{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T05:46:00Z","timestamp":1792734360198,"version":"4.5.0"},"reference-count":114,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,5,21]],"date-time":"2024-05-21T00:00:00Z","timestamp":1716249600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>The rabies virus enters the nervous system by interacting with several molecular targets on host cells to modify behavior and trigger receptor-mediated endocytosis of the virion by poorly understood mechanisms. The rabies virus glycoprotein (RVG) interacts with the muscle acetylcholine receptor and the neuronal \u03b14\u03b22 subtype of the nicotinic acetylcholine receptor (nAChR) family by the putative neurotoxin-like motif. Given that the neurotoxin-like motif is highly homologous to the \u03b17 nAChR subtype selective snake toxin \u03b1-bungarotoxin (\u03b1BTX), other nAChR subtypes are likely involved. The purpose of this study is to determine the activity of the RVG neurotoxin-like motif on nAChR subtypes that are expressed in brain regions involved in rabid animal behavior. nAChRs were expressed in <jats:italic>Xenopus laevis<\/jats:italic> oocytes, and two-electrode voltage clamp electrophysiology was used to collect concentration-response data to measure the functional effects. The RVG peptide preferentially and completely inhibits \u03b17 nAChR ACh-induced currents by a competitive antagonist mechanism. Tested heteromeric nAChRs are also inhibited, but to a lesser extent than the \u03b17 subtype. Residues of the RVG peptide with high sequence homology to \u03b1BTX and other neurotoxins were substituted with alanine. Altered RVG neurotoxin-like peptides showed that residues phenylalanine 192, arginine 196, and arginine 199 are important determinants of RVG peptide apparent potency on \u03b17 nAChRs, while serine 195 is not. The evaluation of the rabies ectodomain reaffirmed the observations made with the RVG peptide, illustrating a significant inhibitory impact on \u03b17 nAChR with potency in the nanomolar range. In a mammalian cell culture model of neurons, we confirm that the RVG peptide binds preferentially to cells expressing the \u03b17 nAChR. Defining the activity of the RVG peptide on nAChRs expands our understanding of basic mechanisms in host-pathogen interactions that result in neurological disorders.<\/jats:p>","DOI":"10.3389\/fcimb.2024.1394713","type":"journal-article","created":{"date-parts":[[2024,5,21]],"date-time":"2024-05-21T04:44:46Z","timestamp":1716266686000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":20,"title":["The human alpha7 nicotinic acetylcholine receptor is a host target for the rabies virus glycoprotein"],"prefix":"10.3389","volume":"14","author":[{"given":"Brittany C. V.","family":"O\u2019Brien","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shelly","family":"Thao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lahra","family":"Weber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helen L.","family":"Danielson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agatha D.","family":"Boldt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karsten","family":"Hueffer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maegan M.","family":"Weltzin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,5,21]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1242\/jeb.073601","article-title":"Parasites: evolution's neurobiologists","volume":"216","author":"Adamo","year":"2013","journal-title":"J. Exp. Biol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1111\/j.1749-6632.1995.tb17464.x","article-title":"Nicotinic receptor function in the mammalian central nervous system","volume":"757","author":"Albuquerque","year":"1995","journal-title":"Ann. N Y Acad. Sci."},{"key":"B3","doi-asserted-by":"publisher","first-page":"34851","DOI":"10.1074\/jbc.274.49.34851","article-title":"Variability among the sites by which curaremimetic toxins bind to torpedo acetylcholine receptor, as revealed by identification of the functional residues of alpha-cobratoxin","volume":"274","author":"Antil","year":"1999","journal-title":"J. Biol. Chem."},{"key":"B4","doi-asserted-by":"publisher","first-page":"29594","DOI":"10.1074\/jbc.M909746199","article-title":"Molecular determinants by which a long chain toxin from snake venom interacts with the neuronal alpha 7-nicotinic acetylcholine receptor","volume":"275","author":"Antil-Delbeke","year":"2000","journal-title":"J. Biol. Chem."