Glyprolines: Regulatory peptides with an integrative action
DOI:
https://doi.org/10.33910/2687-1270-2020-1-4-303-316Keywords:
glyprolines, inflammation, regeneration, gastroprotective effect, neuroprotective effect, hypolipidemic effect, normoglycemic effectAbstract
Glyprolines (short proline and glycine containing peptides) are a new type of regulatory peptides. They are of interest to both fundamental physiology and medicine (possible use for medical purposes). The main advantages of glyprolines are their relative resistance to biodegradation and the integrative effect on human body. Initially, the amino acid sequence Pro-Gly-Pro (PGP) was used to increase the stability of an in vivo unstable peptide such as adrenocorticotropic hormone. The study of the intrinsic properties of PGP, as well as its possible metabolites — GP and PG — showed that all the three peptides have a wide range of physiological effects. Recently, biological activity has also been demonstrated for N-acetylated PGP, cyclic prolyl-hydroxyproline, cycloprolylglycine, di-, tri- and tetrapeptides containing proline and glycine with additional inclusion of arginine or leucine in various positions, as well as for the N-terminal fragment of the insulin-like growth factor-1 — Gly-Pro-Glu. The obtained data allowed classifying short proline and glycine containing peptides into a separate class of regulatory peptides — glyprolines. Endogenous PGP and cycloprolylglycine have been found. Collagen and insulin-like growth factor-1, respectively, are considered the most likely sources of these peptides in human body. Glyprolines have a neuroprotective effect, protect the gastric mucosa from damage, regulate inflammation and regeneration processes, have a positive effect on hemostasis, and exhibit hypolipidemic and normoglycemic effects. The article discusses the physiological effects of glyprolines, their possible endogenous and exogenous sources, mechanisms of action, and prospects for use in medicine.
References
ЛИТЕРАТУРА
Абдуллина, А. А., Васильева, Е. В., Кондрахин, Е. А., Ковалев, Г. И. (2019) Участие серотониновых, глутаматных и ГАМК-рецепторов в проявлении антидепрессивноподобного эффекта циклопролилглицина. Нейрохимия, т. 36, № 3, с. 218–225. DOI: 10.1134/S1027813319030026
Абдуллина, А. А., Васильева, Е. В., Кудрин, В. С. и др. (2020) Влияние циклопролилглицина и его аналогов на моноаминергические системы мозга мышей BALB/c. Фармакокинетика и фармакодинамика, № 1, с. 3–10. DOI: 10.37489/2587-7836-2020-1-3-10
Ашмарин, И. П., Бакаева, З. В., Васьковский, Б. В. и др. (2003) Высокостабильные регуляторные олигопептиды: опыт и перспективы применения. Патологическая физиология и экспериментальная терапия, № 4, с. 2–5.
Ашмарин, И. П., Каразеева, Е. П., Ляпина, С. А., Самонина, Г. Е. (1998) Регуляторная активность простейших пролинсодержащих пептидов PG, GP, PGP, GPGG и возможные источники их биосинтеза. Биохимия, т. 63, № 2, с. 149–155.
Ашмарин, И. П., Ляпина, Л. А., Пасторова, В. Е. (1996) Модуляция гемостатических реакций in vitro и in vivo представителями семейств регуляторных пептидов. Вестник Российской академии медицинских наук, № 6, с. 50–57.
Ашмарин, И. П., Незавибатько, В. Н., Мясоедов, Н. Ф. и др. (1997) Ноотропный аналог адренокортикотропина 4-10-семакс (15-летний опыт разработки и изучения). Журнал высшей нервной деятельности им. И. П. Павлова, т. 47, № 2, с. 420–430.
Бойко, С. С., Жердев, В. П., Шевченко, Р. В. (2018) Фармакокинетика ноопепта и его активного метаболита циклопролилглицина у крыс. Биомедицинская химия, т. 64, № 5, с. 455–458. DOI: 10.18097/PBMC20186405455
Жуйкова, С. Е., Бадмаева, К. Е., Бакаева, З. В. и др. (2004) Противоязвенные эффекты трипептида PGP и его возможных метаболитов — PG, GP, глицина и пролина — на разных моделях вызова язв у крыс. Известия РАН. Серия биологическая, № 5, с. 585–588.
Жуйкова, С. Е., Бадмаева, K. E., Самонина, Г. Е., Плесская, Л. Г. (2003a) Семакс и некоторые глипролиновые пептиды ускоряют заживление ацетатных язв у крыс. Экспериментальная и клиническая гастроэнтерология, № 4, с. 88–92.
Жуйкова, С. Е., Бакаева, З. В., Самонина, Г. Е. (2003b) Дифференцированные противоязвенные эффекты возможных метаболитов пептида PGP — PG и GP — на этаноловой и стрессорной моделях вызова язв у крыс. Вестник Московского университета. Серия 16. Биология, № 2, с. 20–22.
Жуйкова, С. Е., Хропычева, Р. П., Золотарев, В. А., Поленов, С. А. (2003c) Новые пептидные регуляторы желудочной секреции крыс (амилин, PGP, семакс). Экспериментальная и клиническая гастроэнтерология, № 2, с. 86–90.
Ковалев, Г. И., Абдуллина, А. А., Васильева, Е. В. и др. (2018) Антидепрессантоподобные свойства циклопролилглицина. Экспериментальная и клиническая фармакология, т. 81, № 11, с. 3–6. DOI: 10.30906/0869-2092-2018-81-11-3-6
Колясникова, К. Н., Гудашева, Т. А., Назарова, Г. А. и др. (2012) Сходство цикло-пролилглицина с пирацетамом по антигипоксическому и нейропротекторному эффектам. Экспериментальная и клиническая фармакология, т. 75, № 9, с. 3–6. DOI: 10.30906/0869-2092-2012-75-9-3-6
Кузник, Б. И., Давыдов, С. О., Поправка, Е. С. и др. (2019) Эпигенетические механизмы пептидной регуляции и нейропротекторный белок Fkbp1b. Молекулярная биология, т. 53, № 2, с. 339–348. DOI: 10.1134/S0026898419020095
Куренкова, А. Д., Умарова, Б. А., Гаврилова, С. А. (2016) Влияние пролил-глицил-пролина (PGP) и его ацетилированной формы (N-ACPGP) на проницаемость сосудов кожи крыс. Российский физиологический журнал им. И. М. Сеченова, т. 102, № 9, с. 1111–1119.
Ляпина, Л. А., Мясоедов, Н. Ф., Григорьева, М. Е. и др. (2013) Современная концепция регуляторной роли пептидов семейства глипролинов в коррекции функции системы гемостаза при развитии сахарного диабета. Известия РАН. Серия биологическая, № 4, с. 453–462. DOI: 10.7868/S0002332913040103
Мясоедов, Н. Ф., Шубина, Т. А., Оберган, Т. Ю. и др. (2013) Гипохолестеринемическое действие регуляторного пептида Pro-Gly-Pro-Leu. Вопросы питания, т. 82, № 5, с. 41–45.
Самонина, Г. Е., Копылова, Г. Н., Сергеев, В. И. и др. (2001) Коррекция желудочного кровотока как один из возможных механизмов противоязвенных эффектов коротких пролинсодержащих пептидов. Российский физиологический журнал им. И. М. Сеченова, т. 87, № 11, с. 1488–1492.
Хавинсон, В. Х. (2020) Лекарственные пептидные препараты: прошлое, настоящее, будущее. Клиническая медицина, т. 98, № 3, с. 165–177. DOI: 10.30629/0023-2149-2020-98-3-165-177
Шабалина, А. А., Ляпина, Л. А., Рочев, Д. Л. и др. (2015) Гиполипидемические и фибриндеполимеризационные эффекты регуляторных лейцинсодержащих глипролинов в крови человека in vitro. Известия РАН. Серия биологическая, № 1, с. 85–89. DOI: 10.7868/S0002332915010129
Шевченко, К. В., Нагаев, И. Ю., Андреева, Л. А. и др. (2019) Устойчивость пролинсодержащих пептидов в биологических средах. Биомедицинская химия, т. 65, № 3, с. 180–201. DOI: 10.18097/PBMC20196503180
Badmaeva, S. E., Kopylova, G. N., Abushinova, N. N. et al. (2006) Effects of glyprolines on stress-induced behavioral disorders in rats. Neuroscience and Behavioral Physiology, vol. 36, no. 4, pp. 409–413. DOI: 10.1007/s11055- 006-0032-x
Bakaeva, Z. V., Sangadzhieva, A. D., Tani, S. et al. (2016) Glyprolines exert protective and repair-promoting effects in the rat stomach: Potential role of the cytokine GRO/CINC-1. Journal of Physiology and Pharmacology, vol. 67, no. 2, pp. 253–260.
Bakaeva, Z. V., Surin, A. M., Lizunova, N. V. et al. (2020) Neuroprotective potential of peptides HFRWPGP (ACTH 6-9 PGP), KKRRPGP, and PyrRP in cultured cortical neurons at glutamate excitotoxicity. Doklady Biochemistry and Biophysics, vol. 491, no. 1, pp. 62–69. DOI: 10.1134/S1607672920020040
Bondarenko, N. S., Shneiderman, A. N., Guseva, A. A., Umarova, B. A. (2017) Prolyl-glycyl-proline (PGP) peptide prevents an increase in vascular permeability in inflammation. Acta Naturae, vol. 9, no. 1, pp. 52–55. DOI: 10.32607/20758251-2017-9-1-52-55
Braber, S., Overbeek, S. A., Koelink, P. J. et al. (2011) CXCR2 antagonists block the N-Ac-PGP-induced neutrophil influx in the airways of mice, but not the production of the chemokine CXCL1. European Journal of Pharmacology, vol. 668, no. 3, pp. 443–449. DOI: 10.1016/j.ejphar.2011.03.025
Chen, B., Luo, M., Liang, J. et al. (2018) Surface modification of PGP for a neutrophil-nanoparticle co-vehicle to enhance the anti-depressant effect of baicalein. Acta Pharmaceutica Sinica B, vol. 8, no. 1, pp. 64–73. DOI: 10.1016/j. apsb.2017.11.012
Edeeva, S. E., Kopylova, G. N., Bakaeva, Z. V. et al. (2008) Protective and therapeutic effects of glyprolines in psychoemotional stress induced by cholecystokinin-4 injection. Bulletin of Experimental Biology and Medicine, vol. 145, no. 3, article 302. DOI: 10.1007/s10517-008-0076-8
Falalyeyeva, T. M., Samonina, G. E., Beregovaya, T. V. et al. (2010) Effect of glyprolines PGP, GP, and PG on homeostasis of gastric mucosa in rats with experimental ethanol-induced gastric ulcers. Bulletin of Experimental Biology and Medicine, vol. 149, no. 6, pp. 699–701. DOI: 10.1007/s10517-010-1028-7
Fleishman, M. Yu., Tolstenok, I. V., Lebed’ko, O. A. et al. (2015) Effects of glyprolines on DNA synthesis and free radical oxidation in mouse gastric mucosa under physiological conditions and during therapy with oral non-steroid anti-inflammatory drugs. Bulletin of Experimental Biology and Medicine, vol. 159, no. 4, pp. 502–504. DOI: 10.1007/s10517-015-3003-9
Grigorjeva, M. E., Kazancheva, M. Kh., Lyapina, L. A. (2013) Anticoagulant effects of arginine-containing peptide Arg-Pro-Gly-Pro under conditions of immobilization stress. Bulletin of Experimental Biology and Medicine, vol. 154, no. 6, pp. 723–727. DOI: 10.1007/s10517-013-2039-y
