 77(9), 699-706.
[http://dx.doi.org/10.1139/y99-076] [PMID: 10566947]
[111]
Khurgel, M.; Ivy, G.O. Astrocytes in kindling: relevance to epileptogenesis. Epilepsy Res., 1996, 26(1), 163-175.
[http://dx.doi.org/10.1016/S0920-1211(96)00051-4] [PMID: 8985698]
[112]
Elisevich, K.; Rempel, S.A.; Smith, B.J.; Edvardsen, K. Hippocampal connexin 43 expression in human complex partial seizure disorder. Exp. Neurol., 1997, 145(1), 154-164.
[http://dx.doi.org/10.1006/exnr.1997.6467] [PMID: 9184118]
[113]
Collignon, F.; Wetjen, N.M.; Cohen-Gadol, A.A.; Cascino, G.D.; Parisi, J.; Meyer, F.B.; Marsh, W.R.; Roche, P.; Weigand, S.D. Altered expression of connexin subtypes in mesial temporal lobe epilepsy in humans. J. Neurosurg., 2006, 105(1), 77-87.
[http://dx.doi.org/10.3171/jns.2006.105.1.77] [PMID: 16874892]
[114]
Garbelli, R.; Frassoni, C.; Condorelli, D.F.; Salinaro, A.T.; Musso, N.; Medici, V.; Tassi, L.; Bentivoglio, M.; Spreafico, R. Expression of connexin 43 in the human epileptic and drug-resistant cerebral cortex. Neurology, 2011, 76(10), 895-902.
[http://dx.doi.org/10.1212/WNL.0b013e31820f2da6] [PMID: 21383325]
[115]
Kosaka, T.; Deans, M.R.; Paul, D.L.; Kosaka, K. Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. Neuroscience, 2005, 134(3), 757-769.
[http://dx.doi.org/10.1016/j.neuroscience.2005.04.057] [PMID: 15979807]
[116]
Vincze, R.; Péter, M.; Szabó, Z.; Kardos, J.; Héja, L.; Kovács, Z. Connexin 43 Differentially regulates epileptiform activity in models of convulsive and non-convulsive epilepsies. Front. Cell. Neurosci., 2019, 13, 173.
[http://dx.doi.org/10.3389/fncel.2019.00173] [PMID: 31133805]
[117]
Walrave, L.; Pierre, A.; Albertini, G.; Aourz, N.; De Bundel, D.; Van Eeckhaut, A.; Vinken, M.; Giaume, C.; Leybaert, L.; Smolders, I. Inhibition of astroglial connexin43 hemichannels with TAT-Gap19 exerts anticonvulsant effects in rodents. Glia, 2018, 66(8), 1788-1804.
[http://dx.doi.org/10.1002/glia.23341] [PMID: 29683209]
[118]
Fonseca, C.G.; Green, C.R.; Nicholson, L.F. Upregulation in astrocytic connexin 43 gap junction levels may exacerbate generalized seizures in mesial temporal lobe epilepsy. Brain Res., 2002, 929(1), 105-116.
[http://dx.doi.org/10.1016/S0006-8993(01)03289-9] [PMID: 11852037]
[119]
Condorelli, D.F.; Mudò, G.; Trovato-Salinaro, A.; Mirone, M.B.; Amato, G.; Belluardo, N. Connexin-30 mRNA is up-regulated in astrocytes and expressed in apoptotic neuronal cells of rat brain following kainate-induced seizures. Mol. Cell. Neurosci., 2002, 21(1), 94-113.
[http://dx.doi.org/10.1006/mcne.2002.1155] [PMID: 12359154]
[120]
Condorelli, D.F.; Trovato-Salinaro, A.; Mudò, G.; Mirone, M.B.; Belluardo, N. Cellular expression of connexins in the rat brain: neuronal localization, effects of kainate-induced seizures and expression in apoptotic neuronal cells. Eur. J. Neurosci., 2003, 18(7), 1807-1827.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02910.x] [PMID: 14622215]
[121]
Parys, B.; Côté, A.; Gallo, V.; De Koninck, P.; Sík, A. Intercellular calcium signaling between astrocytes and oligodendrocytes via gap junctions in culture. Neuroscience, 2010, 167(4), 1032-1043.