},{"key":"B5","doi-asserted-by":"publisher","first-page":"771","DOI":"10.1038\/aps.2009.47","article-title":"Alpha-conotoxins as pharmacological probes of nicotinic acetylcholine receptors","volume":"30","author":"Azam","year":"2009","journal-title":"Acta Pharmacol. Sin."},{"key":"B6","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.neures.2008.05.004","article-title":"p75NTR activation of NF-\u03baB is involved in PrP106\u2013126-induced apoptosis in mouse neuroblastoma cells","volume":"62","author":"Bai","year":"2008","journal-title":"Neurosci. Res."},{"key":"B7","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.toxicon.2013.01.019","article-title":"Alpha neurotoxins","volume":"66","author":"Barber","year":"2013","journal-title":"Toxicon"},{"key":"B8","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1016\/j.virol.2017.08.019","article-title":"The phenotype of the RABV glycoprotein determines cellular and global virus load in the brain and is decisive for the pace of the disease","volume":"511","author":"Bertoune","year":"2017","journal-title":"Virology"},{"key":"B9","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1159\/000111973","article-title":"Neuroblastoma cell-oligodendrocyte interaction is mediated by neural cell adhesion molecules","volume":"10","author":"Bhat","year":"1988","journal-title":"Dev. Neurosci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1512","DOI":"10.1038\/sj.emboj.7600620","article-title":"Crystal structure of a Cbtx-AChBP complex reveals essential interactions between snake alpha-neurotoxins and nicotinic receptors","volume":"24","author":"Bourne","year":"2005","journal-title":"EMBO J."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1350","DOI":"10.1124\/mol.106.026682","article-title":"Incorporation of the beta3 subunit has a dominant-negative effect on the function of recombinant central-type neuronal nicotinic receptors","volume":"70","author":"Broadbent","year":"2006","journal-title":"Mol. Pharmacol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"i207","DOI":"10.1093\/bioinformatics\/btn268","article-title":"Comprehensive in silico mutagenesis highlights functionally important residues in proteins","volume":"24","author":"Bromberg","year":"2008","journal-title":"Bioinformatics"},{"key":"B13","doi-asserted-by":"publisher","first-page":"970","DOI":"10.1111\/j.1476-5381.2008.00104.x","article-title":"Pentameric concatenated (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) nicotinic acetylcholine receptors: subunit arrangement determines functional expression","volume":"156","author":"Carbone","year":"2009","journal-title":"Br. J. Pharmacol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.pt.2010.03.009","article-title":"Host-manipulation by parasites with complex life cycles: adaptive or not","volume":"26","author":"Cezilly","year":"2010","journal-title":"Trends Parasitol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"7820","DOI":"10.1523\/JNEUROSCI.23-21-07820.2003","article-title":"Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice","volume":"23","author":"Champtiaux","year":"2003","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1243","DOI":"10.1016\/S0041-0101(96)00110-9","article-title":"Binding of native kappa-neurotoxins and site-directed mutants to nicotinic acetylcholine receptors","volume":"34","author":"Chiappinelli","year":"1996","journal-title":"Toxicon"},{"key":"B17","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1111\/j.1471-4159.2012.07685.x","article-title":"Modulation of recombinant, alpha2*, alpha3* or alpha4*-nicotinic acetylcholine receptor (nAChR) function by nAChR beta3 subunits","volume":"121","author":"Dash","year":"2012","journal-title":"J. Neurochem."},{"key":"B18","doi-asserted-by":"publisher","first-page":"28338","DOI":"10.1074\/jbc.M114.566018","article-title":"Roles for N-terminal extracellular domains of nicotinic acetylcholine receptor (nAChR) beta3 subunits in enhanced functional expression of mouse alpha6beta2beta3- and alpha6beta4beta3-nAChRs","volume":"289","author":"Dash","year":"2014","journal-title":"J. Biol. Chem."