Фибринолитики: от разрушения тромбов до процессов роста и ремоделирования сосудов, нейрогенеза, канцерогенеза и фиброза
Фибринолитики: от разрушения тромбов до процессов роста и ремоделирования сосудов, нейрогенеза, канцерогенеза и фиброза
Ткачук В.А., Парфенова Е.В., Плеханова О.С. и др. Фибринолитики: от разрушения тромбов до процессов роста и ремоделирования сосудов, нейрогенеза, канцерогенеза и фиброза. Терапевтический архив. 2019; 91 (9): 4–9. DOI: 10.26442/00403660.2019.09.000411
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Аннотация
Одним из самых выдающихся научных достижений в области тромболизиса является разработка, создание и внедрение фибринолизина – первого советского препарата, разрушающего тромбы. Внутрикоронарное введение фибринолизина позволило снизить летальность больных инфарктом миокарда почти на 20%. За исследования в этой области в 1982 г. Евгений Иванович Чазов был удостоен Ленинской премии. В течение последующих десятилетий под его руководством в Кардиоцентре созданы научные и клинические лаборатории, в которых создавалось новое поколение препаратов на основе фибринолитиков для лечения больных инфарктом миокарда, восстановления кровоснабжения ишемизированной ткани, а также изучались механизмы ремоделирования кровеносных сосудов с участием системы фибринолиза. В результате научных исследований обнаружены новые механизмы регуляции направленного роста сосудов и нервов, роста опухоли и ее метастазирования с участием белков системы фибринолиза. В обзоре рассматривается современное представление о роли системы фибринолиза в разрушении тромба, роста и ремоделирования сосудов, нейрогенеза, канцерогенеза и фиброза. Статья посвящена 90-летию академика Е.И. Чазова.
Ключевые слова: фибринолитическая система, урокиназа, урокиназный рецептор, тканевый активатор плазминогена, ремоделирование сосудов, ангиогенез, нейрогенез, канцерогенез, метастазирование опухоли.
Keywords: fibrinolytic system, urokinase, urokinase receptor, tissue plasminogen activator, arterial remodeling, angiogenesis, neurogenesis, carcinogenesis, tumor metastasis.
Ключевые слова: фибринолитическая система, урокиназа, урокиназный рецептор, тканевый активатор плазминогена, ремоделирование сосудов, ангиогенез, нейрогенез, канцерогенез, метастазирование опухоли.
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Keywords: fibrinolytic system, urokinase, urokinase receptor, tissue plasminogen activator, arterial remodeling, angiogenesis, neurogenesis, carcinogenesis, tumor metastasis.
Список литературы
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2. [Chazov EI, Andreenko GV. The first experience of thrombosis therapy with domestic fibrinolysin. Kardiologiia. 1962;4:59-64 (In Russ.)].
3. [Chazov EI, Matveeva LS, Mazaev AV, Sargin KE, Sadovskaia GV, Ruda MI. Intracoronary administration of fibrinolysin in acute myocardial infarct. Therapeutic Archive.1976;48(4):8-19 (In Russ.)].
4. [Патент RF for the invention №1692151 Bull. №13. Belogurov AA, Bibilashvili RSh, Goryunova LE, Delver EP, Domkin VD, Efimova EP, Rybalkin IN, Savochkina LP, Sidorov MA, Skamrov AV, Chenchik AA, Shevelev AI, Yuzhakov AA. Rekombinantnaya plazmidnaya DNK ruavs, kodiruyushchaya aktivator plazminogena urokinaznogo tipa, sposob yeye konstruirovaniya i shtamm bakteriy escherichia coli produtsent aktivatora plazminogena urokinaznogo tipa (In Russ.)].
5. [Chazov EI. The role of fundamental science achievements in raising treatment efficacy. Therapeutic Archive. 2005;77(8):5-9 (In Russ.)].