Guan, J., Gluckman, P., Yang, P. et al. (2014) Cyclic glycine-proline regulates IGF-1 homeostasis by altering the binding of IGFBP-3 to IGF-1. Scientific Reports, vol. 4, article 4388. DOI: 10.1038/srep04388
Guan, J., Mathai, S., Liang, H.-p., Gunn, A. J. (2013) Insulin-like growth factor-1 and its derivatives: Potential pharmaceutical application for treating neurological conditions. Recent Patents on CNS Drug Discovery, vol. 8, no. 2, pp. 142–160. DOI: 10.2174/1574889811308020004
Gudasheva, T. A., Boyko, S. S., Akparov, V. Kh. et al. (1996) Identification of a novel endogenous memory facilitating cyclic dipeptide cyclo-prolylglycine in rat brain. FEBS Letters, vol. 391, no. 1–2, pp. 149–152. DOI: 10.1016/0014-5793(96)00722-3
Gudasheva, T. A., Grigoriev, V. V., Koliasnikova, K. N. et al. (2016a) Neuropeptide cycloprolylglycine is an endogenous positive modulator of AMPA receptors. Doklady Biochemistry and Biophysics, vol. 471, no. 1, pp. 387–389. DOI: 10.1134/S160767291606003X
Gudasheva, T. A., Koliasnikova, K. N., Antipova, T. A., Seredenin, S. B. (2016b) Neuropeptide cycloprolylglycine increases the levels of brain-derived neurotrophic factor in neuronal cells. Doklady Biochemistry and Biophysics, vol. 469, no. 1, pp. 273–276. DOI: 10.1134/S1607672916040104
Hill, J. W., Nemoto, E. M. (2015) Matrix-derived inflammatory mediator N-acetyl proline-glycine-proline is neurotoxic and upregulated in brain after ischemic stroke. Journal of Neuroinflammation, vol. 12, article 214. DOI: 10.1186/s12974-015-0428-z
Ichikawa, S., Morifuji, M., Ohara, H. et al. (2010) Hydroxyproline-containing dipeptides and tripeptides quantified at high concentration in human blood after oral administration of gelatin hydrolysate. International Journal of Food Sciences and Nutrition, vol. 61, no. 1, pp. 52–60. DOI: 10.3109/09637480903257711
Jia, X., Gharibyan, A. L., Öhman, A. et al. (2011) Neuroprotective and nootropic drug noopept rescues α-synuclein amyloid cytotoxicity. Journal of Molecular Biology, vol. 414, no. 5, pp. 699–712. DOI: 10.1016/j.jmb.2011.09.044
Kim, S. D., Lee, H. Y., Shim, J. W. et al. (2011) Activation of CXCR2 by extracellular matrix degradation product acetylated Pro-Gly-Pro has therapeutic effects against sepsis. American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 2, pp. 243–251. DOI: 10.1164/rccm.201101-0004OC
Koroleva, S. V., Ashmarin, I. P. (2002) Functional continuum of regulatory peptides (RPs): Vector model of RP-effects representation. Journal of Theoretical Biology, vol. 216, no. 3, pp. 257–271. DOI: 10.1006/jtbi.2002.2555
Kruijf, P., Lim, H. D., Overbeek, S. A. et al. (2010) The collagen-breakdown product N-acetyl-Proline-Glycine- Proline (N-α-PGP) does not interact directly with human CXCR1 and CXCR2. European Journal of Pharmacology, vol. 643, no. 1, pp. 29–33. DOI: 10.1016/j.ejphar.2010.06.017
Kwon, Y. W., Heo, S. C., Lee, T. W. et al. (2017) N-acetylated proline-glycine-proline accelerates cutaneous wound healing and neovascularization by human endothelial progenitor cells. Scientific Reports, vol. 7, article 43057. DOI: 10.1038/srep43057
Kwon, Y. W., Lee, S. J., Heo, S. C. et al. (2019) Role of CXCR2 in the ac-PGP-induced mobilization of circulating angiogenic cells and its therapeutic implications. Stem Cells Translational Medicine Journal, vol. 8, no. 3, pp. 236–246. DOI: 10.1002/sctm.18-0035
Ma, Y., Kleinbeck, K., Kao, W. J. (2011) Extracellular matrix-derived tripeptide proline-glycine-proline inhibits keratinocyte proliferation and migration. Wound Repair and Regeneration, vol. 19, no. 6, pp. 718–726. DOI: 10.1111/j.1524-475X.2011.00734.x
Marinelli, L., Fornasari, E., Di Stefano, A. D. et al. (2019) Synthesis and biological evaluation of novel analogues of Gly-l-Pro-l-Glu (GPE) as neuroprotective agents. Bioorganic & Medicinal Chemistry Letters, vol. 29, no. 2, pp. 194–198. DOI: 10.1016/j.bmcl.2018.11.057
O’Reilly, P., Jackson, P. L., Noerager, B. et al. (2009) N-alpha-PGP and PGP, potential biomarkers and therapeutic targets for COPD. Respiratory Research, vol. 10, article 38. DOI: 10.1186/1465-9921-10-38
Overbeek, S. A., Henricks, P. A. J., Srienc, A. I. et al. (2011) N-acetylated Proline-Glycine-Proline induced G-protein dependent chemotaxis of neutrophils is independent of CXCL8 release. European Journal of Pharmacology, vol. 668, no. 3, pp. 428–434. DOI: 10.1016/j.ejphar.2011.03.022
Pastorova, V. E., Lyapina, L. A., Ashmarin, I. P. (2003) Prevention of thrombus formation with glyprolines on various models of prethrombotic state and thrombosis in rats. Bulletin of Experimental Biology and Medicine, vol. 136, no. 4, pp. 319–322. DOI: 10.1023/b:bebm.0000010940.80757.90
Pfister, R. R., Haddox, J. L., Sommers, C. I. (1998) Injection of chemoattractants into normal cornea: A model of inflammation after alkali injury. Investigative Ophthalmology & Visual Science, vol. 39, no. 9, pp. 1744–1750. PMID: 9699566.