[http://dx.doi.org/10.1016/j.neuroscience.2010.03.004] [PMID: 20211698]
[122]
Bedner, P.; Dupper, A.; Hüttmann, K.; Müller, J.; Herde, M.K.; Dublin, P.; Deshpande, T.; Schramm, J.; Häussler, U.; Haas, C.A.; Henneberger, C.; Theis, M.; Steinhäuser, C. Astrocyte uncoupling as a cause of human temporal lobe epilepsy. Brain, 2015, 138(Pt 5), 1208-1222.
[http://dx.doi.org/10.1093/brain/awv067] [PMID: 25765328]
[123]
Gigout, S.; Louvel, J.; Rinaldi, D.; Martin, B.; Pumain, R. Thalamocortical relationships and network synchronization in a new genetic model “in mirror” for absence epilepsy. Brain Res., 2013, 1525, 39-52.
[http://dx.doi.org/10.1016/j.brainres.2013.05.044] [PMID: 23743261]
[124]
Chang, W.P.; Wu, J.J.; Shyu, B.C. Thalamic modulation of cingulate seizure activity via the regulation of gap junctions in mice thalamocingulate slice. PLoS One, 2013, 8(5), e62952.
[http://dx.doi.org/10.1371/journal.pone.0062952] [PMID: 23690968]
[125]
Ross, F.M.; Gwyn, P.; Spanswick, D.; Davies, S.N. Carbenoxolone depresses spontaneous epileptiform activity in the CA1 region of rat hippocampal slices. Neuroscience, 2000, 100(4), 789-796.
[http://dx.doi.org/10.1016/S0306-4522(00)00346-8] [PMID: 11036212]
[126]
Uusisaari, M.; Smirnov, S.; Voipio, J.; Kaila, K. Spontaneous epileptiform activity mediated by GABA(A) receptors and gap junctions in the rat hippocampal slice following long-term exposure to GABA(B) antagonists. Neuropharmacology, 2002, 43(4), 563-572.
[http://dx.doi.org/10.1016/S0028-3908(02)00156-9] [PMID: 12367602]
[127]
Gajda, Z.; Szupera, Z.; Blazsó, G.; Szente, M. Quinine, a blocker of neuronal cx36 channels, suppresses seizure activity in rat neocortex in vivo. Epilepsia, 2005, 46(10), 1581-1591.
[http://dx.doi.org/10.1111/j.1528-1167.2005.00254.x] [PMID: 16190928]
[128]
Gajda, Z.; Gyengési, E.; Hermesz, E.; Ali, K.S.; Szente, M. Involvement of gap junctions in the manifestation and control of the duration of seizures in rats in vivo. Epilepsia, 2003, 44(12), 1596-1600.
[http://dx.doi.org/10.1111/j.0013-9580.2003.25803.x] [PMID: 14636335]
[129]
Kim, Y.; Davidson, J.O.; Gunn, K.C.; Phillips, A.R.; Green, C.R.; Gunn, A.J. Role of hemichannels in CNS inflammation and the inflammasome pathway. Adv. Protein Chem. Struct. Biol., 2016, 104, 1-37.
[http://dx.doi.org/10.1016/bs.apcsb.2015.12.001] [PMID: 27038371]
[130]
Hagberg, H.; Mallard, C.; Ferriero, D.M.; Vannucci, S.J.; Levison, S.W.; Vexler, Z.S.; Gressens, P. The role of inflammation in perinatal brain injury. Nat. Rev. Neurol., 2015, 11(4), 192-208.
[http://dx.doi.org/10.1038/nrneurol.2015.13] [PMID: 25686754]
[131]
Liddelow, S.A.; Guttenplan, K.A.; Clarke, L.E.; Bennett, F.C.; Bohlen, C.J.; Schirmer, L.; Bennett, M.L.; Münch, A.E.; Chung, W.S.; Peterson, T.C.; Wilton, D.K.; Frouin, A.; Napier, B.A.; Panicker, N.; Kumar, M.; Buckwalter, M.S.; Rowitch, D.H.; Dawson, V.L.; Dawson, T.M.; Stevens, B.; Barres, B.A. Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 2017, 541(7638), 481-487.