},{"key":"B19","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1038\/ni1229","article-title":"Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway","volume":"6","author":"de Jonge","year":"2005","journal-title":"Nat. Immunol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1124\/mol.108.046623","article-title":"Presynaptic alpha 7- and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms","volume":"74","author":"Dickinson","year":"2008","journal-title":"Mol. Pharmacol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/0169-328X(91)90112-B","article-title":"Structural and conformational similarity between synthetic peptides of curaremimetic neurotoxins and rabies virus glycoprotein","volume":"11","author":"Donnelly-Roberts","year":"1991","journal-title":"Brain Res. Mol. Brain Res."},{"key":"B22","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1124\/jpet.113.208389","article-title":"The unique \u03b14+\/-\u03b14 agonist binding site in (\u03b14)3(\u03b22)2 subtype nicotinic acetylcholine receptors permits differential agonist desensitization pharmacology versus the (\u03b14)2(\u03b22)3 subtype","volume":"348","author":"Eaton","year":"2014","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"B23","first-page":"54","article-title":"HIV-associated neurocognitive disorders (HAND)","volume":"17","author":"Elbirt","year":"2015","journal-title":"Isr. Med. Assoc. J."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.622516","article-title":"Street RABV Induces the Cholinergic Anti-inflammatory Pathway in Human Monocyte-Derived Macrophages by Binding to nAChr alpha7","volume":"12","author":"Embregts","year":"2021","journal-title":"Front. Immunol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"7993","DOI":"10.1523\/JNEUROSCI.21-20-07993.2001","article-title":"Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus","volume":"21","author":"Fabian-Fine","year":"2001","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."},{"key":"B26","doi-asserted-by":"publisher","first-page":"7993","DOI":"10.1523\/JNEUROSCI.21-20-07993.2001","article-title":"Ultrastructural distribution of the \u03b17 nicotinic acetylcholine receptor subunit in rat hippocampus","volume":"21","author":"Fabian-Fine","year":"2001","journal-title":"J. Neurosci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/j.biopsych.2013.08.014","article-title":"A mouse model that recapitulates cardinal features of the 15q13.3 microdeletion syndrome including schizophrenia- and epilepsy-related alterations","volume":"76","author":"Fejgin","year":"2014","journal-title":"Biol. Psychiatry"},{"key":"B28","volume-title":"Measuring Cell Fluorescence Using ImageJ","author":"Fitzpatrick","year":"2014"},{"key":"B29","doi-asserted-by":"publisher","first-page":"17091","DOI":"10.1038\/nrdp.2017.91","article-title":"Rabies","volume":"3","author":"Fooks","year":"2017","journal-title":"Nat. Rev. Dis. Primers."},{"key":"B30","doi-asserted-by":"publisher","first-page":"3216","DOI":"10.1073\/pnas.042699899","article-title":"Experimentally based model of a complex between a snake toxin and the alpha 7 nicotinic receptor","volume":"99","author":"Fruchart-Gaillard","year":"2002","journal-title":"Proc. Natl. Acad. Sci. U S A."},{"key":"B31","doi-asserted-by":"publisher","first-page":"3207","DOI":"10.1111\/j.1742-4658.2008.06473.x","article-title":"Conserved structural determinants in three-fingered protein domains","volume":"275","author":"Galat","year":"2008","journal-title":"FEBS J."},{"key":"B32","doi-asserted-by":"publisher","first-page":"25151","DOI":"10.1074\/jbc.M112.379339","article-title":"Function of human alpha3beta4alpha5 nicotinic acetylcholine receptors is reduced by the alpha5(D398N) variant","volume":"287","author":"George","year":"2012","journal-title":"J. Biol. Chem."},{"key":"B33","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1007\/s10803-016-2961-8","article-title":"The cognitive and behavioral phenotypes of individuals with CHRNA7 duplications","volume":"47","author":"Gillentine","year":"2017","journal-title":"J. Autism Dev. Disord."},{"key":"B34","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1016\/j.pneurobio.2004.09.006","article-title":"Neuronal nicotinic receptors: from structure to pathology","volume":"74","author":"Gotti","year":"2004","journal-title":"Prog. Neurobiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1016\/j.bcp.2009.05.024","article-title":"Structural and functional diversity of native brain neuronal nicotinic receptors","volume":"78","author":"Gotti","year":"2009","journal-title":"Biochem. Pharmacol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"5311","DOI":"10.1523\/JNEUROSCI.5095-09.2010","article-title":"Nicotinic acetylcholine receptors in the mesolimbic pathway: primary role of ventral tegmental area alpha6beta2* receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement","volume":"30","author":"Gotti","year":"2010","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"2007","DOI":"10.1124\/mol.105.011940","article-title":"Expression of nigrostriatal alpha 6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by beta 3 subunit gene deletion","volume":"67","author":"Gotti","year":"2005","journal-title":"Mol. Pharmacol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"1796","DOI":"10.1124\/mol.108.045203","article-title":"Partial deletion of the nicotinic cholinergic receptor alpha 4 or beta 2 subunit genes changes the acetylcholine sensitivity of receptor-mediated 86Rb+ efflux in cortex and thalamus and alters relative expression of alpha 4 and beta 2 subunits","volume":"73","author":"Gotti","year":"2008","journal-title":"Mol. Pharmacol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1235","DOI":"10.1016\/j.bcp.2007.07.032","article-title":"The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum","volume":"74","author":"Grady","year":"2007","journal-title":"Biochem. Pharmacol."},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0003709","article-title":"Estimating the global burden of endemic canine rabies","volume":"9","author":"Hampson","year":"2015","journal-title":"PloS Negl. Trop. Dis."},{"key":"B41","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.jns.2017.07.027","article-title":"Retroviral envelope proteins: Involvement in neuropathogenesis","volume":"380","author":"Hansen","year":"2017","journal-title":"J. neurological Sci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/978-3-540-36622-5","article-title":"Nicotinic acetylcholine receptors: from structure to brain function","volume":"147","author":"Hogg","year":"2003","journal-title":"Rev. Physiol. Biochem. Pharmacol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"6262","DOI":"10.1021\/acs.jmedchem.9b00566","article-title":"PeIA-5466: A novel peptide antagonist containing non-natural amino acids that selectively targets alpha3beta2 nicotinic acetylcholine receptors","volume":"62","author":"Hone","year":"2019","journal-title":"J. Med. Chem."},{"key":"B44","doi-asserted-by":"publisher","first-page":"2483","DOI":"10.1021\/acschembio.2c00315","article-title":"Discovery and structural and functional characterization of a novel A-superfamily conotoxin targeting alpha9alpha10 nicotinic acetylcholine receptor","volume":"17","author":"Huang","year":"2022","journal-title":"ACS Chem. Biol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1042\/BJ20130636","article-title":"Complex between alpha-bungarotoxin and an alpha7 nicotinic receptor ligand-binding domain chimaera","volume":"454","author":"Huang","year":"2013","journal-title":"Biochem. J."},{"key":"B46","doi-asserted-by":"publisher","first-page":"12818","DOI":"10.1038\/s41598-017-12726-4","article-title":"Rabies virus modifies host behaviour through a snake-toxin like region of its glycoprotein that inhibits neurotransmitter receptors in the CNS","volume":"7","author":"Hueffer","year":"2017","journal-title":"Sci. Rep."},{"key":"B47","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1016\/j.pharmthera.2012.08.012","article-title":"Nicotinic acetylcholine receptors: from basic science to therapeutics","volume":"137","author":"Hurst","year":"2013","journal-title":"Pharmacol. Ther."},{"key":"B48","doi-asserted-by":"publisher","first-page":"169","DOI":"10.7705\/biomedica.v29i2.18","article-title":"Therapy of rabies encephalitis","volume":"29","author":"Jackson","year":"2009","journal-title":"Biomedica"},{"key":"B49","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1007\/s13365-015-0365-8","article-title":"Mind-altering microbes","volume":"22","author":"Jackson","year":"2016","journal-title":"J. Neurovirol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1007\/s13365-015-0351-1","article-title":"Diabolical effects of rabies encephalitis","volume":"22","author":"Jackson","year":"2016","journal-title":"J. Neurovirol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"11244","DOI":"10.1523\/JNEUROSCI.3009-04.2004","article-title":"Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area","volume":"24","author":"Jones","year":"2004","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"354","DOI":"10.1016\/j.tips.2018.01.002","article-title":"Beyond the channel: metabotropic signaling by nicotinic receptors","volume":"39","author":"Kabbani","year":"2018","journal-title":"Trends Pharmacol. Sci."