{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T07:26:06Z","timestamp":1788852366763,"version":"build-2803163510"},"reference-count":71,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,12,16]],"date-time":"2022-12-16T00:00:00Z","timestamp":1671148800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation (RSF)","doi-asserted-by":"publisher","award":["19-14-00268"],"award-info":[{"award-number":["19-14-00268"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Glyprolines are Gly-Pro (GP)- or Pro-Gly (PG)-containing biogenic peptides. These peptides can act as neutrophil chemoattractants, or atheroprotective, anticoagulant, and neuroprotective agents. The Pro-Gly-Pro (PGP) tripeptide is an active factor of resistance to the biodegradation of peptide drugs. The synthetic Semax peptide, which includes Met-Glu-His-Phe (MEHF) fragments of adrenocorticotropic hormone and the C-terminal tripeptide PGP, serves as a neuroprotective drug for the treatment of ischemic stroke. Previously, we revealed that Semax mostly prevented the disruption of the gene expression pattern 24 h after a transient middle cerebral artery occlusion (tMCAO) in a rat brain model. The genes of this pattern were grouped into an inflammatory cluster (IC) and a neurotransmitter cluster (NC). Here, using real-time RT-PCR, the effect of other PGP-containing peptides, PGP and Pro-Gly-Pro-Leu (PGPL), on the expression of a number of genes in the IC and NC was studied 24 h after tMCAO. Both the PGP and PGPL peptides showed Semax-unlike effects, predominantly without changing gene expression 24 h after tMCAO. Moreover, there were IC genes (iL1b, iL6, and Socs3) for PGP, as well as IC (iL6, Ccl3, Socs3, and Fos) and NC genes (Cplx2, Neurod6, and Ptk2b) for PGPL, that significantly changed in expression levels after peptide administration compared to Semax treatment under tMCAO conditions. Furthermore, gene enrichment analysis was carried out, and a regulatory gene network was constructed. Thus, the spectra of the common and unique effects of the PGP, PGPL, and Semax peptides under ischemia\u2013reperfusion were distinguished.<\/jats:p>","DOI":"10.3390\/genes13122380","type":"journal-article","created":{"date-parts":[[2022,12,19]],"date-time":"2022-12-19T06:58:29Z","timestamp":1671433109000},"page":"2380","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Insight into Glyproline Peptides\u2019 Activity through the Modulation of the Inflammatory and Neurosignaling Genetic Response Following Cerebral Ischemia\u2013Reperfusion"],"prefix":"10.3390","volume":"13","author":[{"given":"Vasily V.","family":"Stavchansky","sequence":"first","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6964-3405","authenticated-orcid":false,"given":"Ivan B.","family":"Filippenkov","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia A.","family":"Remizova","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alina E.","family":"Denisova","sequence":"additional","affiliation":[{"name":"Department of Neurology, Neurosurgery and Medical Genetics, Pirogov Russian National Research Medical University, Ostrovitianov Str. 1, Moscow 117997, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivan V.","family":"Mozgovoy","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leonid V.","family":"Gubsky","sequence":"additional","affiliation":[{"name":"Department of Neurology, Neurosurgery and Medical Genetics, Pirogov Russian National Research Medical University, Ostrovitianov Str. 1, Moscow 117997, Russia"},{"name":"Federal Center for the Brain and Neurotechnologies, Federal Biomedical Agency, Ostrovitianov Str. 1, Building 10, Moscow 117997, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nikolay F.","family":"Myasoedov","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lyudmila A.","family":"Andreeva","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Svetlana A.","family":"Limborska","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lyudmila V.","family":"Dergunova","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of National Research Center \u201cKurchatov Institute\u201d, Kurchatov Sq. 2, Moscow 123182, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S0928-4680(02)00018-4","article-title":"Glyproline peptide family: Review on bioactivity and possible origins","volume":"8","author":"Samonina","year":"2002","journal-title":"Pathophysiology"},{"key":"ref_2","first-page":"119","article-title":"The simplest proline-containing peptides PG, GP, PGP, and GPGG: Regulatory activity and possible sources of biosynthesis","volume":"63","author":"Ashmarin","year":"1998","journal-title":"Biochemistry"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/1465-9921-10-38","article-title":"N-alpha-PGP and PGP, potential biomarkers and therapeutic targets for COPD","volume":"10","author":"Jackson","year":"2009","journal-title":"Respir. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5662","DOI":"10.4049\/jimmunol.180.8.5662","article-title":"A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation","volume":"180","author":"Gaggar","year":"2008","journal-title":"J. Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1002\/biof.1554","article-title":"Proline-containing peptides-New insight and implications: A Review","volume":"45","author":"Misiura","year":"2019","journal-title":"Biofactors"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.pathophys.2004.10.001","article-title":"Natural and hybrid (\u201cchimeric\u201d) stable regulatory glyproline peptides","volume":"11","author":"Ashmarin","year":"2005","journal-title":"Pathophysiology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1134\/S1819712407030014","article-title":"Glyprolines in regulatory tripeptides","volume":"1","author":"Ashmarin","year":"2007","journal-title":"Neurochem. J."},{"key":"ref_8","first-page":"420","article-title":"V [A nootropic adrenocorticotropin analog 4-10-semax (l5 years experience in its design and study)]","volume":"47","author":"Asmarin","year":"1997","journal-title":"Zh. Vyssh. Nerv. Deiat. Im. I P Pavlova"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S0166-4328(97)86050-0","article-title":"Neuropeptides in learning and memory processes","volume":"83","year":"1997","journal-title":"Behav. Brain Res."},{"key":"ref_10","first-page":"104","article-title":"Increased resistance to hypoxia effected by the neuropeptide preparation SEMAX","volume":"18","author":"Kaplan","year":"1992","journal-title":"Fiziol. Cheloveka"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1007\/s10517-007-0192-x","article-title":"Effects of semax and its Pro-Gly-Pro fragment on calcium homeostasis of neurons and their survival under conditions of glutamate toxicity","volume":"143","author":"Storozhevykh","year":"2007","journal-title":"Bull. Exp. Biol. Med."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1134\/S0012496616030066","article-title":"Semax prevents learning and memory inhibition by heavy metals","volume":"468","author":"Inozemtsev","year":"2016","journal-title":"Dokl. Biol. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/S0006-8993(00)03324-2","article-title":"Novel synthetic analogue of ACTH 4\u201310 (Semax) but not glycine prevents the enhanced nitric oxide generation in cerebral cortex of rats with incomplete global ischemia","volume":"894","author":"Bashkatova","year":"2001","journal-title":"Brain Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.jinorgbio.2014.09.008","article-title":"Semax, an ACTH4\u201310 peptide analog with high affinity for copper(II) ion and protective ability against metal induced cell toxicity","volume":"142","author":"Giuffrida","year":"2015","journal-title":"J. Inorg. Biochem."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Filippenkov, I.B., Stavchansky, V.V., Denisova, A.E., Yuzhakov, V.V., Sevan\u2019kaeva, L.E., Sudarkina, O.Y., Dmitrieva, V.G., Gubsky, L.V., Myasoedov, N.F., and Limborska, S.A. (2020). Novel insights into the protective properties of acth(4\u20137)pgp (semax) peptide at the transcriptome level following cerebral ischaemia\u2013 reperfusion in rats. Genes, 11.","DOI":"10.3390\/genes11060681"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1134\/S0026893321010040","article-title":"The Peptide Drug ACTH(4\u20137)PGP (Semax) Suppresses mRNA Transcripts Encoding Proinflammatory Mediators Induced by Reversible Ischemia of the Rat Brain","volume":"55","author":"Dergunova","year":"2021","journal-title":"Mol. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Sudarkina, O.Y., Filippenkov, I.B., Stavchansky, V.V., Denisova, A.E., Yuzhakov, V.V., Sevan\u2019kaeva, L.E., Valieva, L.V., Remizova, J.A., Dmitrieva, V.G., and Gubsky, L.V. (2021). Brain Protein Expression Profile Confirms the Protective Effect of the ACTH(4\u20137)PGP Peptide (Semax) in a Rat Model of Cerebral Ischemia\u2013Reperfusion. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22126179"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1007\/s12031-012-9853-y","article-title":"Effect of semax and its C-terminal fragment Pro-Gly-Pro on the expression of VEGF family genes and their receptors in experimental focal ischemia of the rat brain","volume":"49","author":"Medvedeva","year":"2013","journal-title":"J. Mol. Neurosci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Medvedeva, E.V., Dmitrieva, V.G., Povarova, O.V., Limborska, S.A., Skvortsova, V.I., Myasoedov, N.F., and Dergunova, L.V. (2014). The peptide semax affects the expression of genes related to the immune and vascular systems in rat brain focal ischemia: Genome-wide transcriptional analysis. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-228"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1134\/S1068162006010055","article-title":"Kinetics of semax penetration into the brain and blood of rats after its intranasal administration","volume":"32","author":"Shevchenko","year":"2006","journal-title":"Russ. J. Bioorg. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1134\/S1607672908050037","article-title":"The effect of semax and the C-terminal peptide PGP on expression of growth factor genes and receptors in rats under conditions of experimental cerebral ischemia","volume":"422","author":"Dmitrieva","year":"2008","journal-title":"Dokl. Biochem. Biophys."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1134\/S0026893314020125","article-title":"Tripeptide Pro-Gly-Pro affects rat-brain transcriptome during focal ischemia","volume":"48","author":"Medvedeva","year":"2014","journal-title":"Mol. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1007\/s00438-017-1297-1","article-title":"Semax, an analog of ACTH(4\u20137), regulates expression of immune response genes during ischemic brain injury in rats","volume":"292","author":"Medvedeva","year":"2017","journal-title":"Mol. Genet. Genom."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1134\/S0012496613060124","article-title":"Leucine-containing glyprolines (Pro-Gly-Pro-Leu and Leu-Pro-Gly-Pro): Participation in hemostatic reactions in vitro and in vivo in rats with blood coagulation and lipid metabolism disorders","volume":"453","author":"Myasoedov","year":"2013","journal-title":"Dokl. Biol. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1134\/S0012496613060069","article-title":"Effect of the PRO-GLY-PRO peptide on hemostasis and lipid metabolism in rats with hypercholesterolemia","volume":"453","author":"Andreeva","year":"2013","journal-title":"Dokl. Biol. Sci."},{"key":"ref_26","first-page":"17","article-title":"Functional state of the anticoagulation system after the administration of complexes formed by natural heparin and the regulatory peptides: Pro-Gly, Pro-Gly-Pro, Semax and tuftsin","volume":"2","author":"Lyapina","year":"2008","journal-title":"Neurochem. J."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Dergunova, L.V., Filippenkov, I.B., Stavchansky, V.V., Denisova, A.E., Yuzhakov, V.V., Mozerov, S.A., Gubsky, L.V., and Limborska, S.A. (2018). Genome-wide transcriptome analysis using RNA-Seq reveals a large number of differentially expressed genes in a transient MCAO rat model. BMC Genom., 19.","DOI":"10.1186\/s12864-018-5039-5"},{"key":"ref_28","first-page":"105","article-title":"Design and Investigation of an ACTH(4-10) Analog Lacking D-Amino Acids and Hydrophobic Radicals","volume":"16","author":"Ashmarin","year":"1995","journal-title":"Neurosci. Res. Commun."},{"key":"ref_29","first-page":"15","article-title":"Investigation of mechanisms of neuro-protective effect of semax in acute period of ischemic stroke","volume":"99","author":"Miasoedova","year":"1999","journal-title":"Zhurnal Nevrol. I Psikhiatrii Im. S.S. Korsakova"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1007\/s10517-014-2684-9","article-title":"Hypoglycemic and anticoagulant effects of tetrapeptide Pro-Gly-Pro-Leu in hypercholesterolemia","volume":"158","author":"Shubina","year":"2014","journal-title":"Bull. Exp. Biol. Med."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Filippenkov, I.B., Stavchansky, V.V., Glazova, N.Y., Sebentsova, E.A., Remizova, J.A., Valieva, L.V., Levitskaya, N.G., Myasoedov, N.F., Limborska, S.A., and Dergunova, L.V. (2021). Antistress action of melanocortin derivatives associated with correction of gene expression patterns in the hippocampus of male rats following acute stress. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms221810054"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.ab.2004.09.010","article-title":"Denaturing RNA electrophoresis in TAE agarose gels","volume":"336","author":"Masek","year":"2005","journal-title":"Anal. Biochem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e36","DOI":"10.1093\/nar\/30.9.e36","article-title":"Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR","volume":"30","author":"Pfaffl","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Huang","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"15545","DOI":"10.1073\/pnas.0506580102","article-title":"Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles","volume":"102","author":"Subramanian","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"W83","DOI":"10.1093\/nar\/gkw199","article-title":"g:Profiler-a web server for functional interpretation of gene lists (2016 update)","volume":"44","author":"Reimand","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"W147","DOI":"10.1093\/nar\/gkw419","article-title":"Heatmapper: Web-enabled heat mapping for all","volume":"44","author":"Babicki","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A software Environment for integrated models of biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.pathophys.2015.11.001","article-title":"Mechanisms for glyproline protection in hypercholesterolemia","volume":"23","author":"Myasoedov","year":"2016","journal-title":"Pathophysiology"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Ceprian, M., and Fulton, D. (2019). Glial Cell AMPA Receptors in Nervous System Health, Injury and Disease. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20102450"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"33746","DOI":"10.1038\/srep33746","article-title":"Neuronal networks provide rapid neuroprotection against spreading toxicity","volume":"6","author":"Samson","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1016\/j.freeradbiomed.2013.08.166","article-title":"NOX2 deficiency ameliorates cerebral injury through reduction of complexin II-mediated glutamate excitotoxicity in experimental stroke","volume":"65","author":"Wang","year":"2013","journal-title":"Free Radic. Biol. Med."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1002\/jnr.22182","article-title":"NeuroD6 genomic signature bridging neuronal differentiation to survival via the molecular chaperone network","volume":"88","author":"Uittenbogaard","year":"2010","journal-title":"J. Neurosci. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"660342","DOI":"10.3389\/fimmu.2021.660342","article-title":"Cholinergic System and Its Therapeutic Importance in Inflammation and Autoimmunity","volume":"12","author":"Halder","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"C821","DOI":"10.1152\/ajpcell.00504.2008","article-title":"Vascular endothelial growth factor induces protein kinase D-dependent production of proinflammatory cytokines in endothelial cells","volume":"296","author":"Hao","year":"2009","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Wang, X., Bao, X., Pal, R., Agbas, A., and Michaelis, E.K. (2010). Transcriptomic responses in mouse brain exposed to chronic excess of the neurotransmitter glutamate. BMC Genom., 11.","DOI":"10.1186\/1471-2164-11-360"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/nrneurol.2016.125","article-title":"Inflammatory risk factors, biomarkers and associated therapy in ischaemic stroke","volume":"12","author":"Esenwa","year":"2016","journal-title":"Nat. Rev. Neurol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1038\/jcbfm.2012.88","article-title":"Inflammatory cytokines in experimental and human stroke","volume":"32","author":"Lambertsen","year":"2012","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1007\/s12265-013-9508-6","article-title":"Role of inflammation and its mediators in acute ischemic stroke","volume":"6","author":"Jin","year":"2013","journal-title":"J. Cardiovasc. Transl. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"8","DOI":"10.2741\/1207","article-title":"AP-1 targets in the brain","volume":"9","author":"Rylski","year":"2004","journal-title":"Front. Biosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1016\/j.neuint.2007.04.019","article-title":"Role of transcription factors in mediating post-ischemic cerebral inflammation and brain damage","volume":"50","author":"Yi","year":"2007","journal-title":"Neurochem. Int."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.it.2009.07.001","article-title":"SOCS1 and SOCS3 in the control of CNS immunity","volume":"30","author":"Baker","year":"2009","journal-title":"Trends Immunol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.neuroscience.2014.07.073","article-title":"Phosphorylation enhances recombinant HSP27 neuroprotection against focal cerebral ischemia in mice","volume":"278","author":"Shimada","year":"2014","journal-title":"Neuroscience"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"180017","DOI":"10.1183\/16000617.0017-2018","article-title":"The multifaceted roles of the matrikine Pro-Gly-Pro in pulmonary health and disease","volume":"27","author":"Patel","year":"2018","journal-title":"Eur. Respir. Rev."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1038\/nm1361","article-title":"A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation","volume":"12","author":"Weathington","year":"2006","journal-title":"Nat. Med."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.celrep.2012.08.022","article-title":"Memory deficits induced by inflammation are regulated by \u03b15-subunit-containing GABAA receptors","volume":"2","author":"Wang","year":"2012","journal-title":"Cell Rep."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1002\/glia.21087","article-title":"Astrocytes are GABAergic cells that modulate microglial activity","volume":"59","author":"Lee","year":"2011","journal-title":"Glia"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.bbrc.2010.11.098","article-title":"Identification of complexin II in astrocytes: A possible regulator of glutamate release in these cells","volume":"404","author":"Hazell","year":"2011","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Gamir-Morralla, A., L\u00f3pez-Men\u00e9ndez, C., Medina, M., and Iglesias, T. (2017). A Novel Neuroprotection Target With Distinct Regulation in Stroke and Alzheimer\u2019s Disease. Neuroprot. Alzheimer\u2019s Dis., 123\u2013147.","DOI":"10.1016\/B978-0-12-803690-7.00007-7"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e2597","DOI":"10.1002\/jmr.2597","article-title":"Synacton and individual activity of synthetic and natural corticotropins","volume":"30","author":"Vyunova","year":"2017","journal-title":"J. Mol. Recognit."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1134\/S1607672914030077","article-title":"Characteristic features of specific binding of pentapeptide HFPGP labeled at the C-terminal proline residue to rat forebrain plasma membranes","volume":"456","author":"Vyunova","year":"2014","journal-title":"Dokl. Biochem. Biophys."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1134\/S0012496608020075","article-title":"Binding of tripeptide Pro-Gly-Pro labeled at the C-terminal proline residue to plasma membranes of the rat forebrain","volume":"419","author":"Andreeva","year":"2008","journal-title":"Dokl. Biol. Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1002\/med.21704","article-title":"Pharmacotranscriptomics of peptide drugs with neuroprotective properties","volume":"41","author":"Dergunova","year":"2021","journal-title":"Med. Res. Rev."},{"key":"ref_65","first-page":"53","article-title":"The Non-receptor Tyrosine Kinase Pyk2 in Brain Function and Neurological and Psychiatric Diseases","volume":"13","author":"Mendes","year":"2021","journal-title":"Front. Synaptic Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1134\/S1607672914030090","article-title":"Comparison of pharmacokinetics and metabolism of Pro-Gly-Pro-Leu administered intranasally and intravenously in the blood and brain of rats","volume":"456","author":"Shevchenko","year":"2014","journal-title":"Dokl. Biochem. Biophys."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1134\/S1068162013030151","article-title":"Proteolysis of simple glyprolines by leucine aminopeptidase and enzymes from nasal mucus, brain membranes, and blood of rats","volume":"39","author":"Shevchenko","year":"2013","journal-title":"Russ. J. Bioorg. Chem."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1002\/jlcr.3785","article-title":"An integrated approach to study the molecular aspects of regulatory peptides biological mechanism","volume":"62","author":"Vyunova","year":"2019","journal-title":"J. Labelled Comp. Radiopharm."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1038\/jcbfm.2009.240","article-title":"Role of chemokines in CNS health and pathology: A focus on the CCL2\/CCR2 and CXCL8\/CXCR2 networks","volume":"30","author":"Semple","year":"2010","journal-title":"J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.jneuroim.2008.04.022","article-title":"Chemokines and neuromodulation","volume":"198","year":"2008","journal-title":"J. Neuroimmunol."},{"key":"ref_71","unstructured":"(2018, September 18). National Center for Biotechnology Information, Available online: https:\/\/www.ncbi.nlm.nih.gov\/sra\/PRJNA491404."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/13\/12\/2380\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:42:48Z","timestamp":1760146968000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/13\/12\/2380"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,16]]},"references-count":71,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["genes13122380"],"URL":"https:\/\/doi.org\/10.3390\/genes13122380","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,16]]}}}