[http://dx.doi.org/10.1038/nature21029] [PMID: 28099414]
[132]
Boulay, A.C.; Gilbert, A.; Oliveira Moreira, V.; Blugeon, C.; Perrin, S.; Pouch, J.; Le Crom, S.; Ducos, B.; Cohen-Salmon, M. Connexin 43 controls the astrocyte immunoregulatory phenotype. Brain Sci., 2018, 8(4), E50.
[http://dx.doi.org/10.3390/brainsci8040050] [PMID: 29565275]
[133]
Broux, B.; Gowing, E.; Prat, A. Glial regulation of the blood-brain barrier in health and disease. Semin. Immunopathol., 2015, 37(6), 577-590.
[http://dx.doi.org/10.1007/s00281-015-0516-2] [PMID: 26245144]
[134]
Zhou, K.Q.; Green, C.R.; Bennet, L.; Gunn, A.J.; Davidson, J.O. The role of connexin and pannexin channels in perinatal brain injury and inflammation. Front. Physiol., 2019, 10, 141.
[http://dx.doi.org/10.3389/fphys.2019.00141] [PMID: 30873043]
[135]
Liao, C.K.; Jeng, C.J.; Wang, H.S.; Wang, S.H.; Wu, J.C. Lipopolysaccharide induces degradation of connexin43 in rat astrocytes via the ubiquitin-proteasome proteolytic pathway. PLoS One, 2013, 8(11), e79350.
[http://dx.doi.org/10.1371/journal.pone.0079350] [PMID: 24236122]
[136]
Chen, Y.; Wang, L.; Zhang, L.; Chen, B.; Yang, L.; Li, X.; Li, Y.; Yu, H. Inhibition of connexin 43 hemichannels alleviates cerebral ischemia/reperfusion injury via the TLR4 signaling pathway. Front. Cell. Neurosci., 2018, 12, 372.
[http://dx.doi.org/10.3389/fncel.2018.00372] [PMID: 30386214]
[137]
Yin, X.; Feng, L.; Ma, D.; Yin, P.; Wang, X.; Hou, S.; Hao, Y.; Zhang, J.; Xin, M.; Feng, J. Roles of astrocytic connexin-43, hemichannels, and gap junctions in oxygen-glucose deprivation/reperfusion injury induced neuroinflammation and the possible regulatory mechanisms of salvianolic acid B and carbenoxolone. J. Neuroinflammation, 2018, 15(1), 97.
[http://dx.doi.org/10.1186/s12974-018-1127-3] [PMID: 29587860]
[138]
Castellano, P.; Eugenin, E.A. Regulation of gap junction channels by infectious agents and inflammation in the CNS. Front. Cell. Neurosci., 2014, 8, 122.
[http://dx.doi.org/10.3389/fncel.2014.00122] [PMID: 24847208]
[139]
Robertson, J.; Lang, S.; Lambert, P.A.; Martin, P.E. Peptidoglycan derived from Staphylococcus epidermidis induces connexin43 hemichannel activity with consequences on the innate immune response in endothelial cells. Biochem. J., 2010, 432(1), 133-143.
[http://dx.doi.org/10.1042/BJ20091753] [PMID: 20815816]
[140]
Froger, N.; Orellana, J.A.; Calvo, C.F.; Amigou, E.; Kozoriz, M.G.; Naus, C.C.; Sáez, J.C.; Giaume, C. Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective. Mol. Cell. Neurosci., 2010, 45(1), 37-46.
[http://dx.doi.org/10.1016/j.mcn.2010.05.007] [PMID: 20684043]
[141]
Ma, Y.; Bu, J.; Dang, H.; Sha, J.; Jing, Y.; Shan-jiang, A.I.; Li, H.; Zhu, Y. Inhibition of adenosine monophosphate-activated protein kinase reduces glial cell-mediated inflammation and induces the expression of Cx43 in astroglias after cerebral ischemia. Brain Res., 2015, 1605, 1-11.
[http://dx.doi.org/10.1016/j.brainres.2014.11.030] [PMID: 25619553]
[142]
Cui, Y.; Masaki, K.; Yamasaki, R.; Imamura, S.; Suzuki, S.O.; Hayashi, S.; Sato, S.; Nagara, Y.; Kawamura, M.F.; Kira, J. Extensive dysregulations of oligodendrocytic and astrocytic connexins are associated with disease progression in an amyotrophic lateral sclerosis mouse model. J. Neuroinflammation, 2014, 11, 42.
[http://dx.doi.org/10.1186/1742-2094-11-42] [PMID: 24597481]
[143]
Díaz-Amarilla, P.; Olivera-Bravo, S.; Trias, E.; Cragnolini, A.; Martínez-Palma, L.; Cassina, P.; Beckman, J.; Barbeito, L. Phenotypically aberrant astrocytes that promote motoneuron damage in a model of inherited amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA, 2011, 108(44), 18126-18131.
[http://dx.doi.org/10.1073/pnas.1110689108] [PMID: 22010221]
[144]
Béhin, A.; Delattre, J.Y. Complications of radiation therapy on the brain and spinal cord. Semin. Neurol., 2004, 24(4), 405-417.
[http://dx.doi.org/10.1055/s-2004-861535] [PMID: 15637652]
[145]
Tang, F.R.; Loganovsky, K. Low dose or low dose rate ionizing radiation-induced health effect in the human. J. Environ. Radioact., 2018, 192, 32-47.
[http://dx.doi.org/10.1016/j.jenvrad.2018.05.018] [PMID: 29883875]
[146]
Tang, F.R.; Loke, W.K.; Khoo, B.C. Low-dose or low-dose-rate ionizing radiation-induced bioeffects in animal models. J. Radiat. Res. (Tokyo), 2017, 58(2), 165-182.
[http://dx.doi.org/10.1093/jrr/rrw120] [PMID: 28077626]
[147]
Yang, B.; Ren, B.X.; Tang, F.R. Prenatal irradiation-induced brain neuropathology and cognitive impairment. Brain Dev., 2017, 39(1), 10-22.
[http://dx.doi.org/10.1016/j.braindev.2016.07.008] [PMID: 27527732]
[148]
Tang, F.R.; Loke, W.K.; Wong, P.; Khoo, B.C. Radioprotective effect of ursolic acid in radiation-induced impairment of neurogenesis, learning and memory in adolescent BALB/c mouse. Physiol. Behav., 2017, 175, 37-46.
[http://dx.doi.org/10.1016/j.physbeh.2017.03.027] [PMID: 28341234]
[149]
Setkowicz, Z.; Gzieło-Jurek, K.; Uram, Ł.; Janicka, D.; Janeczko, K. Brain dysplasia evoked by gamma irradiation at different stages of prenatal development leads to different tonic and clonic seizure reactivity. Epilepsy Res., 2014, 108(1), 66-80.
[http://dx.doi.org/10.1016/j.eplepsyres.2013.10.010] [PMID: 24239322]
[150]
Lowe, X.R.; Bhattacharya, S.; Marchetti, F.; Wyrobek, A.J. Early brain response to low-dose radiation exposure involves molecular networks and pathways associated with cognitive functions, advanced aging and Alzheimer’s disease. Radiat. Res., 2009, 171(1), 53-65.
[http://dx.doi.org/10.1667/RR1389.1] [PMID: 19138050]
[151]
Tang, F.R. Radiation and Alzheimer’s disease. J. Alzheimers Dis. Parkinsonism, 2018, 8(1), 418.
[http://dx.doi.org/10.4172/2161-0460.1000418]
[152]
Sibley, R.F.; Moscato, B.S.; Wilkinson, G.S.; Natarajan, N. Nested case-control study of external ionizing radiation dose and mortality from dementia within a pooled cohort of female nuclear weapons workers. Am. J. Ind. Med., 2003, 44(4), 351-358.
[http://dx.doi.org/10.1002/ajim.10288] [PMID: 14502762]
[153]
Nakane, Y.; Ohta, Y. An example from the Japanese Register: Some long-term consequences of the A-bomb for its survivors in Nagasaki.In: Psychiatric Case Registers in Public Health; Elsevier Science Publishers B.V, 1986, pp. 26-27.
[154]
Shore, D. Schizophrenia: Questions and Answers; U.S. Department of Health and Human Services, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute of Mental Health: Rockville, Md., 1986.
[155]
Nyagu, A.I.; Loganovsky, K.N.; Loganovskaja, T.K. Psychophysiologic aftereffects of prenatal irradiation. Int. J. Psychophysiol., 1998, 30(3), 303-311.
[http://dx.doi.org/10.1016/S0167-8760(98)00022-1] [PMID: 9834886]
[156]
Iwata, Y.; Suzuki, K.; Wakuda, T.; Seki, N.; Thanseem, I.; Matsuzaki, H.; Mamiya, T.; Ueki, T.; Mikawa, S.; Sasaki, T.; Suda, S.; Yamamoto, S.; Tsuchiya, K.J.; Sugihara, G.; Nakamura, K.; Sato, K.; Takei, N.; Hashimoto, K.; Mori, N. Irradiation in adulthood as a new model of schizophrenia. PLoS One, 2008, 3(5), e2283.
[http://dx.doi.org/10.1371/journal.pone.0002283] [PMID: 18509473]
[157]
Torrey, E.F. Prevalence of psychosis among the Hutterites: a reanalysis of the 1950-53 study. Schizophr. Res., 1995, 16(2), 167-170.
[http://dx.doi.org/10.1016/0920-9964(95)00042-K] [PMID: 7577770]
[158]
Loganovsky, K.; Havenaar, J.M.; Tintle, N.L.; Guey, L.T.; Kotov, R.; Bromet, E.J. The mental health of clean-up workers 18 years after the Chernobyl accident. Psychol. Med., 2008, 38(4), 481-488.
[http://dx.doi.org/10.1017/S0033291707002371] [PMID: 18047772]
[159]
Feudell, P. Radiation-induced spinal amyotrophy. Neurologija, 1979, 27(1-4), 103-106.
[PMID: 261995]
[160]
Glenn, S.A.; Ross, M.A. Delayed radiation-induced bulbar palsy mimicking ALS. Muscle Nerve, 2000, 23(5), 814-817.
[http://dx.doi.org/10.1002/(SICI)1097-4598(200005)23: 5<814::AID-MUS22>3.0.CO;2-V] [PMID: 10797408]
[161]
Tang, F.R.; Loke, W.K.; Khoo, B.C. Postnatal irradiation-induced hippocampal neuropathology, cognitive impairment and aging. Brain Dev., 2017, 39(4), 277-293.
[http://dx.doi.org/10.1016/j.braindev.2016.11.001] [PMID: 27876394]
[162]
Hwang, S.Y.; Jung, J.S.; Kim, T.H.; Lim, S.J.; Oh, E.S.; Kim, J.Y.; Ji, K.A.; Joe, E.H.; Cho, K.H.; Han, I.O. Ionizing radiation induces astrocyte gliosis through microglia activation. Neurobiol. Dis., 2006, 21(3), 457-467.
[http://dx.doi.org/10.1016/j.nbd.2005.08.006] [PMID: 16202616]
[163]
Wilson, C.M.; Gaber, M.W.; Sabek, O.M.; Zawaski, J.A.; Merchant, T.E. Radiation-induced astrogliosis and blood-brain barrier damage can be abrogated using anti-TNF treatment. Int. J. Radiat. Oncol. Biol. Phys., 2009, 74(3), 934-941.
[http://dx.doi.org/10.1016/j.ijrobp.2009.02.035] [PMID: 19480972]
[164]
Moravan, M.J.; Olschowka, J.A.; Williams, J.P.; O’Banion, M.K. Cranial irradiation leads to acute and persistent neuroinflammation with delayed increases in T-cell infiltration and CD11c expression in C57BL/6 mouse brain. Radiat. Res., 2011, 176(4), 459-473.
[http://dx.doi.org/10.1667/RR2587.1] [PMID: 21787181]
[165]
Wang, S.W.; Ren, B.X.; Qian, F.; Luo, X.Z.; Tang, X.; Peng, X.C.; Huang, J.R.; Tang, F.R. Radioprotective effect of epimedium on neurogenesis and cognition after acute radiation exposure. Neurosci. Res., 2019, 145, 46-53.
[http://dx.doi.org/10.1016/j.neures.2018.08.011] [PMID: 30145270]
[166]
Peng, S.; Yang, B.; Duan, M.Y.; Liu, Z.W.; Wang, W.F.; Zhang, X.Z.; Ren, B.X.; Tang, F.R. The disparity of impairment of neurogenesis and cognition after acute or fractionated radiation exposure in adolescent BALB/c mice. Dose Response, 2019, 17(1), 1559325818822574.
[http://dx.doi.org/10.1177/1559325818822574] [PMID: 30670940]
[167]
Hellström, N.A.; Björk-Eriksson, T.; Blomgren, K.; Kuhn, H.G. Differential recovery of neural stem cells in the subventricular zone and dentate gyrus after ionizing radiation. Stem Cells, 2009, 27(3), 634-641.
[http://dx.doi.org/10.1634/stemcells.2008-0732] [PMID: 19056908]
[168]
Guo, Y.R.; Liu, Z.W.; Peng, S.; Duan, M.Y.; Feng, J.W.; Wang, W.F.; Xu, Y.H.; Tang, X.; Zhang, X.Z.; Ren, B.X.; Tang, F.R. The neuroprotective effect of amitriptyline on radiation-induced impairment of hippocampal neurogenesis. Dose Response, 2019, 17(4), 1559325819895912.
[http://dx.doi.org/10.1177/1559325819895912] [PMID: 31903069]
[169]
Peiffer, A.M.; Creer, R.M.; Linville, C.; Olson, J.; Kulkarni, P.; Brown, J.A.; Riddle, D.R.; Robbins, M.E.; Brunso-Bechtold, J.E. Radiation-induced cognitive impairment and altered diffusion tensor imaging in a juvenile rat model of cranial radiotherapy. Int. J. Radiat. Biol., 2014, 90(9), 799-806.
[http://dx.doi.org/10.3109/09553002.2014.938278] [PMID: 24991879]
[170]
Piao, J.; Major, T.; Auyeung, G.; Policarpio, E.; Menon, J.; Droms, L.; Gutin, P.; Uryu, K.; Tchieu, J.; Soulet, D.; Tabar, V. Human embryonic stem cell-derived oligodendrocyte progenitors remyelinate the brain and rescue behavioral deficits following radiation. Cell Stem Cell, 2015, 16(2), 198-210.
[http://dx.doi.org/10.1016/j.stem.2015.01.004] [PMID: 25658373]
[171]
Brown, W.R.; Blair, R.M.; Moody, D.M.; Thore, C.R.; Ahmed, S.; Robbins, M.E.; Wheeler, K.T. Capillary loss precedes the cognitive impairment induced by fractionated whole-brain irradiation: a potential rat model of vascular dementia. J. Neurol. Sci., 2007, 257(1-2), 67-71.
[http://dx.doi.org/10.1016/j.jns.2007.01.014] [PMID: 17316691]
[172]
Ljubimova, N.V.; Levitman, M.K.; Plotnikova, E.D.; Eidus, L.Kh. Endothelial cell population dynamics in rat brain after local irradiation. Br. J. Radiol., 1991, 64(766), 934-940.
[http://dx.doi.org/10.1259/0007-1285-64-766-934] [PMID: 1954536]
[173]
Fukuda, H.; Fukuda, A.; Zhu, C.; Korhonen, L.; Swanpalmer, J.; Hertzman, S.; Leist, M.; Lannering, B.; Lindholm, D.; Björk-Eriksson, T.; Marky, I.; Blomgren, K. Irradiation-induced progenitor cell death in the developing brain is resistant to erythropoietin treatment and caspase inhibition. Cell Death Differ., 2004, 11(11), 1166-1178.
[http://dx.doi.org/10.1038/sj.cdd.4401472] [PMID: 15243583]
[174]
Zhu, C.; Xu, F.; Fukuda, A.; Wang, X.; Fukuda, H.; Korhonen, L.; Hagberg, H.; Lannering, B.; Nilsson, M.; Eriksson, P.S.; Northington, F.J.; Björk-Eriksson, T.; Lindholm, D.; Blomgren, K. X chromosome-linked inhibitor of apoptosis protein reduces oxidative stress after cerebral irradiation or hypoxia-ischemia through up-regulation of mitochondrial antioxidants. Eur. J. Neurosci., 2007, 26(12), 3402-3410.
[http://dx.doi.org/10.1111/j.1460-9568.2007.05948.x] [PMID: 18052985]
[175]
Wang, H.; Sethi, G.; Loke, W.K.; Sim, M.K.; Des-Aspartate-Angiotensin, I. Des-aspartate-angiotensin I attenuates mortality of mice exposed to gamma radiation via a novel mechanism of action. PLoS One, 2015, 10(9), e0138009.
[http://dx.doi.org/10.1371/journal.pone.0138009] [PMID: 26378927]
[176]
Wang, H.; Sim, M.K.; Loke, W.K.; Chinnathambi, A.; Alharbi, S.A.; Tang, F.R.; Sethi, G. Potential protective effects of ursolic acid against gamma irradiation-induced damage are mediated through the modulation of diverse inflammatory mediators. Front. Pharmacol., 2017, 8, 352.
[http://dx.doi.org/10.3389/fphar.2017.00352] [PMID: 28670276]
[177]
Ramachandran, S.; Xie, L.H.; John, S.A.; Subramaniam, S.; Lal, R. A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury. PLoS One, 2007, 2(8), e712.
[http://dx.doi.org/10.1371/journal.pone.0000712] [PMID: 17684558]
[178]
Li, J.; Meng, Z.; Zhang, G.; Xing, Y.; Feng, L.; Fan, S.; Fan, F.; Buren, B.; Liu, Q. N-acetylcysteine relieves oxidative stress and protects hippocampus of rat from radiation-induced apoptosis by inhibiting caspase-3. Biomed. Pharmacother., 2015, 70, 1-6.
[http://dx.doi.org/10.1016/j.biopha.2014.12.029] [PMID: 25776470]
[179]
Leavitt, R.J.; Limoli, C.L.; Baulch, J.E. miRNA-based therapeutic potential of stem cell-derived extracellular vesicles: a safe cell-free treatment to ameliorate radiation-induced brain injury. Int. J. Radiat. Biol., 2019, 95(4), 427-435.
[http://dx.doi.org/10.1080/09553002.2018.1522012] [PMID: 30252569]
[180]
Pogribny, I.; Koturbash, I.; Tryndyak, V.; Hudson, D.; Stevenson, S.M.; Sedelnikova, O.; Bonner, W.; Kovalchuk, O. Fractionated low-dose radiation exposure leads to accumulation of DNA damage and profound alterations in DNA and histone methylation in the murine thymus. Mol. Cancer Res., 2005, 3(10), 553-561.
[http://dx.doi.org/10.1158/1541-7786.MCR-05-0074] [PMID: 16254189]
[181]
Koturbash, I.; Zemp, F.; Kolb, B.; Kovalchuk, O. Sex-specific radiation-induced microRNAome responses in the hippocampus, cerebellum and frontal cortex in a mouse model. Mutat. Res., 2011, 722(2), 114-118.
[http://dx.doi.org/10.1016/j.mrgentox.2010.05.007] [PMID: 20478395]
[182]
Wang, Y.; Zhou, K.; Li, T.; Xu, Y.; Xie, C.; Sun, Y.; Zhang, Y.; Rodriguez, J.; Blomgren, K.; Zhu, C. Inhibition of autophagy prevents irradiation-induced neural stem and progenitor cell death in the juvenile mouse brain. Cell Death Dis., 2017, 8(3), e2694.
[http://dx.doi.org/10.1038/cddis.2017.120] [PMID: 28333139]
[183]
Lu, Y.; He, M.; Zhang, Y.; Xu, S.; Zhang, L.; He, Y.; Chen, C.; Liu, C.; Pi, H.; Yu, Z.; Zhou, Z. Differential pro-inflammatory responses of astrocytes and microglia involve STAT3 activation in response to 1800 MHz radiofrequency fields. PLoS One, 2014, 9(9), e108318.