},{"key":"B53","doi-asserted-by":"publisher","first-page":"1025","DOI":"10.1002\/bies.201300082","article-title":"Are nicotinic acetylcholine receptors coupled to G proteins","volume":"35","author":"Kabbani","year":"2013","journal-title":"Bioessays"},{"key":"B54","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1083\/jcb.110.1.193","article-title":"The neural cell adhesion molecule N-CAM enhances L1-dependent cell-cell interactions","volume":"110","author":"Kadmon","year":"1990","journal-title":"J. Cell Biol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1016\/j.neuropharm.2004.06.024","article-title":"Beta2-subunit-containing nicotinic acetylcholine receptors are critical for dopamine-dependent locomotor activation following repeated nicotine administration","author":"King","year":"2004","journal-title":"Neuropharmacology"},{"key":"B56","doi-asserted-by":"publisher","first-page":"i","DOI":"10.1242\/jeb.083162","article-title":"How pernicious parasites turn victims into zombies","volume":"216","author":"Knight","year":"2013","journal-title":"J. Exp. Biol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1124\/mol.110.066159","article-title":"Expression of functional human alpha6beta2beta3* acetylcholine receptors in Xenopus laevis oocytes achieved through subunit chimeras and concatamers","volume":"79","author":"Kuryatov","year":"2011","journal-title":"Mol. Pharmacol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"2570","DOI":"10.1016\/S0028-3908(00)00144-1","article-title":"Human alpha6 AChR subtypes: subunit composition, assembly, and pharmacological responses","volume":"39","author":"Kuryatov","year":"2000","journal-title":"Neuropharmacology"},{"key":"B59","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1111\/jmi.2011.243.issue-2","article-title":"Application of regularized Richardson\u2013Lucy algorithm for deconvolution of confocal microscopy images","volume":"243","author":"Laasmaa","year":"2011","journal-title":"J. Microscopy"},{"key":"B60","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1080\/13550280590900427","article-title":"Rabies virus receptors","volume":"11","author":"Lafon","year":"2005","journal-title":"J. Neurovirol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1080\/13550280701883857","article-title":"Furious and paralytic rabies of canine origin: neuroimaging with virological and cytokine studies","volume":"14","author":"Laothamatas","year":"2008","journal-title":"J. Neurovirol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"10949","DOI":"10.1021\/bi00109a020","article-title":"Structure-function relationships of curaremimetic neurotoxin loop 2 and of a structurally similar segment of rabies virus glycoprotein in their interaction with the nicotinic acetylcholine receptor","volume":"30","author":"Lentz","year":"1991","journal-title":"Biochemistry"},{"key":"B63","first-page":"315","article-title":"The acetylcholine receptor as a cellular receptor for rabies virus","volume":"56","author":"Lentz","year":"1983","journal-title":"Yale J. Biol. Med."},{"key":"B64","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1002\/prot.340020406","article-title":"Synthetic peptides corresponding to sequences of snake venom neurotoxins and rabies virus glycoprotein bind to the nicotinic acetylcholine receptor","volume":"2","author":"Lentz","year":"1987","journal-title":"Proteins"},{"key":"B65","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-4939-1167-7","volume-title":"Nicotinic Receptors","author":"Lester","year":"2014"},{"key":"B66","doi-asserted-by":"publisher","first-page":"488","DOI":"10.1016\/j.bcp.2015.07.019","article-title":"Modulation of aggressive behavior in mice by nicotinic receptor subtypes","volume":"97","author":"Lewis","year":"2015","journal-title":"Biochem. Pharmacol."},{"key":"B67","doi-asserted-by":"publisher","first-page":"107929","DOI":"10.1016\/j.neuropharm.2019.107929","article-title":"Regulation of aggressive behaviors by nicotinic acetylcholine receptors: Animal models, human genetics, and clinical studies","volume":"167","author":"Lewis","year":"2020","journal-title":"Neuropharmacology"},{"key":"B68","doi-asserted-by":"publisher","first-page":"1267","DOI":"10.1038\/npp.2017.276","article-title":"Bidirectional regulation of aggression in mice by hippocampal alpha-7 nicotinic acetylcholine receptors","volume":"43","author":"Lewis","year":"2018","journal-title":"Neuropsychopharmacology"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1016\/j.heliyon.2022.e10434","article-title":"Interactions between the rabies virus and nicotinic acetylcholine receptors: A potential role in rabies virus induced behavior modifications","volume":"8","author":"Lian","year":"2022","journal-title":"Heliyon"},{"key":"B70","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1007\/978-1-4614-7651-1_7","article-title":"Cellular entry of retroviruses","volume":"790","author":"Lindemann","year":"2013","journal-title":"Adv. Exp. Med. Biol."},{"key":"B71","doi-asserted-by":"publisher","first-page":"1333","DOI":"10.1124\/mol.65.6.1333","article-title":"Getting past the asterisk: the subunit composition of presynaptic nicotinic receptors that modulate striatal dopamine release","volume":"65","author":"Luetje","year":"2004","journal-title":"Mol. Pharmacol."},{"key":"B72","doi-asserted-by":"publisher","first-page":"1842","DOI":"10.1096\/fj.13-244103","article-title":"A novel alpha4\/7-conotoxin LvIA from Conus lividus that selectively blocks alpha3beta2 vs. alpha6\/alpha3beta2beta3 nicotinic acetylcholine receptors","volume":"28","author":"Luo","year":"2014","journal-title":"FASEB J."},{"key":"B73","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1042\/bj20021537","article-title":"Identification of regions involved in the binding of alpha-bungarotoxin to the human alpha7 neuronal nicotinic acetylcholine receptor using synthetic peptides","volume":"372","author":"Marinou","year":"2003","journal-title":"Biochem. J."},{"key":"B74","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1242\/jeb.074088","article-title":"An overview of parasite-induced behavioral alterations - and some lessons from bats","volume":"216","author":"Moore","year":"2013","journal-title":"J. Exp. Biol."},{"key":"B75","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1006\/viro.1993.1405","article-title":"Shedding of Gs protein (a soluble form of the viral glycoprotein) by the rabies virus-infected BHK-21 cells","volume":"195","author":"Morimoto","year":"1993","journal-title":"Virology"},{"key":"B76","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1124\/mol.63.2.332","article-title":"Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors","volume":"63","author":"Nelson","year":"2003","journal-title":"Mol. Pharmacol."},{"key":"B77","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1186\/1742-4690-1-9","article-title":"Early steps of retrovirus replicative cycle","volume":"1","author":"Nisole","year":"2004","journal-title":"Retrovirology"},{"key":"B78","doi-asserted-by":"publisher","first-page":"2121","DOI":"10.1016\/j.cell.2021.02.049","article-title":"Structure and gating mechanism of the alpha7 nicotinic acetylcholine receptor","volume":"184","author":"Noviello","year":"2021","journal-title":"Cell"},{"key":"B79","doi-asserted-by":"publisher","first-page":"104707","DOI":"10.1016\/j.jbc.2023.104707","article-title":"SARS-CoV-2 spike ectodomain targets \u03b17 nicotinic acetylcholine receptors","volume":"299","author":"O'Brien","year":"2023","journal-title":"J. Biol. Chem."},{"key":"B80","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.bcp.2014.01.029","article-title":"Merging old and new perspectives on nicotinic acetylcholine receptors","volume":"89","author":"Papke","year":"2014","journal-title":"Biochem. Pharmacol."},{"key":"B81","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/j.neuropharm.2014.12.028","article-title":"Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states","volume":"96","author":"Picciotto","year":"2015","journal-title":"Neuropharmacology"},{"key":"B82","doi-asserted-by":"publisher","first-page":"1371","DOI":"10.1016\/0020-7519(95)00100-X","article-title":"\"Adaptive\" changes in the behaviour of parasitized animals: a critical review","volume":"25","author":"Poulin","year":"1995","journal-title":"Int. J. Parasitol."},{"key":"B83","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1016\/j.bcp.2011.06.001","article-title":"Role of alpha6 nicotinic receptors in CNS dopaminergic function: relevance to addiction and neurological disorders","volume":"82","author":"Quik","year":"2011","journal-title":"Biochem. Pharmacol."},{"key":"B84","doi-asserted-by":"publisher","first-page":"952","DOI":"10.1016\/j.neuron.2020.03.012","article-title":"Structure of the native muscle-type nicotinic receptor and inhibition by snake venom toxins","volume":"106","author":"Rahman","year":"2020","journal-title":"Neuron"},{"key":"B85","doi-asserted-by":"publisher","first-page":"6431","DOI":"10.1523\/JNEUROSCI.20-17-06431.2000","article-title":"Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse","volume":"20","author":"Ross","year":"2000","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."},{"key":"B86","article-title":"Rhabdoviruses: rabies virus","volume-title":"Medical Microbiology 4th Edition","author":"Rupprecht","year":"1996"},{"key":"B87","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/S1473-3099(02)00287-6","article-title":"Rabies re-examined","volume":"2","author":"Rupprecht","year":"2002","journal-title":"Lancet Infect. diseases."},{"key":"B88","doi-asserted-by":"publisher","first-page":"961","DOI":"10.1002\/bip.360330612","article-title":"A model of the rabies virus glycoprotein active site","volume":"33","author":"Rustici","year":"1993","journal-title":"Biopolymers"},{"key":"B89","doi-asserted-by":"publisher","first-page":"1526","DOI":"10.1124\/mol.65.6.1526","article-title":"Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice","volume":"65","author":"Salminen","year":"2004","journal-title":"Mol. Pharmacol."},{"key":"B90","doi-asserted-by":"publisher","first-page":"5858","DOI":"10.1523\/JNEUROSCI.17-15-05858.1997","article-title":"Quantitative ultrastructural analysis of hippocampal excitatory synapses","volume":"17","author":"Schikorski","year":"1997","journal-title":"J. Neurosci."},{"key":"B91","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1038\/nrmicro2260","article-title":"The cell biology of rabies virus: using stealth to reach the brain","volume":"8","author":"Schnell","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"B92","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1016\/S0014-2999(00)00095-9","article-title":"Molecular characterization of the specificity of interactions of various neurotoxins on two distinct nicotinic acetylcholine receptors","volume":"393","author":"Servent","year":"2000","journal-title":"Eur. J. Pharmacol."},{"key":"B93","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1083\/jcb.201404107","article-title":"pHuji, a pH-sensitive red fluorescent protein for imaging of exo- and endocytosis","volume":"207","author":"Shen","year":"2014","journal-title":"J. Cell Biol."},{"key":"B94","doi-asserted-by":"publisher","first-page":"1269","DOI":"10.1038\/ng.481","article-title":"A small recurrent deletion within 15q13.3 is associated with a range of neurodevelopmental phenotypes","volume":"41","author":"Shinawi","year":"2009","journal-title":"Nat. Genet."},{"key":"B95","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.01819-19","article-title":"Integrin beta1 promotes peripheral entry by rabies virus","volume":"94","author":"Shuai","year":"2020","journal-title":"J. Virol."},{"key":"B96","doi-asserted-by":"publisher","first-page":"733","DOI":"10.1111\/j.1348-0421.2005.tb03664.x","article-title":"Further studies on the soluble form (gs) of rabies virus glycoprotein (g): molecular structure of gs protein and possible mechanism of the shedding","volume":"49","author":"Thirapanmethee","year":"2005","journal-title":"Microbiol. Immunol."},{"key":"B97","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.jneuroim.2012.07.006","article-title":"The \u03b17 nicotinic acetylcholine receptor ligands methyllycaconitine, NS6740 and GTS-21 reduce lipopolysaccharide-induced TNF-\u03b1 release from microglia","volume":"251","author":"Thomsen","year":"2012","journal-title":"J. Neuroimmunol"},{"key":"B98","doi-asserted-by":"publisher","first-page":"7181","DOI":"10.1128\/JVI.72.9.7181-7190.1998","article-title":"The neural cell adhesion molecule is a receptor for rabies virus","volume":"72","author":"Thoulouze","year":"1998","journal-title":"J. Virol."},{"key":"B99","doi-asserted-by":"publisher","first-page":"7250","DOI":"10.1093\/emboj\/17.24.7250","article-title":"Low-affinity nerve-growth factor receptor (P75NTR) can serve as a receptor for rabies virus","volume":"17","author":"Tuffereau","year":"1998","journal-title":"EMBO J."},{"key":"B100","doi-asserted-by":"publisher","first-page":"6442","DOI":"10.1073\/pnas.0608310104","article-title":"Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors","volume":"104","author":"Vyas","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U S A."},{"key":"B101","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1002\/cne.902840212","article-title":"Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat","volume":"284","author":"Wada","year":"1989","journal-title":"J. Comp. Neurol."},{"key":"B102","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1007189","article-title":"Metabotropic glutamate receptor subtype 2 is a cellular receptor for rabies virus","volume":"14","author":"Wang","year":"2018","journal-title":"PloS Pathog."},{"key":"B103","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1242\/jeb.074716","article-title":"Toxoplasma gondii infection, from predation to schizophrenia: can animal behaviour help us understand human behaviour","volume":"216","author":"Webster","year":"2013","journal-title":"J. Exp. Biol."},{"key":"B104","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0213143","article-title":"Distinctive single-channel properties of alpha4beta2-nicotinic acetylcholine receptor isoforms","volume":"14","author":"Weltzin","year":"2019","journal-title":"PloS One"},{"key":"B105","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1016\/j.neuropharm.2015.11.004","article-title":"Distinctive effects of nicotinic receptor intracellular-loop mutations associated with nocturnal frontal lobe epilepsy","volume":"102","author":"Weltzin","year":"2016","journal-title":"Neuropharmacology"},{"key":"B106","doi-asserted-by":"publisher","first-page":"6628","DOI":"10.1021\/bi7004202","article-title":"Discovery, synthesis, and structure activity of a highly selective alpha7 nicotinic acetylcholine receptor antagonist","volume":"46","author":"Whiteaker","year":"2007","journal-title":"Biochemistry"},{"key":"B107","unstructured":"Rabies2017"},{"key":"B108","doi-asserted-by":"publisher","first-page":"800","DOI":"10.1016\/j.bcp.2011.07.067","article-title":"Naturally-expressed nicotinic acetylcholine receptor subtypes","volume":"82","author":"Wu","year":"2011","journal-title":"Biochem. Pharmacol."},{"key":"B109","doi-asserted-by":"publisher","first-page":"10092","DOI":"10.1021\/acs.jmedchem.3c01023","article-title":"Structure-activity relationships of alanine scan mutants alphaO-conotoxins geXIVA[1,2] and geXIVA[1,4]","volume":"66","author":"Xu","year":"2023","journal-title":"J. Med. Chem."},{"key":"B110","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1016\/j.chom.2019.12.012","article-title":"Structural analysis of rabies virus glycoprotein reveals pH-dependent conformational changes and interactions with a neutralizing antibody","volume":"27","author":"Yang","year":"2020","journal-title":"Cell Host Microbe"},{"key":"B111","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1016\/S0306-4522(98)00246-2","article-title":"Distributions of nicotinic acetylcholine receptor \u03b17 and \u03b22 subunits on cultured hippocampal neurons","volume":"88","author":"Zarei","year":"1999","journal-title":"Neuroscience"},{"key":"B112","doi-asserted-by":"publisher","first-page":"e700","DOI":"10.1002\/ctm2.700","article-title":"A spatial and cellular distribution of rabies virus infection in the mouse brain revealed by fMOST and single-cell RNA sequencing","volume":"12","author":"Zhang","year":"2022","journal-title":"Clin. Transl. Med."},{"key":"B113","doi-asserted-by":"publisher","first-page":"9111","DOI":"10.1523\/JNEUROSCI.0381-08.2008","article-title":"Presynaptic type III neuregulin 1 is required for sustained enhancement of hippocampal transmission by nicotine and for axonal targeting of alpha7 nicotinic acetylcholine receptors","volume":"28","author":"Zhong","year":"2008","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."},{"key":"B114","doi-asserted-by":"publisher","first-page":"4461","DOI":"10.1523\/JNEUROSCI.18-12-04461.1998","article-title":"Identification of four classes of brain nicotinic receptors using beta2 mutant mice","volume":"18","author":"Zoli","year":"1998","journal-title":"J. neuroscience: Off. J. Soc. Neurosci."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1394713\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,21]],"date-time":"2024-05-21T04:44:52Z","timestamp":1716266692000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1394713\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,21]]},"references-count":114,"alternative-id":["10.3389\/fcimb.2024.1394713"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2024.1394713","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,21]]},"article-number":"1394713"}}