6. Nicholl SM, Roztocil E, Davies MG. Plasminogen activator system and vascular disease. Curr Vasc Pharmacol. 2006;4:101-16. doi: 10.2174/ 157016106776359880
7. Blasi F. The urokinase receptor: a cell surface, regulated chemokine. APMIS. 1999;107:96-101. doi: https://doi.org/10.1111/j.1699-0463.1999. tb01531.x
8. Tkachuk VA, Plekhanova OS, Parfyonova YV. Regulation of arterial remodeling and angiogenesis by urokinase-type plasminogen activator. Can J Physiol Pharmacol. 2009;87(4):231-51. doi: 10.1139/Y08-113
9. Cui K, Lyu S, Song X, Yuan F, Xu F, Zhang M, Wang W, Zhang D, Dai J. Drug-eluting balloon versus bare-mental stent and drug-eluting stent for de novo coronary artery disease: A systematic review and meta-analysis of 14 randomized controlled trials. PLoS One. 2017;12(4):e0176365. doi: 10.1371/journal.pone.0176365. eCollection 2017
10. Araújo PV, Ribeiro MS, Dalio MB, Rocha LA, Viaro F, Dellalibera Joviliano R, Piccinato CE, Évora PR, Joviliano EE. Interleukins and inflammatory markers in in-stent restenosis after femoral percutaneous transluminal angioplasty. Ann Vasc Surg. 2015;29(4):731-7. doi: 10.1016/ j.avsg.2014.12.006
11. Plekhanova O, Parfyonova Ye, Bibilashvily R, Domogatskii S, Stepanova V, Gulba DC, Agrotis A, Bobik A, Tkachuk V. Urokinase plasminogen activator augments cell proliferation and neointima formation in injured arteries via proteolytic mechanisms. Atherosclerosis. 2001;159(2):297-306. doi: https://doi.org/10.1016/S0021-9150(01)00511-1
12. Plekhanova O, Parfyonova Ye, Bibilashvily R, Stepanova V, Bobik A, Tkachuk V. Urokinase plasminogen activator enhances intima and media growth and reduces lumen size in carotid arteries. J Hypertension. 2000;18(8):1065-9. doi: 10.1097/00004872-200018080-00011
13. Plekhanova O, Stepanova V, Ratner E, Bobik A, Tkachuk V, Parfyonova Ye. Urokinase plasminogen activator in injured adventitia increases the number of myofibroblasts and augments early proliferation. J Vasc Res. 2006;43(5):437-46. doi: 10.1159/000094906
14. [Plekhanova OS, Solomatina MA, Domogatskii SP, Naumov VG, Tkachuk VA, Parfenova EV, Chazov EI. Urokinase stimulates whereas tissue plasminogen activator attenuates blood vessel stenosis. Ross Fiziol Zh Im IM Sechenova. 2001;87(5):584-93 (In Russ.)].
15. Plekhanova O, Berk BC, Bashtrykov P, Brooks A, Tkachuk V, Parfyonova Ye. Oligonucleotide microarrays reveal regulated genes related to inward arterial remodeling induced by urokinase plasminogen activator. J Vasc Res. 2009;46(3):177-87. doi: 10.1159/000156703
16. Plekhanova O, Parfyonova Y, Beloglazova I, Berk BC and Tkachuk V. Oligonucleotide microarrays identified potential regulatory genes related to early outward arterial remodeling induced by tissue plasminogen activator. Front Physiol. 2019;10:493. doi: 10.3389/fphys.2019.00493
17. Menshikov M, Plekhanova O, Cai H, Chalupsky K, Parfyonova Y, Bashtrikov P, Tkachuk V, Berk BC. Urokinase plasminogen activator stimulates vascular smooth muscle cell proliferation via redox-dependent pathways. Arterioscler Thromb Vasc Biol. 2006;26:801-7. doi: 10.1161/0 1.ATV.0000207277.27432.15
18. Stepanova V, Lebedeva T, Kuo A, Yarovoi S, Tkachuk S, Zaitsev S, Bdeir K, Dumler I, Marks MS, Parfyonova Y, Tkachuk VA, Higazi AA, Cines DB. Nuclear translocation of urokinase-type plasminogen activator. Blood. 2008;112:100-10. doi: 10.1182/blood-2007-07-104455
19. Stepanova V, Jayaraman PS, Zaitsev SV, Lebedeva T, Bdeir K, Kershaw R, Holman KR, Parfyonova YV, Semina EV, Beloglazova IB, Tkachuk VA, Cines DB. Urokinase-type plasminogen activator (uPA) promotes angiogenesis by attenuating proline-rich homeodomain protein (PRH) transcription factor activity and de-repressing vascular endothelial growth factor (VEGF) receptor expression. J Biol Chem. 2016;291(29):15029-45. doi: 10.1074/jbc.M115.678490
20. Van Weel V, van Tongeren RB, van Hinsbergh VW, van Bockel JH, Quax PH. Vascular growth in ischemic limbs: a review of mechanisms and possible therapeutic stimulation. Ann Vasc Surg. 2008;22:582-97. doi: 10.1016/j.avsg.2008.02.017
21. Beloglazova IB, Zubkova ES, Stambol'skii DV, Plekhanova OS, Men'shikov MY, Akopyan ZhA, Bibilashvili RSh, Parfenova EV, Tkachuk VA. Proteolytically inactive recombinant forms of urokinase suppress migration of endothelial cells. Bull Exp Biol Med. 2014;156(6):756-9. doi: 10.1007/s10517-014-2442-z
22. [Parfenova EV, Plekhanova OS, Men'shikov MIu, Stepanova VV, Tkachuk VA. Regulation of growth and remodeling of blood vessels: the unique role of urokinase. Ross Fiziol Zh Im IM Sechenova. 2009;95(5):442-64 (In Russ.)].
23. Traktuev DO, Tsokolaeva ZI, Shevelev AA, Talitskiy KA, Stepanova VV, Johnstone BH, Rahmat-Zade TM, Kapustin AN, Tkachuk VA, March KL, Parfyonova YV. Urokinase gene transfer augments angiogenesis in ischemic skeletal and myocardial muscle. Mol Ther. 2007;15:1939-46. doi: 10.1038/sj.mt.6300262
24. Semina E, Rubina K, Sysoeva V, Rysenkova K, Klimovich P, Plekhanova O, Tkachuk V. Urokinase and urokinase receptor participate in regulation of neuronal migration, axon growth and branching. Eur J Cell Biol. 2016 Sep;95(9):295-310. doi: 10.1016/j.ejcb.2016.05.003
25. [Semina EV, Rubina KA, Sysoeva VYu, Makarevich PI, Parfenova EV, Tkachuk VA. Participation of the urokinase system in the migration of vascular cells and in the regulation of growth and branching of capillaries. Citologia. 2015;57(10):689-98 (In Russ.)].
26.[Rubina KA, Semina EV, Tkachuk VA. Navigation molecules and chemokines in the processes of growth and remodeling of blood vessels. J Evolutionary Biochemistry and Physiology. 2017;5:313-27 (In Russ.)].
27. Witmer AN, van Blijswijk BC, van Noorden CJ, Vrensen GF, Schlingemann RO. In vivo angiogenic phenotype of endothelial cells and pericytes induced by vascular endothelial growth factor-A. J Histochem Cytochem. 2004;52(1):39-52. doi: 10.1177/002215540405200105
28. [Semina EV, Rubina KA, Stepanova VV, Tkachuk VA. The participation of the urokinase receptor and its endogenous ligands in the development of the brain and the formation of cognitive functions. Russian physiological journal IM Sechenov. 2016;102(8):881-903 (In Russ.)].
29. Levitt P. Disruption of Interneuron Development. Epilepsia. 2005; 46(7):22-8. doi: https://doi.org/10.1111/j.1528-1167.2005.00305.x
30. Semina EV, Rubina KA, Stepanova VV, Tkachuk VA. Involvement of the Urokinase Receptor and Its Endogenous Ligands in the Development of the Brain and the Formation of Cognitive Functions. Neuroscience and Behavioral Physiology. 2018;48(1):16-27. doi: 10.1007/s11055-017-0525-9
31. Stone RC, Pastar I, Ojeh N, Chen V, Liu S, Garzon KI, Tomic-Canic M. Epithelial-mesenchymal transition in tissue repair and fibrosis. Cell Tissue Res. 2016;365(3):495-506. doi: 10.1007/s00441-016-2464-0
32. Rybinski B, Franco-Barraza J, Cukierman E. The wound healing, chronic fibrosis, and cancer progression triad. Physiol Genomics. 2014;46(7):223-44. doi: 10.1152/physiolgenomics.00158.2013
33. Weidenfeld K, Barkan D. EMT and Stemness in Tumor Dormancy and Outgrowth: Are They Intertwined Processes? Front Oncol. 2018;8:381. doi: 10.3389/fonc.2018.00381
34. Rubina KA, Sysoeva VYu, Zagorujko EI, Tsokolaeva ZI, Kurdina MI, Parfyonova YeV, Tkachuk VA. Increased expression of uPA, uPAR, andPAI-1 in psoriatic skin and in basal cell carcinomas. Archives of Dermatological Research. 2017;309(6):433-42. doi: 10.1007/s00403-017-1738-z
35. Rysenkova KD, Semina EV, Karagyaur MN, Shmakova AA, Dyikanov DT, Vasiluev PA, Rubtsov YP, Rubina KA, Tkachuk VA. CRISPR/Cas9 nickase mediated targeting of urokinase receptor gene inhibits neuroblastoma cell proliferation. Oncotarget. 2018;9(50):29414-30. doi: 10.18632/oncotarget.25647
36. Dyikanov DT, Vasiluev PA, Rysenkova KD, Aleksandrushkina NA, Tyurin-Kuzmin PA, Kulebyakin KY, Rubtsov YP, Shmakova AA, Evseeva MN, Balatskiy AV, Semina EV, Rostovtseva AI, Makarevich PI, Karagyaur MN. Optimization of CRISPR/Cas9 Technology to Knock Out Genes of Interest in Aneuploid Cell Lines. Tissue Eng Part C Methods. 2019;25(3):168-75. doi: 10.1089/ten.TEC.2018.0365
2. Чазов Е.И., Андреенко Г.В. Первый опыт терапии тромбоза отечественным фибринолизином. Кардиология. 1962;4:59-64 [Chazov EI, Andreenko GV. The first experience of thrombosis therapy with domestic fibrinolysin. Kardiologiia. 1962;4:59-64 (In Russ.)].
3. Чазов Е.И., Матвеева Л.С., Мазаев А.В., Саргин К.Е., Садовская Г.В., Руда М.Я. Внутрикоронарное назначение фибринолизина при остром инфаркте миокарда. Терапевтический архив. 1976;48(4):8-19 [Chazov EI, Matveeva LS, Mazaev AV, Sargin KE, Sadovskaia GV, Ruda MI. Intracoronary administration of fibrinolysin in acute myocardial infarct. Therapeutic Archive.1976;48(4):8-19 (In Russ.)].
4. Патент СССР на изобретение №1692151. Бюллетень №13. Белогуров А.А., Бибилашвили Р.Ш., Горюнова Л.Е., Дельвер Е.П., Домкин В.Д., Ефимова Е.П., Рыбалкин И.Н., Савочкина Л.П., Сидоров М.А., Скамров А.В., Ченчик А.А., Шевелев А.Я., Южаков А.А. Рекомбинантная плазмидная ДНК рuавс, кодирующая активатор плазминогена урокиназного типа, способ ее конструирования и штамм бактерий escherichia coli продуцент активатора плазминогена урокиназного типа. Ссылка активна на 07.07.2019 http://patents.su/1-1692151-rekombinantnaya-plazmidnaya-dnk-ruavs-kodiruyushhaya-aktivator-plazminog... [Патент RF for the invention №1692151 Bull. №13. Belogurov AA, Bibilashvili RSh, Goryunova LE, Delver EP, Domkin VD, Efimova EP, Rybalkin IN, Savochkina LP, Sidorov MA, Skamrov AV, Chenchik AA, Shevelev AI, Yuzhakov AA. Rekombinantnaya plazmidnaya DNK ruavs, kodiruyushchaya aktivator plazminogena urokinaznogo tipa, sposob yeye konstruirovaniya i shtamm bakteriy escherichia coli produtsent aktivatora plazminogena urokinaznogo tipa (In Russ.)].
5. Чазов Е.И. Роль достижений фундаментальной науки в повышении эффективности лечения. Терапевтический архив. 2005;77(8):5-9 [Chazov EI. The role of fundamental science achievements in raising treatment efficacy. Therapeutic Archive. 2005;77(8):5-9 (In Russ.)].
6. Nicholl SM, Roztocil E, Davies MG. Plasminogen activator system and vascular disease. Curr Vasc Pharmacol. 2006;4:101-16. doi: 10.2174/ 157016106776359880
7. Blasi F. The urokinase receptor: a cell surface, regulated chemokine. APMIS. 1999;107:96-101. doi: https://doi.org/10.1111/j.1699-0463.1999. tb01531.x
8. Tkachuk VA, Plekhanova OS, Parfyonova YV. Regulation of arterial remodeling and angiogenesis by urokinase-type plasminogen activator. Can J Physiol Pharmacol. 2009;87(4):231-51. doi: 10.1139/Y08-113
9. Cui K, Lyu S, Song X, Yuan F, Xu F, Zhang M, Wang W, Zhang D, Dai J. Drug-eluting balloon versus bare-mental stent and drug-eluting stent for de novo coronary artery disease: A systematic review and meta-analysis of 14 randomized controlled trials. PLoS One. 2017;12(4):e0176365. doi: 10.1371/journal.pone.0176365. eCollection 2017
10. Araújo PV, Ribeiro MS, Dalio MB, Rocha LA, Viaro F, Dellalibera Joviliano R, Piccinato CE, Évora PR, Joviliano EE. Interleukins and inflammatory markers in in-stent restenosis after femoral percutaneous transluminal angioplasty. Ann Vasc Surg. 2015;29(4):731-7. doi: 10.1016/ j.avsg.2014.12.006
11. Plekhanova O, Parfyonova Ye, Bibilashvily R, Domogatskii S, Stepanova V, Gulba DC, Agrotis A, Bobik A, Tkachuk V. Urokinase plasminogen activator augments cell proliferation and neointima formation in injured arteries via proteolytic mechanisms. Atherosclerosis. 2001;159(2):297-306. doi: https://doi.org/10.1016/S0021-9150(01)00511-1
12. Plekhanova O, Parfyonova Ye, Bibilashvily R, Stepanova V, Bobik A, Tkachuk V. Urokinase plasminogen activator enhances intima and media growth and reduces lumen size in carotid arteries. J Hypertension. 2000;18(8):1065-9. doi: 10.1097/00004872-200018080-00011
13. Plekhanova O, Stepanova V, Ratner E, Bobik A, Tkachuk V, Parfyonova Ye. Urokinase plasminogen activator in injured adventitia increases the number of myofibroblasts and augments early proliferation. J Vasc Res. 2006;43(5):437-46. doi: 10.1159/000094906
14. Плеханова О.С., Соломатина М.А., Домогатский С.П., Наумов В.Г., Ткачук В.А., Парфенова Е.В., Чазов Е.И. Урокиназа стимулирует, а тканевой активатор плазминогена подавляет развитие стеноза кровеносных сосудов. Российский физиологический журнал им. И.М. Сеченова. 2001;87(5):584-93 [Plekhanova OS, Solomatina MA, Domogatskii SP, Naumov VG, Tkachuk VA, Parfenova EV, Chazov EI. Urokinase stimulates whereas tissue plasminogen activator attenuates blood vessel stenosis. Ross Fiziol Zh Im IM Sechenova. 2001;87(5):584-93 (In Russ.)].
15. Plekhanova O, Berk BC, Bashtrykov P, Brooks A, Tkachuk V, Parfyonova Ye. Oligonucleotide microarrays reveal regulated genes related to inward arterial remodeling induced by urokinase plasminogen activator. J Vasc Res. 2009;46(3):177-87. doi: 10.1159/000156703
16. Plekhanova O, Parfyonova Y, Beloglazova I, Berk BC and Tkachuk V. Oligonucleotide microarrays identified potential regulatory genes related to early outward arterial remodeling induced by tissue plasminogen activator. Front Physiol. 2019;10:493. doi: 10.3389/fphys.2019.00493
17. Menshikov M, Plekhanova O, Cai H, Chalupsky K, Parfyonova Y, Bashtrikov P, Tkachuk V, Berk BC. Urokinase plasminogen activator stimulates vascular smooth muscle cell proliferation via redox-dependent pathways. Arterioscler Thromb Vasc Biol. 2006;26:801-7. doi: 10.1161/0 1.ATV.0000207277.27432.15
18. