Contribution of 25-hydroxycholesterol to the cross-interaction of the immune and nervous systems

Abstract

25-hydroxycholesterol (25HC) is produced from cholesterol by cholesterol-25-hydroxylase, and its expression, similar to the 25HC level, increases significantly in macrophages, dendritic cells, and microglia during an inflammatory reaction. In turn, 25HC acts on many immune cells; therefore, it can modulate the course of the inflammatory reaction and prevent the penetration of viruses into cells. Data are accumulating about the involvement of 25HC in the regulation of synaptic transmission in both the central and peripheral nervous systems. 25HC production is increased not only during inflammation but in certain neurodegenerative diseases, such as Alzheimer’s disease and amyotrophic lateral sclerosis; thus, this hydroxycholesterol can be important in the adaptation of synaptic activity to inflammatory conditions, pathogenesis of neurodegenerative diseases, and formation of synaptic dysfunctions. The targets of 25HC in the nervous system are glutamate NMDA receptors, liver X-receptors, and estrogen receptors. 25HC can also directly influence the properties of synaptic membranes by changing the formation of membrane microdomains (lipid rafts) where proteins, which are important for synaptic plasticity, are clustered. Current data indicate that the effects of 25HC strongly depend on its concentration and “context” (norm, pathology, and presence of an inflammatory reaction) in which the effect of 25HC is being investigated. This minireview focused on the key aspects of the action of 25HC as both a local regulator of cholesterol homeostasis and a paracrine molecule that realizes the influence of inflammation on neurotransmission processes in the central and peripheral nervous systems.

Keywords

synaptic transmission / 25-hydroxycholesterol / skeletal muscle / vesicle / lipid rafts / neurotransmitter

References

[1] Lipowsky R, Sackmsnn E, editors. Structure and dynamics of membranes. 1st ed. Elsevier; 1995. 1052 p.

[2] Lipowsky R., Sackmsnn E., editors. Structure and dynamics of membranes. 1st ed. Elsevier, 1995. 1052 p.

[3] Ma L, Nelson ER. Oxysterols and nuclear receptors. Mol Cell Endocrinol. 2019;484:42–51. doi: 10.1016/j.mce.2019.01.016

[4] Ma L., Nelson E.R. Oxysterols and nuclear receptors // Mol Cell Endocrinol. 2019. Vol. 484. P. 42–51. doi: 10.1016/j.mce.2019.01.016

[5] Olivier E, Dutot M, Regazzetti A, et al. P2X7-pannexin-1 and amyloid β-induced oxysterol input in human retinal cell: role in age-related macular degeneration? Biochimie. 2016;127:70–78. doi: 10.1016/j.biochi.2016.04.014

[6] Olivier E., Dutot M., Regazzetti A., et al. P2X7-pannexin-1 and amyloid β-induced oxysterol input in human retinal cell: Role in age-related macular degeneration? // Biochimie. 2016. Vol. 127. P. 70–78. doi: 10.1016/j.biochi.2016.04.014

[7] Bezine M, Namsi A, Sghaier R, et al. The effect of oxysterols on nerve impulses. Biochimie. 2018;153:46–51. doi: 10.1016/j.biochi.2018.04.013

[8] Bezine M., Namsi A., Sghaier R., et al. The effect of oxysterols on nerve impulses // Biochimie. 2018. Vol. 153. P. 46–51. doi: 10.1016/j.biochi.2018.04.013

[9] Gargiulo S, Gamba P, Testa G, et al. Molecular signaling involved in oxysterol-induced β₁-integrin over-expression in human macrophages. Int J Mol Sci. 2012;13(11):14278–14293. doi: 10.3390/ijms131114278

[10] Gargiulo S., Gamba P., Testa G., et al. Molecular signaling involved in oxysterol-induced β₁-integrin over-expression in human macrophages // Int J Mol Sci. 2012. Vol. 13, N 11. P. 14278–14293. doi: 10.3390/ijms131114278

[11] Yan D, Mäyränpää MI, Wong J, et al. OSBP-related protein 8 (ORP8) suppresses ABCA1 expression and cholesterol efflux from macrophages. J Biol Chem. 2008;283(1):332–340. doi: 10.1074/jbc.M705313200

[12] Yan D., Mäyränpää M.I., Wong J., et al. OSBP-related protein 8 (ORP8) suppresses ABCA1 expression and cholesterol efflux from macrophages // J Biol Chem. 2008. Vol. 283, N 1. P. 332–340. doi: 10.1074/jbc.M705313200

[13] Kasimov MR, Fatkhrakhmanova MR, Mukhutdinova KA, Petrov AM. 24S-hydroxycholesterol enhances synaptic vesicle cycling in the mouse neuromuscular junction: implication of glutamate NMDA receptors and nitric oxide. Neuropharmacology. 2017;117:61–73. doi: 10.1016/j.neuropharm.2017.01.030

[14] Kasimov M.R., Fatkhrakhmanova M.R., Mukhutdinova K.A., Petrov A.M. 24S-hydroxycholesterol enhances synaptic vesicle cycling in the mouse neuromuscular junction: Implication of glutamate NMDA receptors and nitric oxide // Neuropharmacology. 2017. Vol. 117. P. 61–73. doi: 10.1016/j.neuropharm.2017.01.030