Pfister, R. R., Haddox, J. L., Sommers, C. I., Lam, K. W. (1995) Identification and synthesis of chemotactic tripeptides from alkali-degraded whole cornea. A study of N-acetyl-proline-glycine-proline and N-methyl-proline-glycine-proline. Investigative Ophthalmology & Visual Science, vol. 36, no. 7, pp. 1306–1316. PMID: 7775108.
Roda, M. A., Xu, X., Abdalla, T. H. et al. (2019) Proline-glycine-proline peptides are critical in the development of smoke-induced emphysema. American Journal of Respiratory Cell and Molecular Biology, vol. 61, no. 5, pp. 560–566. DOI: 10.1165/rcmb.2018-0216OC
Samonina, G., Lyapina, L., Kopylova, G. et al. (2000) Protection of gastric mucosal integrity by gelatin and simple proline-containing peptides. Pathophysiology, vol. 7, no. 1, pp. 69–73. DOI: 10.1016/s0928-4680(00)00045-6
Saura, J., Curatolo, L., Williams, C. E. et al. (1999) Neuroprotective effects of Gly-Pro-Glu, the N-terminal tripeptide of IGF-1, in the hippocampus in vitro. NeuroReport, vol. 10, no. 1, pp. 161–164. DOI: 10.1097/00001756-199901180-00031
Seredenin, S. B., Gudasheva, T. A., Boiko, S. S. et al. (2002) Endogenous dipeptide cycloprolylglycine shows selective anxiolytic activity in animals with manifest fear reaction. Bulletin of Experimental Biology and Medicine, vol. 133, no. 4, pp. 360–362. DOI: 10.1023/A:1016293904149
Shigemura, Y., Iwasaki, Y., Tateno, M. et al. (2018) A pilot study for the detection of cyclic prolyl-hydroxyproline (Pro-Hyp) in human blood after ingestion of collagen hydrolysate. Clinical Trial Nutrients, vol. 10, no. 10, article 1356. DOI: 10.3390/nu10101356
Sikiric, P., Seiwerth, S., Rucman, R. et al. (2016) Brain-gut axis and pentadecapeptide BPC 157: Theoretical and practical implications. Current Neuropharmacology, vol. 14, no. 8, pp. 857–865. DOI: 10.2174/1570159X13666160502153022
Snelgrove, R. J., Jackson, P. L., Hardison, M. T. et al. (2010) A critical role for LTA4H in limiting chronic pulmonary neutrophilic inflammation. Science, vol. 330, no. 6000, pp. 90–94. DOI: 10.1126/science.1190594
Umarova, B. A., Kopylova, G. N., Smirnova, E. A. et al. (2003) Secretory activity of mast cell during stress: Effect of prolyl-glycyl-proline and Semax. Bulletin of Experimental Biology and Medicine, vol. 136, no. 4, pp. 325–327. DOI: 10.1023/b:bebm.0000010942.14275.50
van Houwelingen, A. H., Weathington, N. M., Verweij, V. et al. (2008) Induction of lung emphysema is prevented by L-arginine-threonine-arginine. The FASEB Journal, vol. 22, no. 9, pp. 3403–3408. DOI: 10.1096/fj.07-096230
Wells, J. M., Gaggar, A., Blalock, J. E. (2015) MMP generated matrikines. Matrix Biology, vol. 44–46, pp. 122–129. DOI: 10.1016/j.matbio.2015.01.016
Zolotarev, Yu. A., Zhuikova, S. E., Ashmarin, I. P. et al. (2003) Metabolism of PGP peptide after administration via different routes. Bulletin of Experimental Biology and Medicine, vol. 135, no. 4, pp. 361–364. DOI: 10.1023/a:1024612831380
REFERENCES
Abdullina, A. A., Vasilyeva, E. V., Kondrakhin, E. A., Kovalev, G. I. (2019) Uchastie serotoninovykh, glutamatnykh i GAMK-retseptorov v proyavlenii antidepressivnopodobnogo effekta tsikloprolilglitsina [Participation of serotonin, glutamate, and GABA receptors in the manifestation of the antidepressant-like effect of cycloprolylglycine]. Nejrokhimiya — Neurochemical Journal, vol. 36, no. 3, pp. 218–225. DOI: 10.1134/ S1027813319030026 (In Russian)
Abdullina, A. A., Vasileva, E. V., Kudrin, V. P. et al. (2020) Vliyanie tsikloprolilglitsina i ego analogov na monoaminergicheskie sistemy mozga myshej BALB/c [The effects of cycloprolylglycine and its analogues on brain monoaminergic systems in BALB/c mice]. Farmakokinetika i farmakodinamika — Pharmacokinetics and Pharmacodynamics, no. 1, pp. 3–10. DOI: 10.37489/2587-7836-2020-1-3-10 (In Russian)
Ashmarin, I. P., Bakaeva, Z. V., Vaskovskij, B. V. et al. (2003) Vysokostabil’nye regulyatornye oligopeptidy: opyt i perspektivy primeneniya [Highly stable regulatory oligopeptides: Experience and application prospects]. Patologicheskaya fiziologiya i eksperimetalnaya terapiya — Pathological Physiology and Experimental Therapy, no. 4, pp. 2–5. (In Russian)
Ashmarin, I. P., Karazeeva, E. P., Lyapina, P. A., Samorina, G. E. (1998) Regulyatornaya aktivnost’ prostejshikh prolinsoderzhashchikh peptidov PG, GP, PGP, GPGG i vozmozhnye istochniki ikh biosinteza [The simplest proline containing peptides PG, GP, PGP AND GPGG as putative bioregulators and possible sources of their synthesis]. Biokhimiya — Biochemistry (Moscow), vol. 63, no. 2, pp. 149–155. (In Russian)
Ashmarin, I. P., Lyapina, L. A., Pastorova, V. E. (1996) Modulyatsiya gemostaticheskikh reaktsij in vitro i in vivo predstavitelyami semejstv regulyatornykh peptidov [Modulation of hemostatic reactions in vitro and in vivo by representatives of the families of regulatory peptides]. Vestnik Rossijskoj akademii meditsinskikh nauk — Annals of the Russian Academy of Medical Sciences, no. 6, pp. 50–57. (In Russian)
Ashmarin, I. P., Nezavibat’ko, V. N., Miasoedov, N. F. et al. (1997) Nootropnyj analog adrenokortikotropina 4-10-semaks (15-letnij opyt razrabotki i izucheniya) [A nootropic adrenocorticotropin analog 4-10-semax (l5 years experience in its design and study)]. Zhurnal vysshej nervnoj deyatel’nosti im. I. P. Pavlova — I. P. Pavlov Journal of Higher Nervous Activity, vol. 47, no. 2, pp. 420–430. (In Russian)
Badmaeva, S. E., Kopylova, G. N., Abushinova, N. N. et al. (2006) Effects of glyprolines on stress-induced behavioral disorders in rats. Neuroscience and Behavioral Physiology, vol. 36, no. 4, pp. 409–413. DOI: 10.1007/s11055-006-0032-x (In English)
Bakaeva, Z. V., Sangadzhieva, A. D., Tani, S. et al. (2016) Glyprolines exert protective and repair-promoting effects in the rat stomach: Potential role of the cytokine GRO/CINC-1. Journal of Physiology and Pharmacology, vol. 67, no. 2, pp. 253–260. (In English)
Bakaeva, Z. V., Surin, A. M., Lizunova, N. V. et al. (2020) Neuroprotective potential of peptides HFRWPGP (ACTH 6-9 PGP), KKRRPGP, and PyrRP in cultured cortical neurons at glutamate excitotoxicity. Doklady Biochemistry and Biophysics, vol. 491, no. 1, pp. 62–69. DOI: 10.1134/S1607672920020040 (In English)
Boyko, S. S., Zherdev, V. P., Shevchenko, R. V. (2018) Farmakokinetika noopepta i ego aktivnogo metabolita tsikloprolilglitsina u krys [Pharmacokinetics of noopept and its active metabolite cycloprolyl glycine in rats]. Biomeditsinskaya khimiya, vol. 64, no. 5, pp. 455–458. DOI: 10.18097/PBMC20186405455 (In Russian)
Bondarenko, N. S., Shneiderman, A. N., Guseva, A. A., Umarova, B. A. (2017) Prolyl-glycyl-proline (PGP) peptide prevents an increase in vascular permeability in inflammation. Acta Naturae, vol. 9, no. 1, pp. 52–55. DOI: 10.32607/20758251-2017-9-1-52-55 (In English)
Braber, S., Overbeek, S. A., Koelink, P. J. et al. (2011) CXCR2 antagonists block the N-Ac-PGP-induced neutrophil influx in the airways of mice, but not the production of the chemokine CXCL1. European Journal of Pharmacology, vol. 668, no. 3, pp. 443–449. DOI: 10.1016/j.ejphar.2011.03.025 (In English)
Chen, B., Luo, M., Liang, J. et al. (2018) Surface modification of PGP for a neutrophil-nanoparticle co-vehicle to enhance the anti-depressant effect of baicalein. Acta Pharmaceutica Sinica B, vol. 8, no. 1, pp. 64–73. DOI: 10.1016/j.apsb.2017.11.012 (In English)
Edeeva, S. E., Kopylova, G. N., Bakaeva, Z. V. et al. (2008) Protective and therapeutic effects of glyprolines in psychoemotional stress induced by cholecystokinin-4 injection. Bulletin of Experimental Biology and Medicine, vol. 145, no. 3, article 302. DOI: 10.1007/s10517-008-0076-8 (In English)
Falalyeyeva, T. M., Samonina, G. E., Beregovaya, T. V. et al. (2010) Effect of glyprolines PGP, GP, and PG on homeostasis of gastric mucosa in rats with experimental ethanol-induced gastric ulcers. Bulletin of Experimental Biology and Medicine, vol. 149, no. 6, pp. 699–701. DOI: 10.1007/s10517-010-1028-7 (In English)
Fleishman, M. Yu., Tolstenok, I. V., Lebed’ko, O. A. et al. (2015) Effects of glyprolines on DNA synthesis and free radical oxidation in mouse gastric mucosa under physiological conditions and during therapy with oral non-steroid anti-inflammatory drugs. Bulletin of Experimental Biology and Medicine, vol. 159, no. 4, pp. 502–504. DOI: 10.1007/s10517-015-3003-9 (In English)
Grigorjeva, M. E., Kazancheva, M. Kh., Lyapina, L. A. (2013) Anticoagulant effects of arginine-containing peptide Arg-Pro-Gly-Pro under conditions of immobilization stress. Bulletin of Experimental Biology and Medicine, vol. 154, no. 6, pp. 723–727. DOI: 10.1007/s10517-013-2039-y (In English)
Guan, J., Gluckman, P., Yang, P. et al. (2014) Cyclic glycine-proline regulates IGF-1 homeostasis by altering the binding of IGFBP-3 to IGF-1. Scientific Reports, vol. 4, article 4388. DOI: 10.1038/srep04388 (In English)
Guan, J., Mathai, S., Liang, H.-p., Gunn, A. J. (2013) Insulin-like growth factor-1 and its derivatives: Potential pharmaceutical application for treating neurological conditions. Recent Patents on CNS Drug Discovery, vol. 8, no. 2, pp. 142–160. DOI: 10.2174/1574889811308020004 (In English)
Gudasheva, T. A., Boyko, S. S., Akparov, V. Kh. et al. (1996) Identification of a novel endogenous memory facilitating cyclic dipeptide cyclo-prolylglycine in rat brain. FEBS Letters, vol. 391, no. 1–2, pp. 149–152. DOI: 10.1016/0014-5793(96)00722-3 (In English)
Gudasheva, T. A., Grigoriev, V. V., Koliasnikova, K. N. et al. (2016a) Neuropeptide cycloprolylglycine is an endogenous positive modulator of AMPA receptors. Doklady Biochemistry and Biophysics, vol. 471, no. 1, pp. 387–389. DOI: 10.1134/S160767291606003X (In English)
Gudasheva, T. A., Koliasnikova, K. N., Antipova, T. A., Seredenin, S. B. (2016b) Neuropeptide cycloprolylglycine increases the levels of brain-derived neurotrophic factor in neuronal cells. Doklady Biochemistry and Biophysics, vol. 469, no. 1, pp. 273–276. DOI: 10.1134/S1607672916040104 (In English)
Hill, J. W., Nemoto, E. M. (2015) Matrix-derived inflammatory mediator N-acetyl proline-glycine-proline is neurotoxic and upregulated in brain after ischemic stroke. Journal of Neuroinflammation, vol. 12, article 214. DOI: 10.1186/s12974-015-0428-z (In English)
Ichikawa, S., Morifuji, M., Ohara, H. et al. (2010) Hydroxyproline-containing dipeptides and tripeptides quantified at high concentration in human blood after oral administration of gelatin hydrolysate. International Journal of Food Sciences and Nutrition, vol. 61, no. 1, pp. 52–60. DOI: 10.3109/09637480903257711 (In English)
Jia, X., Gharibyan, A. L., Öhman, A. et al. (2011) Neuroprotective and nootropic drug noopept rescues α-synuclein amyloid cytotoxicity. Journal of Molecular Biology, vol. 414, no. 5, pp. 699–712. DOI: 10.1016/j.jmb.2011.09.044 (In English)
Khavinson, V. Kh. (2020) Lekarstvennye peptidnye preparaty: proshloe, nastoyashchee, budushchee [Peptide medicines: Past, present, future]. Klinicheskaya meditsina — Clinical Medicine (Russian Journal), vol. 98, no. 3, pp. 165–177. DOI: 10.30629/0023-2149-2020-98-3-165-177 (In Russian)
Kim, S. D., Lee, H. Y., Shim, J. W. et al. (2011) Activation of CXCR2 by extracellular matrix degradation product acetylated Pro-Gly-Pro has therapeutic effects against sepsis. American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 2, pp. 243–251. DOI: 10.1164/rccm.201101-0004OC (In English)
Kolyasnikova, K. N., Gudasheva, T. A., Nazarova, G. A. et al. (2012) Skhodstvo tsiklo-prolilglitsina s piratsetamom po antigipoksicheskomu i nejroprotektornomu effektam [Similarity of cycloprolylglycine to piracetam in antihypoxic and neuroprotective effects]. Eksperimental’naya i klinicheskaya farmakologiya — Experimental and Clinical Pharmacology, vol. 75, no. 9, pp. 3–6. DOI: 10.30906/0869-2092-2012-75-9-3-6 (In Russian)
Koroleva, S. V., Ashmarin, I. P. (2002) Functional continuum of regulatory peptides (RPs): Vector model of RP-effects representation. Journal of Theoretical Biology, vol. 216, no. 3, pp. 257–271. DOI: 10.1006/jtbi.2002.2555 (In English)
Kovalev, G. I., Abdullina, A. A., Vasileva, E. V. et al. (2018) Antidepressantopodobnye svojstva tsikloprolilglitsina [Antidepressant-like properties of cycloprolylglycine]. Eksperimental’naya i klinicheskaya farmakologiya — Experimental and Clinical Pharmacology, vol. 81, no. 11, pp. 3–6. DOI: 10.30906/0869-2092-2018-81-11-3-6 (In Russian)
Kruijf, P., Lim, H. D., Overbeek, S. A. et al. (2010) The collagen-breakdown product N-acetyl-Proline-Glycine- Proline (N-α-PGP) does not interact directly with human CXCR1 and CXCR2. European Journal of Pharmacology, vol. 643, no. 1, pp. 29–33. DOI: 10.1016/j.ejphar.2010.06.017 (In English)
Kurenkova, A. D., Umarova, B. A., Gavrilova, S. A. (2016) Vliyanie prolil-glitsil-prolina (PGP) i ego atsetilirovannoj formy (N-ACPGP) na pronitsaemost’ sosudov kozhi krys [Effect of the prolyl-glycyl-proline (PGP) and its acetylated form (N-ACPGP) on vascular permeability in rat skin]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 102, no. 9, pp. 1111–1119. (In Russian)
Kuznik, B. I., Davydov, S. O., Popravka, E. S. et al. (2019) Epigeneticheskie mekhanizmy peptidnoj regulyatsii i nejroprotektornyj belok Fkbp1b [Epigenetic mechanisms of peptide-driven regulation and neuroprotective protein Fkbp1b]. Molekularnaya biologiya — Molecular Biology, vol. 53, no. 2, pp. 339–348. DOI: 10.1134/S0026898419020095 (In Russian)
Kwon, Y. W., Heo, S. C., Lee, T. W. et al. (2017) N-acetylated proline-glycine-proline accelerates cutaneous wound healing and neovascularization by human endothelial progenitor cells. Scientific Reports, vol. 7, article 43057. DOI: 10.1038/srep43057 (In English)
Kwon, Y. W., Lee, S. J., Heo, S. C. et al. (2019) Role of CXCR2 in the ac-PGP-induced mobilization of circulating angiogenic cells and its therapeutic implications. Stem Cells Translational Medicine Journal, vol. 8, no. 3, pp. 236–246. DOI: 10.1002/sctm.18-0035 (In English)
Lyapina, L. A., Myasoedov, N. F., Grigor’eva, M. E. et al. (2013) Sovremennaya kontseptsiya regulyatornoj roli peptidov semejstva gliprolinov v korrektsii funktsii sistemy gemostaza pri razvitii sakharnogo diabeta [The modern concept of the regulatory role of peptides of the glyproline family in the correction of hemostasis system function during development of diabetes mellitus]. Izvestiya Rossijskoj akademii nauk. Seriya biologicheskaya — Proceedings of the Russian Academy of Sciences. Biological Series, no. 4, pp. 453–462. DOI: 10.7868/S0002332913040103 (In Russian)
Ma, Y., Kleinbeck, K., Kao, W. J. (2011) Extracellular matrix-derived tripeptide proline-glycine-proline inhibits keratinocyte proliferation and migration. Wound Repair and Regeneration, vol. 19, no. 6, pp. 718–726. DOI: 10.1111/j.1524-475X.2011.00734.x (In English)
Marinelli, L., Fornasari, E., Di Stefano, A. D. et al. (2019) Synthesis and biological evaluation of novel analogues of Gly-l-Pro-l-Glu (GPE) as neuroprotective agents. Bioorganic & Medicinal Chemistry Letters, vol. 29, no. 2, pp. 194–198. DOI: 10.1016/j.bmcl.2018.11.057 (In English)
Myasoedov, N. F., Shubina, T. A., Obergan, T. Yu. et al. (2013) Gipokholesterinemicheskoe dejstvie regulyatornogo peptida Pro-Gly-Pro-Leu [Cholesterol-lowering effect of the regulatory peptide Pro-Gly-Pro-Leu]. Voprosy pitaniya — Problems of Nutrition, vol. 82, no. 5, pp. 41–45. (In Russian)
O’Reilly, P., Jackson, P. L., Noerager, B. et al. (2009) N-alpha-PGP and PGP, potential biomarkers and therapeutic targets for COPD. Respiratory Research, vol. 10, article 38. DOI: 10.1186/1465-9921-10-38 (In English)
Overbeek, S. A., Henricks, P. A. J., Srienc, A. I. et al. (2011) N-acetylated Proline-Glycine-Proline induced G-protein dependent chemotaxis of neutrophils is independent of CXCL8 release. European Journal of Pharmacology, vol. 668, no. 3, pp. 428–434. DOI: 10.1016/j.ejphar.2011.03.022 (In English)
Pastorova, V. E., Lyapina, L. A., Ashmarin, I. P. (2003) Prevention of thrombus formation with glyprolines on various models of prethrombotic state and thrombosis in rats. Bulletin of Experimental Biology and Medicine, vol. 136, no. 4, pp. 319–322. DOI: 10.1023/b:bebm.0000010940.80757.90 (In English)
Pfister, R. R., Haddox, J. L., Sommers, C. I. (1998) Injection of chemoattractants into normal cornea: A model of inflammation after alkali injury. Investigative Ophthalmology & Visual Science, vol. 39, no. 9, pp. 1744–1750. PMID: 9699566. (In English)
Pfister, R. R., Haddox, J. L., Sommers, C. I., Lam, K. W. (1995) Identification and synthesis of chemotactic tripeptides from alkali-degraded whole cornea. A study of N-acetyl-proline-glycine-proline and N-methyl-proline-glycine-proline. Investigative Ophthalmology & Visual Science, vol. 36, no. 7, pp. 1306–1316. PMID: 7775108. (In English)
Roda, M. A., Xu, X., Abdalla, T. H. et al. (2019) Proline-glycine-proline peptides are critical in the development of smoke-induced emphysema. American Journal of Respiratory Cell and Molecular Biology, vol. 61, no. 5, pp. 560–566. DOI: 10.1165/rcmb.2018-0216OC (In English)
Samonina, G., Lyapina, L., Kopylova, G. et al. (2000) Protection of gastric mucosal integrity by gelatin and simple proline-containing peptides. Pathophysiology, vol. 7, no. 1, pp. 69–73. DOI: 10.1016/s0928-4680(00)00045-6 (In English)
Samonina, G. E., Kopylova, G. N., Sergeev, V. I. et al. (2001) Korrektsiya zheludochnogo krovotoka kak odin iz vozmozhnykh mekhanizmov protivoyazvennykh effektov korotkikh prolinsoderzhashchikh peptidov [Correction of gastric blood flow as one of the possible mechanisms of antiulcer effects of short proline-containing peptides]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 87, no. 11, pp. 1488–1492. (In Russian)
Saura, J., Curatolo, L., Williams, C. E. et al. (1999) Neuroprotective effects of Gly-Pro-Glu, the N-terminal tripeptide of IGF-1, in the hippocampus in vitro. NeuroReport, vol. 10, no. 1, pp. 161–164. DOI: 10.1097/00001756-199901180-00031 (In English)
Seredenin, S. B., Gudasheva, T. A., Boiko, S. S. et al. (2002) Endogenous dipeptide cycloprolylglycine shows selective anxiolytic activity in animals with manifest fear reaction. Bulletin of Experimental Biology and Medicine, vol. 133, no. 4, pp. 360–362. DOI: 10.1023/A:1016293904149 (In English)
Shabalina, A. A., Lyapina, L. A., Rochev, D. L. et al. (2015) Gipolipidemicheskie i fibrindepolimerizatsionnye effekty regulyatornykh lejtsinsoderzhashchikh gliprolinov v krovi cheloveka in vitro [In vitro lipid-lowering and fibrinolytic effects of regulatory leucine-containing glyprolines in human blood]. Izvestiya Rossijskoj akademii nauk. Seriya biologicheskaya — Proceedings of the Russian Academy of Sciences. Biological Series, no. 1, pp. 85– 89. DOI: 10.7868/S0002332915010129 (In Russian)
Shevchenko, K. V., Nagaev, I. Yu., Andreeva, L. A. et al. (2019) Ustojchivost’ prolinsoderzhashchikh peptidov v biologicheskikh sredakh [Stability of prolin-containing peptides in biological media]. Biomeditsinskaya khimiya, vol. 65, no. 3, pp. 180–201. DOI: 10.18097/PBMC20196503180 (In Russian)
Shigemura, Y., Iwasaki, Y., Tateno, M. et al. (2018) A pilot study for the detection of cyclic prolyl-hydroxyproline (Pro-Hyp) in human blood after ingestion of collagen hydrolysate. Clinical Trial Nutrients, vol. 10, no. 10, article 1356. DOI: 10.3390/nu10101356 (In English)
Sikiric, P., Seiwerth, S., Rucman, R. et al. (2016) Brain-gut axis and pentadecapeptide BPC 157: Theoretical and practical implications. Current Neuropharmacology, vol. 14, no. 8, pp. 857–865. DOI: 10.2174/1570159X13666160502153022 (In English)
Snelgrove, R. J., Jackson, P. L., Hardison, M. T. et al. (2010) A critical role for LTA4H in limiting chronic pulmonary neutrophilic inflammation. Science, vol. 330, no. 6000, pp. 90–94. DOI: 10.1126/science.1190594 (In English)
Umarova, B. A., Kopylova, G. N., Smirnova, E. A. et al. (2003) Secretory activity of mast cell during stress: Effect of prolyl-glycyl-proline and Semax. Bulletin of Experimental Biology and Medicine, vol. 136, no. 4, pp. 325–327. DOI: 10.1023/b:bebm.0000010942.14275.50 (In English)
van Houwelingen, A. H., Weathington, N. M., Verweij, V. et al. (2008) Induction of lung emphysema is prevented by L-arginine-threonine-arginine. The FASEB Journal, vol. 22, no. 9, pp. 3403–3408. DOI: 10.1096/fj.07-096230 (In English)
Wells, J. M., Gaggar, A., Blalock, J. E. (2015) MMP generated matrikines. Matrix Biology, vol. 44–46, pp. 122–129. DOI: 10.1016/j.matbio.2015.01.016 (In English)
Zhuikova, S. E., Badmaeva, K. E., Bakaeva, Z. V. et al. (2004) Protivoyazvennye effekty tripeptida PGP i ego vozmozhnykh metabolitov — PG, GP, glitsina i prolina — na raznykh modelyakh vyzova yazv u krys [Antiulcer effects of PGP tripeptide and its possible metabolites — PG, GP, glycine and proline — in different models of ulceration in rats]. Izvestiya Rossijskoj akademii nauk. Seriya biologicheskaya — Proceedings of the Russian Academy of Sciences. Biological Series, no. 5, pp. 585–588. (In Russian)
Zhuikova, S. E., Badmaeva, K. E., Samonina, G. E., Plesskaya, L. G. (2003a) Semaks i nekotorye gliprolinovye peptidy uskoryayut zazhivlenie atsetatnykh yazv u krys [Semax and certain glyproline peptides accelerate acetate ulcer healing in rats]. Eksperimental’naya i klinicheskaya gastroenterologiya — Experimental & Clinical Gastroenterology, no. 4, pp. 88–92. (In Russian)
Zhuikova, S. E., Bakaeva, Z. V., Samonina, G. E. (2003b) Differentsirovannye protivoyazvennye effekty vozmozhnykh metabolitov peptida PGP — PG i GP — na etanolovoj i stressornoj modelyakh vyzova yazv u krys [Differentiated antiulcer effects of possible PGP peptide metabolites — PG and GP — in ethanol and stress models of ulcer induction in rats]. Vestnik Moskovskogo universiteta. Seria 16. Biologia, no. 2, pp. 20–22. (In Russian)
Zhuikova, S. E., Khropycheva, R. P., Zolotarev, V. A., Polenov, S. A. (2003c) Novye peptidnye regulyatory zheludochnoj sekretsii krys (amilin, PGP i semaks) [New peptide regulators of gastric secretion in rats (amylin, PGP and semax)]. Eksperimental’naya i klinicheskaya gastroenterologiya — Experimental & Clinical Gastroenterology, no. 2, pp. 86–90. (In Russian)
Zolotarev, Yu. A., Zhuikova, S. E., Ashmarin, I. P. et al. (2003) Metabolism of PGP peptide after administration via different routes. Bulletin of Experimental Biology and Medicine, vol. 135, no. 4, pp. 361–364. DOI: 10.1023/a:1024612831380 (In English)
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