[http://dx.doi.org/10.1371/journal.pone.0108318] [PMID: 25275372]
[184]
Schneider, L.; Pellegatta, S.; Favaro, R.; Pisati, F.; Roncaglia, P.; Testa, G.; Nicolis, S.K.; Finocchiaro, G.; d’Adda di Fagagna, F. DNA damage in mammalian neural stem cells leads to astrocytic differentiation mediated by BMP2 signaling through JAK-STAT. Stem Cell Reports, 2013, 1(2), 123-138.
[http://dx.doi.org/10.1016/j.stemcr.2013.06.004] [PMID: 24052948]
[185]
Ramadan, R.; Vromans, E.; Anang, D.C.; Decrock, E.; Mysara, M.; Monsieurs, P.; Baatout, S.; Leybaert, L.; Aerts, A. Single and fractionated ionizing radiation induce alterations in endothelial connexin expression and channel function. Sci. Rep., 2019, 9(1), 4643.
[http://dx.doi.org/10.1038/s41598-019-39317-9] [PMID: 31217426]
[186]
Chen, W.; Tong, W.; Guo, Y.; He, B.; Chen, L.; Yang, W.; Wu, C.; Ren, D.; Zheng, P.; Feng, J. Upregulation of connexin-43 is critical for irradiation-induced neuroinflammation. CNS Neurol. Disord. Drug Targets, 2018, 17(7), 539-546.
[http://dx.doi.org/10.2174/1871527317666180706124602] [PMID: 29984671]
[187]
Viczenczova, C.; Kura, B.; Benova, T.E.; Yin, C.; Kukreja, R.C.; Slezak, J.; Tribulova, N.; Bacova, B.S. Irradiation-induced cardiac connexin-43 and miR-21 responses are hampered by treatment with atorvastatin and aspirin. Int. J. Mol. Sci., 2018, 19(4), E1128.
[http://dx.doi.org/10.3390/ijms19041128] [PMID: 29642568]
[188]
de Toledo, S.M.; Buonanno, M.; Harris, A.L.; Azzam, E.I. Genomic instability induced in distant progeny of bystander cells depends on the connexins expressed in the irradiated cells. Int. J. Radiat. Biol., 2017, 93(10), 1182-1194.
[http://dx.doi.org/10.1080/09553002.2017.1334980] [PMID: 28565963]
[189]
Glover, D.; Little, J.B.; Lavin, M.F.; Gueven, N. Low dose ionizing radiation-induced activation of connexin 43 expression. Int. J. Radiat. Biol., 2003, 79(12), 955-964.
[http://dx.doi.org/10.1080/09553000310001632895] [PMID: 14713573]
[190]
Marples, B.; Scott, S.D.; Hendry, J.H.; Embleton, M.J.; Lashford, L.S.; Margison, G.P. Development of synthetic promoters for radiation-mediated gene therapy. Gene Ther., 2000, 7(6), 511-517.
[http://dx.doi.org/10.1038/sj.gt.3301116] [PMID: 10757025]
[191]
Ramadan, R.; Vromans, E.; Anang, D.C.; Goetschalckx, I.; Hoorelbeke, D.; Decrock, E.; Baatout, S.; Leybaert, L.; Aerts, A. Connexin43 hemichannel targeting with TAT-Gap19 alleviates radiation-induced endothelial cell damage. Front. Pharmacol., 2020, 11, 212.
[http://dx.doi.org/10.3389/fphar.2020.00212] [PMID: 32210810]
[192]
Hoorelbeke, D.; Decrock, E.; De Smet, M.; De Bock, M.; Descamps, B.; Van Haver, V.; Delvaeye, T.; Krysko, D.V.; Vanhove, C.; Bultynck, G.; Leybaert, L. Cx43 channels and signaling via IP3/Ca2+, ATP, and ROS/NO propagate radiation-induced DNA damage to non-irradiated brain microvascular endothelial cells. Cell Death Dis., 2020, 11(3), 194.
[http://dx.doi.org/10.1038/s41419-020-2392-5] [PMID: 32188841]

Rights & Permissions Print Cite
Article Metrics
205
2
World Chagas Disease
© 2024 Bentham Science Publishers | Privacy Policy