[15] Mukhutdinova KA, Kasimov MR, Giniatullin AR, et al. 24S-hydroxycholesterol suppresses neuromuscular transmission in SOD1(G93A) mice: a possible role of NO and lipid rafts. Mol Cell Neurosci. 2018;88:308–318. doi: 10.1016/j.mcn.2018.03.006

[16] Mukhutdinova K.A., Kasimov M.R., Giniatullin A.R., et al. 24S-hydroxycholesterol suppresses neuromuscular transmission in SOD1(G93A) mice: a possible role of NO and lipid rafts // Mol Cell Neurosci. 2018. Vol. 88. P. 308–318. doi: 10.1016/j.mcn.2018.03.006

[17] Mukhutdinova KA, Kasimov MR, Zakyrjanova GF, et al. Oxysterol modulates neurotransmission via liver-X receptor/NO synthase-dependent pathway at the mouse neuromuscular junctions. Neuropharmacology. 2019;150:70–79. doi: 10.1016/j.neuropharm.2019.03.018

[18] Mukhutdinova K.A., Kasimov M.R., Zakyrjanova G.F., et al. Oxysterol modulates neurotransmission via liver-X receptor/NO synthase-dependent pathway at the mouse neuromuscular junctions // Neuropharmacology. 2019. Vol. 150. P. 70–79. doi: 10.1016/j.neuropharm.2019.03.018

[19] Petrov AM, Pikuleva IA. Cholesterol 24-hydroxylation by CYP46A1: benefits of modulation for brain diseases. Neurotherapeutics. 2019;16(3):635–648. doi: 10.1007/s13311-019-00731-6

[20] Petrov A.M., Pikuleva I.A. Cholesterol 24-hydroxylation by CYP46A1: benefits of modulation for brain diseases // Neurotherapeutics. 2019. Vol. 16, N 3. P. 635–648. doi: 10.1007/s13311-019-00731-6

[21] Lütjohann D, Breuer O, Ahlborg G, et al. Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation. Proc Natl Acad Sci U S A. 1996;93(18):9799–9804. doi: 10.1073/pnas.93.18.9799

[22] Lütjohann D., Breuer O., Ahlborg G., et al. Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation // Proc Natl Acad Sci U S A. 1996. Vol. 93, N 18. P. 9799–9804. doi: 10.1073/pnas.93.18.9799

[23] Meaney S, Bodin K, Diczfalusy U, Björkhem I. On the rate of translocation in vitro and kinetics in vivo of the major oxysterols in human circulation: critical importance of the position of the oxygen function. J Lipid Res. 2002;43(12):2130–2135. doi: 10.1194/jlr.m200293-jlr200

[24] Meaney S., Bodin K., Diczfalusy U., Björkhem I. On the rate of translocation in vitro and kinetics in vivo of the major oxysterols in human circulation: critical importance of the position of the oxygen function // J Lipid Res. 2002. Vol. 43, N 12. P. 2130–2135. doi: 10.1194/jlr.M200293-JLR200

[25] Lund EG, Xie C, Kotti T, et al. Knockout of the cholesterol 24-hydroxylase gene in mice reveals a brain-specific mechanism of cholesterol turnover. J Biol Chem. 2003;278(25):22980–22988. doi: 10.1074/jbc.M303415200

[26] Lund E.G., Xie C., Kotti T., et al. Knockout of the cholesterol 24-hydroxylase gene in mice reveals a brain-specific mechanism of cholesterol turnover // J Biol Chem. 2003. Vol. 278, N 25. P. 22980–22988. doi: 10.1074/jbc.M303415200

[27] Björkhem I, Lütjohann D, Diczfalusy U, et al. Cholesterol homeostasis in human brain: turnover of 24S-hydroxycholesterol and evidence for a cerebral origin of most of this oxysterol in the circulation. J Lipid Res. 1998;39(8):1594–1600.

[28] Björkhem I., Lütjohann D., Diczfalusy U., et al. Cholesterol homeostasis in human brain: turnover of 24S-hydroxycholesterol and evidence for a cerebral origin of most of this oxysterol in the circulation // J Lipid Res. 1998. Vol. 39, N 8. P. 1594–1600.

[29] Blanc M, Hsieh WY, Robertson KA, et al. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response. Immunity. 2013;38(1):106–118. doi: 10.1016/j.immuni.2012.11.004

[30] Blanc M., Hsieh W.Y., Robertson K.A., et al. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response // Immunity. 2013. Vol. 38, N 1. P. 106–118. doi: 10.1016/j.immuni.2012.11.004

[31] Liu Y, Wei Z, Ma X, et al. 25-hydroxycholesterol activates the expression of cholesterol 25-hydroxylase in an LXR-dependent mechanism. J Lipid Res. 2018;59(3):439–451. doi: 10.1194/jlr.M080440

[32] Liu Y., Wei Z., Ma X., et al. 25-Hydroxycholesterol activates the expression of cholesterol 25-hydroxylase in an LXR-dependent mechanism // J Lipid Res. 2018. Vol. 59, N 3. P. 439–451. doi: 10.1194/jlr.M080440

[33] Bauman DR, Bitmansour AD, McDonald JG, et al. 25-hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production. Proc Natl Acad Sci U S A. 2009;106(39):16764–16769. doi: 10.1073/pnas.0909142106

[34] Bauman D.R., Bitmansour A.D., McDonald J.G., et al. 25-hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production // Proc Natl Acad Sci U S A. 2009. Vol. 106, N 39. P. 16764–16769. doi: 10.1073/pnas.0909142106

[35] Karuna R, Christen I, Sailer AW, et al. Detection of dihydroxycholesterols in human plasma using HPLC-ESI-MS/MS. Steroids. 2015;99(Pt B):131–138. doi: 10.1016/j.steroids.2015.02.002

[36] Karuna R., Christen I., Sailer A.W., et al. Detection of dihydroxycholesterols in human plasma using HPLC-ESI-MS/MS // Steroids. 2015. Vol. 99(Pt B). P. 131–138. doi: 10.1016/j.steroids.2015.02.002

[37] Lehmann JM, Kliewer SA, Moore LB, et al. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem. 1997;272(6):3137–3140. doi: 10.1074/jbc.272.6.3137

[38] Lehmann J.M., Kliewer S.A., Moore L.B., et al. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway // J Biol Chem. 1997. Vol. 272, N 6. P. 3137–3140. doi: 10.1074/jbc.272.6.3137

[39] Zhu R, Ou Z, Ruan X, Gong J. Role of liver X receptors in cholesterol efflux and inflammatory signaling (review). Mol Med Rep. 2012;5(4):895–900. doi: 10.3892/mmr.2012.758

[40] Zhu R., Ou Z., Ruan X., Gong J. Role of liver X receptors in cholesterol efflux and inflammatory signaling (review) // Mol Med Rep. 2012. Vol. 5, N 4. P. 895–900. doi: 10.3892/mmr.2012.758

[41] Ouyang S, Mo Z, Sun S, et al. Emerging role of Insig-1 in lipid metabolism and lipid disorders. Clin Chim Acta. 2020;508:206–212. doi: 10.1016/j.cca.2020.05.042

[42] Ouyang S., Mo Z., Sun S., et al. Emerging role of Insig-1 in lipid metabolism and lipid disorders // Clin Chim Acta. 2020. Vol. 508. P. 206–212. doi: 10.1016/j.cca.2020.05.042

[43] Radhakrishnan A, Ikeda Y, Kwon HJ, et al. Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: oxysterols block transport by binding to INSIG. Proc Natl Acad Sci U S A. 2007;104(16):6511–6518. doi: 10.1073/pnas.0700899104

[44] Radhakrishnan A., Ikeda Y., Kwon H.J., et al. Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: oxysterols block transport by binding to INSIG // Proc Natl Acad Sci U S A. 2007. Vol. 104, N 16. P. 6511–6518. doi: 10.1073/pnas.0700899104

[45] Sever N, Yang T, Brown MS, et al. Accelerated degradation of HMG CoA reductase mediated by binding of INSIG-1 to its sterol-sensing domain. Mol Cell. 2003;11(1):25–33. doi: 10.1016/s1097-2765(02)00822-5

[46] Sever N., Yang T., Brown M.S., et al. Accelerated degradation of HMG CoA reductase mediated by binding of INSIG-1 to its sterol-sensing domain // Mol Cell. 2003. Vol. 11, N 1. P. 25–33. doi: 10.1016/S1097-2765(02)00822-5

[47] Morens DM, Fauci AS. The 1918 influenza pandemic: insights for the 21st century. J Infect Dis. 2007;195(7):1018–1028. doi: 10.1086/511989

[48] Morens D.M., Fauci A.S. The 1918 influenza pandemic: insights for the 21st century // J Infect Dis. 2007. Vol. 195, N 7. P. 1018–1028. doi: 10.1086/511989

[49] Kobasa D, Jones SM, Shinya K, et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature. 2007;445(7125):319–323. doi: 10.1038/nature05495

[50] Kobasa D., Jones S.M., Shinya K., et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus // Nature. 2007. Vol. 445, N 7125. P. 319–323. doi: 10.1038/nature05495

[51] Joseph SB, Bradley MN, Castrillo A, et al. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell. 2004;119(2):299–309. doi: 10.1016/j.cell.2004.09.032

[52] Joseph S.B., Bradley M.N., Castrillo A., et al. LXR-dependent gene expression is important for macrophage survival and the innate immune response // Cell. 2004. Vol. 119, N 2. P. 299–309. doi: 10.1016/j.cell.2004.09.032

[53] Reboldi A, Dang EV, McDonald JG, et al. Inflammation. 25-hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon. Science. 2014;345(6197):679–684. doi: 10.1126/science.1254790

[54] Reboldi A., Dang E.V., McDonald J.G., et al. Inflammation. 25-hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon // Science. 2014. Vol. 345, N 6197. P. 679–684. doi: 10.1126/science.1254790

[55] Liu SY, Aliyari R, Chikere K, et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol. Immunity. 2013;38(1):92–105. doi: 10.1016/j.immuni.2012.11.005

[56] Liu S.Y., Aliyari R., Chikere K., et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol // Immunity. 2013. Vol. 38, N 1. P. 92–105. doi: 10.1016/j.immuni.2012.11.005

[57] Liu Y, Wei Z, Zhang Y, et al. Activation of liver X receptor plays a central role in antiviral actions of 25-hydroxycholesterol. J Lipid Res. 2018;59(12):2287–2296. doi: 10.1194/jlr.M084558

[58] Liu Y., Wei Z., Zhang Y., et al. Activation of liver X receptor plays a central role in antiviral actions of 25-hydroxycholesterol // J Lipid Res. 2018. Vol. 59, N 12. P. 2287–2296. doi: 10.1194/jlr.M084558

[59] Yuan Y, Wang Z, Tian B, et al. Cholesterol 25-hydroxylase suppresses rabies virus infection by inhibiting viral entry. Arch Virol. 2019;164(12):2963–2974. doi: 10.1007/s00705-019-04415-6

[60] Yuan Y., Wang Z., Tian B., et al. Cholesterol 25-hydroxylase suppresses rabies virus infection by inhibiting viral entry // Arch Virol. 2019. Vol. 164, N 12. P. 2963–2974. doi: 10.1007/s00705-019-04415-6

[61] Wong MY, Lewis M, Doherty JJ, et al. 25-hydroxycholesterol amplifies microglial IL-1β production in an apoE isoform-dependent manner. J Neuroinflammation. 2020;17(1):192. doi: 10.1186/s12974-020-01869-3

[62] Wong M.Y., Lewis M., Doherty J.J., et al. 25-hydroxycholesterol amplifies microglial IL-1β production in an apoE isoform-dependent manner // J Neuroinflammation. 2020. Vol. 17, N 1. P. 192. doi: 10.1186/s12974-020-01869-3

[63] Izumi Y, Cashikar AG, Krishnan K, et al. A proinflammatory stimulus disrupts hippocampal plasticity and learning via microglial activation and 25-hydroxycholesterol. J Neurosci. 2021;41(49):10054–10064. doi: 10.1523/JNEUROSCI.1502-21.2021

[64] Izumi Y., Cashikar A.G., K., et al. A proinflammatory stimulus disrupts hippocampal plasticity and learning via microglial activation and 25-hydroxycholesterol // J Neurosci. 2021. Vol. 41, N 49. P. 10054–10064. doi: 10.1523/JNEUROSCI.1502-21.2021

[65] Linsenbardt AJ, Taylor A, Emnett CM, et al. Different oxysterols have opposing actions at N-methyl-D-aspartate receptors. Neuropharmacology. 2014;85:232–242. doi: 10.1016/j.neuropharm.2014.05.027

[66] Linsenbardt A.J., Taylor A., Emnett C.M., et al. Different oxysterols have opposing actions at N-methyl-D-aspartate receptors // Neuropharmacology. 2014. Vol. 85. P. 232–242. doi: 10.1016/j.neuropharm.2014.05.027

[67] Ishikawa T, Yuhanna IS, Umetani J, et al. LXRβ/estrogen receptor-α signaling in lipid rafts preserves endothelial integrity. J Clin Invest. 2013;123(8):3488–3497. doi: 10.1172/JCI66533

[68] Ishikawa T., Yuhanna I.S., Umetani J., et al. LXRβ/estrogen receptor-α signaling in lipid rafts preserves endothelial integrity // J Clin Invest. 2013. Vol. 123, N 8. P. 3488–3497. doi: 10.1172/JCI66533

[69] Clements L, Harvey J. Activation of oestrogen receptor α induces a novel form of LTP at hippocampal temporoammonic-CA1 synapses. Br J Pharmacol. 2020;177(3):642–655. doi: 10.1111/bph.14880

[70] Clements L., Harvey J. Activation of oestrogen receptor α induces a novel form of LTP at hippocampal temporoammonic-CA1 synapses // Br J Pharmacol. 2020. Vol. 177, N 3. P. 642–655. doi: 10.1111/bph.14880

[71] Zakyrjanova GF, Tsentsevitsky AN, Kuznetsova EA, Petrov AM. Immune-related oxysterol modulates neuromuscular transmission via non-genomic liver X receptor-dependent mechanism. Free Radic Biol Med. 2021;174:121–134. doi: 10.1016/j.freeradbiomed.2021.08.013

[72] Zakyrjanova G.F., Tsentsevitsky A.N., Kuznetsova E.A., Petrov A.M. Immune-related oxysterol modulates neuromuscular transmission via non-genomic liver X receptor-dependent mechanism // Free Radic Biol Med. 2021. Vol. 174. P. 121–134. doi: 10.1016/j.freeradbiomed.2021.08.013

[73] Unsworth AJ, Flora GD, Gibbins JM. Non-genomic effects of nuclear receptors: insights from the anucleate platelet. Cardiovasc Res. 2018;114(5):645–655. doi: 10.1093/cvr/cvy044

[74] Unsworth A.J., Flora G.D., Gibbins J.M. Non-genomic effects of nuclear receptors: insights from the anucleate platelet // Cardiovasc Res. 2018. Vol. 114, N 5. P. 645–655. doi: 10.1093/cvr/cvy044

[75] Bigini P, Steffensen KR, Ferrario A, et al. Neuropathologic and biochemical changes during disease progression in liver X receptor beta–/– mice, a model of adult neuron disease. J Neuropathol Exp Neurol. 2010;69(6):593–605. doi: 10.1097/NEN.0b013e3181df20e1

[76] Bigini P., Steffensen K.R., Ferrario A., et al. Neuropathologic and biochemical changes during disease progression in liver X receptor beta–/– mice, a model of adult neuron disease // J Neuropathol Exp Neurol. 2010. Vol. 69, N 6. P. 593–605. doi: 10.1097/NEN.0b013e3181df20e1

[77] Hichor M, Sundaram VK, Eid SA, et al. Liver X receptor exerts a protective effect against the oxidative stress in the peripheral nerve. Sci Rep. 2018;8(1):2524. doi: 10.1038/s41598-018-20980-3

[78] Hichor M., Sundaram V.K., Eid S.A., et al. Liver X receptor exerts a protective effect against the oxidative stress in the peripheral nerve // Sci Rep. 2018. Vol. 8, N 1. P. 2524. doi: 10.1038/s41598-018-20980-3

[79] Zhong W, Pan G, Wang L, et al. ORP4L facilitates macrophage survival via G-protein-coupled signaling: ORP4L–/– mice display a reduction of atherosclerosis. Circ Res. 2016;119(12):1296–1312. doi: 10.1161/CIRCRESAHA.116.309603

[80] Zhong W., Pan G., Wang L., et al. ORP4L facilitates macrophage survival via G-protein-coupled signaling: ORP4L–/– mice display a reduction of atherosclerosis // Circ Res. 2016. Vol. 119, N 12. P. 1296–1312. doi: 10.1161/CIRCRESAHA.116.309603

[81] Jin YH, Wu XS, Shi B, et al. Protein kinase C and calmodulin serve as calcium sensors for calcium-stimulated endocytosis at synapses. J Neurosci. 2019;39(48):9478–9490. doi: 10.1523/JNEUROSCI.0182-19.2019

[82] Jin Y.H., Wu X.S., Shi B., et al. Protein kinase c and calmodulin serve as calcium sensors for calcium-stimulated endocytosis at synapses // J Neurosci. 2019. Vol. 39, N 48. P. 9478–9490. doi: 10.1523/JNEUROSCI.0182-19.2019

[83] Kumar P, Wu Q, Chambliss KL, et al. Direct interactions with G α i and G βγ mediate nongenomic signaling by estrogen receptor α. Mol Endocrinol. 2007;21(6):1370–1380. doi: 10.1210/me.2006-0360

[84] Kumar P., Wu Q., Chambliss K.L., et al. Direct interactions with G α i and G βγ mediate nongenomic signaling by estrogen receptor α // Mol Endocrinol. 2007. Vol. 21, N 6. P. 1370–1380. doi: 10.1210/me.2006-0360

[85] Görlach A, Bertram K, Hudecova S, Krizanova O. Calcium and ROS: a mutual interplay. Redox Biol. 2015;6:260–271. doi: 10.1016/j.redox.2015.08.010

[86] Görlach A., Bertram K., Hudecova S., Krizanova O. Calcium and ROS: a mutual interplay // Redox Biol. 2015. Vol. 6. P. 260–271. doi: 10.1016/j.redox.2015.08.010

[87] Giniatullin AR, Giniatullin RA. Dual action of hydrogen peroxide on synaptic transmission at the frog neuromuscular junction. J Physiol. 2003;552(Pt 1):283–293. doi: 10.1113/jphysiol.2003.050690

[88] Giniatullin A.R., Giniatullin R.A. Dual action of hydrogen peroxide on synaptic transmission at the frog neuromuscular junction // J Physiol. 2003. Vol. 552(Pt 1). P. 283–293. doi: 10.1113/jphysiol.2003.050690

[89] Cosentino-Gomes D, Rocco-Machado N, Meyer-Fernandes JR. Cell signaling through protein kinase C oxidation and activation. Int J Mol Sci. 2012;13(9):10697–10721. doi: 10.3390/ijms130910697

[90] Cosentino-Gomes D., Rocco-Machado N., Meyer-Fernandes J.R. Cell signaling through protein kinase C oxidation and activation // Int J Mol Sci. 2012. Vol. 13, N 9. P. 10697–10721. doi: 10.3390/ijms130910697

[91] Ursan R, Odnoshivkina UG, Petrov AM. Membrane cholesterol oxidation downregulates atrial β-adrenergic responses in ROS-dependent manner. Cell Signal. 2020;67:109503. doi: 10.1016/j.cellsig.2019.109503

[92] Ursan R., Odnoshivkina U.G., Petrov A.M. Membrane cholesterol oxidation downregulates atrial β-adrenergic responses in ROS-dependent manner // Cell Signal. 2020. Vol. 67. P. 109503. doi: 10.1016/j.cellsig.2019.109503

[93] Dodge JC, Yu J, Sardi SP, Shihabuddin LS. Sterol auto-oxidation adversely affects human motor neuron viability and is a neuropathological feature of amyotrophic lateral sclerosis. Sci Rep. 2021;11(1):803. doi: 10.1038/s41598-020-80378-y

[94] Dodge J.C., Yu J., Sardi S.P., Shihabuddin L.S. Sterol auto-oxidation adversely affects human motor neuron viability and is a neuropathological feature of amyotrophic lateral sclerosis // Sci Rep. 2021. Vol. 11, N 1. P. 803. doi: 10.1038/s41598-020-80378-y

[95] Kim SM, Noh MY, Kim H, et al. 25-hydroxycholesterol is involved in the pathogenesis of amyotrophic lateral sclerosis. Oncotarget. 2017;8(7):11855–11867. doi: 10.18632/oncotarget.14416

[96] Kim S.M., Noh M.Y., Kim H., et al. 25-hydroxycholesterol is involved in the pathogenesis of amyotrophic lateral sclerosis // Oncotarget. 2017. Vol. 8, N 7. P. 11855–11867. doi: 10.18632/oncotarget.14416

[97] Choi YK, Kim YS, Choi IY, et al. 25-hydroxycholesterol induces mitochondria-dependent apoptosis via activation of glycogen synthase kinase-3beta in PC12 cells. Free Radic Res. 2008;42(6):544–553. doi: 10.1080/10715760802146062

[98] Choi Y.K., Kim Y.S., Choi I.Y., et al. 25-hydroxycholesterol induces mitochondria-dependent apoptosis via activation of glycogen synthase kinase-3beta in PC12 cells // Free Radic Res. 2008. Vol. 42, N 6. P. 544–553. doi: 10.1080/10715760802146062

[99] Kim SM, Kim H, Kim JE, et al. Amyotrophic lateral sclerosis is associated with hypolipidemia at the presymptomatic stage in mice. PLoS One. 2011;6(3):e17985. doi: 10.1371/journal.pone.0017985

[100] Kim S.M., Kim H., Kim J.E., et al. Amyotrophic lateral sclerosis is associated with hypolipidemia at the presymptomatic stage in mice // PLoS One. 2011. Vol. 6, N 3. P. e17985. doi: 10.1371/journal.pone.0017985

[101] Chen X, Yazdani S, Piehl F, et al. Polygenic link between blood lipids and amyotrophic lateral sclerosis. Neurobiol Aging. 2018;67:202.e1–202.e6. doi: 10.1016/j.neurobiolaging.2018.03.022

[102] Chen X., Yazdani S., Piehl F., et al. Polygenic link between blood lipids and amyotrophic lateral sclerosis // Neurobiol Aging. 2018. Vol. 67. P. 202. doi: 10.1016/j.neurobiolaging.2018.03.022

[103] Zakyrjanova GF, Giniatullin AR, Mukhutdinova KA, et al. Early differences in membrane properties at the neuromuscular junctions of ALS model mice: effects of 25-hydroxycholesterol. Life Sci. 2021;273:119300. doi: 10.1016/j.lfs.2021.119300

[104] Zakyrjanova G.F., Giniatullin A.R., Mukhutdinova K.A., et al. Early differences in membrane properties at the neuromuscular junctions of ALS model mice: effects of 25-hydroxycholesterol // Life Sci. 2021. Vol. 273. P. 119300. doi: 10.1016/j.lfs.2021.119300

[105] Deguise MO, Baranello G, Mastella C, et al. Abnormal fatty acid metabolism is a core component of spinal muscular atrophy. Ann Clin Transl Neurol. 2019;6(8):1519–1532. doi: 10.1002/acn3.50855

[106] Deguise M.O., Baranello G., Mastella C., et al. Abnormal fatty acid metabolism is a core component of spinal muscular atrophy // Ann Clin Transl Neurol. 2019. Vol. 6, N 8. P. 1519–1532. doi: 10.1002/acn3.50855

[107] Darios F, Mochel F, Stevanin G. Lipids in the physiopathology of hereditary spastic paraplegias. Front Neurosci. 2020;14:74. doi: 10.3389/fnins.2020.00074

[108] Darios F., Mochel F., Stevanin G. Lipids in the physiopathology of hereditary spastic paraplegias // Front Neurosci. 2020. Vol. 14. P. 74. doi: 10.3389/fnins.2020.00074

[109] González-Guevara E, Cárdenas G, Pérez-Severiano F, Martínez-Lazcano JC. Dysregulated brain cholesterol metabolism is linked to neuroinflammation in huntington’s disease. Mov Disord. 2020;35(7):1113–1127. doi: 10.1002/mds.28089

[110] González-Guevara E., Cárdenas G., Pérez-Severiano F., Martínez-Lazcano J.C. Dysregulated brain cholesterol metabolism is linked to neuroinflammation in huntington’s disease // Mov Disord. 2020. Vol. 35, N 7. P. 1113–1127. doi: 10.1002/mds.28089

[111] Fanning S, Selkoe D, Dettmer U. Parkinson’s disease: proteinopathy or lipidopathy? NPJ Parkinsons Dis. 2020;6:3. doi: 10.1038/s41531-019-0103-7

[112] Fanning S., Selkoe D., Dettmer U. Parkinson’s disease: proteinopathy or lipidopathy? // NPJ Parkinsons Dis. 2020. Vol. 6. P. 3. doi: 10.1038/s41531-019-0103-7

[113] Luchsinger JA, Cheng D, Tang MX, et al. Central obesity in the elderly is related to late-onset Alzheimer disease. Alzheimer Dis Assoc Disord. 2012;26(2):101–105. doi: 10.1097/WAD.0b013e318222f0d4

[114] Luchsinger J.A., Cheng D., Tang M.X., et al. Central obesity in the elderly is related to late-onset Alzheimer disease // Alzheimer Dis Assoc Disord. 2012. Vol. 26, N 2. P. 101–105. doi: 10.1097/WAD.0b013e318222f0d4

[115] Tolppanen AM, Ngandu T, Kåreholt I, et al. Midlife and late-life body mass index and late-life dementia: results from a prospective population-based cohort. J Alzheimers Dis. 2014;38(1):201–209. doi: 10.3233/JAD-130698

[116] Tolppanen A.M., Ngandu T., Kåreholt I., et al. Midlife and late-life body mass index and late-life dementia: results from a prospective population-based cohort // J Alzheimers Dis. 2014. Vol. 38, N 1. P. 201–209. doi: 10.3233/JAD-130698

[117] Han X. Lipid alterations in the earliest clinically recognizable stage of Alzheimer’s disease: implication of the role of lipids in the pathogenesis of Alzheimer’s disease. Curr Alzheimer Res. 2005;2(1):65–77. doi: 10.2174/1567205052772786

[118] Han X. Lipid alterations in the earliest clinically recognizable stage of Alzheimer’s disease: implication of the role of lipids in the pathogenesis of Alzheimer’s disease // Curr Alzheimer Res. 2005. Vol. 2, N 1. P. 65–77. doi: 10.2174/1567205052772786

[119] Schengrund CL. Lipid rafts: keys to neurodegeneration. Brain Res Bull. 2010;82(1-2):7–17. doi: 10.1016/j.brainresbull.2010.02.013

[120] Schengrund C.L. Lipid rafts: keys to neurodegeneration // Brain Res Bull. 2010. Vol. 82, N 1-2. P. 7–17. doi: 10.1016/j.brainresbull.2010.02.013

[121] Cutler RG, Pedersen WA, Camandola S, et al. Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis. Ann Neurol. 2002;52(4):448–457. doi: 10.1002/ana.10312

[122] Cutler R.G., Pedersen W.A., Camandola S., et al. Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis // Ann Neurol. 2002. Vol. 52, N 4. P. 448–457. doi: 10.1002/ana.10312

[123] Cooper-Knock J, Zhang S, Kenna KP, et al. Rare variant burden analysis within enhancers identifies CAV1 as an ALS risk gene. Cell Rep. 2020;33(9):108456. Corrected and republished from: Cell Rep. 2021. Vol. 34, N 5. doi: 10.1016/j.celrep.2020.108456

[124] Cooper-Knock J., Zhang S., Kenna K.P., et al. Rare variant burden analysis within enhancers identifies CAV1 as an ALS risk gene // Cell Rep. 2020. Vol. 33, N 9. P. 108456. Corrected and republished from: Cell Rep. 2021. Vol. 34, N 5. P. 108730. doi: 10.1016/j.celrep.2020.108456

[125] Zhang S, Cooper-Knock J, Weimer AK, et al. Genome-wide identification of the genetic basis of amyotrophic lateral sclerosis. Neuron. 2022;110(6):992–1008.e11. doi: 10.1016/j.neuron.2021.12.019

[126] Zhang S., Cooper-Knock J., Weimer A.K., et al. Genome-wide identification of the genetic basis of amyotrophic lateral sclerosis // Neuron. 2022. Vol. 110, N 6. P. 992–1008. doi: 10.1016/j.neuron.2021.12.019

[127] Levy M, Futerman AH. Mammalian ceramide synthases. IUBMB Life. 2010;62(5):347–356. doi: 10.1002/iub.319

[128] Levy M., Futerman A.H. Mammalian ceramide synthases // IUBMB Life. 2010. Vol. 62, N 5. P. 347–356. doi: 10.1002/iub.319

[129] Pradhan J, Noakes PG, Bellingham MC. The role of altered BDNF/TrkB signaling in amyotrophic lateral sclerosis. Front Cell Neurosci. 2019;13:368. doi: 10.3389/fncel.2019.00368

[130] Pradhan J., Noakes P.G., Bellingham M.C. The role of altered BDNF/TrkB signaling in amyotrophic lateral sclerosis // Front Cell Neurosci. 2019. Vol. 13. P. 368. doi: 10.3389/fncel.2019.00368

[131] Mojsilovic-Petrovic J, Jeong GB, Crocker A, et al. Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors. J Neurosci. 2006;26(36):9250–9263. Corrected and republished from: J Neurosci. 2006;26(40):10079. doi: 10.1523/JNEUROSCI.1856-06.2006

[132] Mojsilovic-Petrovic J., Jeong G.B., Crocker A., et al. Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors // J Neurosci. 2006. Vol. 26, N 36. P. 9250–9263. Corrected and republished from: J Neurosci. 2006. Vol. 26, N 40. P. 10079. doi: 10.1523/JNEUROSCI.1856-06.2006

[133] Petrov AM, Kravtsova VV, Matchkov VV, et al. Membrane lipid rafts are disturbed in the response of rat skeletal muscle to short-term disuse. Am J Physiol Cell Physiol. 2017;312(5):C627–C637. doi: 10.1152/ajpcell.00365.2016

[134] Petrov A.M., Kravtsova V.V., Matchkov V.V., et al. Membrane lipid rafts are disturbed in the response of rat skeletal muscle to short-term disuse // Am J Physiol Cell Physiol. 2017. Vol. 312, N 5. P. C627–C637. doi: 10.1152/ajpcell.00365.2016

[135] Petrov AM, Shalagina MN, Protopopov VA, et al. Changes in membrane ceramide pools in rat soleus muscle in response to short-term disuse. Int J Mol Sci. 2019;20(19):4860. doi: 10.3390/ijms20194860

[136] Petrov A.M., Shalagina M.N., Protopopov V.A., et al. Changes in membrane ceramide pools in rat soleus muscle in response to short-term disuse // Int J Mol Sci. 2019. Vol. 20, N 19. P. 4860. doi: 10.3390/ijms20194860

[137] Bryndina IG, Shalagina MN, Sekunov AV, et al. Clomipramine counteracts lipid raft disturbance due to short-term muscle disuse. Neurosci Lett. 2018;664:1–6. doi: 10.1016/j.neulet.2017.11.009

[138] Bryndina I.G., Shalagina M.N., Sekunov A.V., et al. Clomipramine counteracts lipid raft disturbance due to short-term muscle disuse // Neurosci Lett. 2018. Vol. 664. P. 1–6. doi: 10.1016/j.neulet.2017.11.009

[139] Petrov AM, Naumenko NV, Uzinskaya KV, et al. Increased non-quantal release of acetylcholine after inhibition of endocytosis by methyl-β-cyclodextrin: the role of vesicular acetylcholine transporter. Neuroscience. 2011;186:1–12. Corrected and republished from: Neuroscience. 2011;192:806. doi: 10.1016/j.neuroscience.2011.04.051

[140] Petrov A.M., Naumenko N.V., Uzinskaya K.V., et al. Increased non-quantal release of acetylcholine after inhibition of endocytosis by methyl-β-cyclodextrin: the role of vesicular acetylcholine transporter // Neuroscience. 2011. Vol. 186. P. 1–12. Corrected and republished from: Neuroscience. 2011. Vol. 192. P. 806. doi: 10.1016/j.neuroscience.2011.04.051

[141] Sugita S, Fleming LL, Wood C, et al. VAChT overexpression increases acetylcholine at the synaptic cleft and accelerates aging of neuromuscular junctions. Skelet Muscle. 2016;6:31. doi: 10.1186/s13395-016-0105-7

[142] Sugita S., Fleming L.L., Wood C., et al. VAChT overexpression increases acetylcholine at the synaptic cleft and accelerates aging of neuromuscular junctions // Skelet Muscle. 2016. Vol. 6. P. 31. doi: 10.1186/s13395-016-0105-7

[143] Rocha MC, Pousinha PA, Correia AM, et al. Early changes of neuromuscular transmission in the SOD1(G93A) mice model of ALS start long before motor symptoms onset. PLoS One. 2013;8(9):e73846. doi: 10.1371/journal.pone.0073846

[144] Rocha M.C., Pousinha P.A., Correia A.M., et al. Early changes of neuromuscular transmission in the SOD1(G93A) mice model of ALS start long before motor symptoms onset // PLoS One. 2013. Vol. 8, N 9. P. e73846. doi: 10.1371/journal.pone.0073846

[145] Petrov AM, Yakovleva AA, Zefirov AL. Role of membrane cholesterol in spontaneous exocytosis at frog neuromuscular synapses: reactive oxygen species-calcium interplay. J Physiol. 2014;592(22):4995–5009. doi: 10.1113/jphysiol.2014.279695

[146] Petrov A.M., Yakovleva A.A., Zefirov A.L. Role of membrane cholesterol in spontaneous exocytosis at frog neuromuscular synapses: reactive oxygen species-calcium interplay // J Physiol. 2014. Vol. 592, N 22. P. 4995–5009. doi: 10.1113/jphysiol.2014.279695

[147] Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med. 1991;11(1):81–128. doi: 10.1016/0891-5849(91)90192-6

[148] Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes // Free Radic Biol Med. 1991. Vol. 11, N 1. P. 81–128. doi: 10.1016/0891-5849(91)90192-6

[149] Teuling E, Ahmed S, Haasdijk E, et al. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J Neurosci. 2007;27(36):9801–9815. doi: 10.1523/JNEUROSCI.2661-07.2007

[150] Teuling E., Ahmed S., Haasdijk E., et al. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates // J Neurosci. 2007. Vol. 27, N 36. P. 9801–9815. doi: 10.1523/JNEUROSCI.2661-07.2007

[151] Perry RJ, Ridgway ND. Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein. Mol Biol Cell. 2006;17(6):2604–2616. doi: 10.1091/mbc.e06-01-0060

[152] Perry R.J., Ridgway N.D. Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein // Mol Biol Cell. 2006. Vol. 17, N 6. P. 2604–2616. doi: 10.1091/mbc.e06-01-0060

[153] Dupuis L, Corcia P, Fergani A, et al. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology. 2008;70(13):1004–1009. doi: 10.1212/01.wnl.0000285080.70324.27

[154] Dupuis L., Corcia P., Fergani A., et al. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis // Neurology. 2008. Vol. 70, N 13. P. 1004–1009. doi: 10.1212/01.wnl.0000285080.70324.27

[155] Zheng Z, Sheng L, Shang H. Statins and amyotrophic lateral sclerosis: a systematic review and meta-analysis. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14(4):241–245. doi: 10.3109/21678421.2012.732078

[156] Zheng Z., Sheng L., Shang H. Statins and amyotrophic lateral sclerosis: a systematic review and meta-analysis // Amyotroph Lateral Scler Frontotemporal Degener. 2013. Vol. 14, N 4. P. 241–245. doi: 10.3109/21678421.2012.732078

[157] Krivoi II, Petrov AM. Cholesterol and the safety factor for neuromuscular transmission. Int J Mol Sci. 2019;20(5):1046. doi: 10.3390/ijms20051046

[158] Krivoi I.I., Petrov A.M. Cholesterol and the safety factor for neuromuscular transmission // Int J Mol Sci. 2019. Vol. 20, N 5. P. 1046. doi: 10.3390/ijms20051046

[159] Ingre C, Chen L, Zhan Y, et al. Lipids, apolipoproteins, and prognosis of amyotrophic lateral sclerosis. Neurology. 2020;94(17):e1835–e1844. doi: 10.1212/WNL.0000000000009322

[160] Ingre C., Chen L., Zhan Y., et al. Lipids, apolipoproteins, and prognosis of amyotrophic lateral sclerosis // Neurology. 2020. Vol. 94, N 17. P. e1835–e1844. doi: 10.1212/WNL.0000000000009322

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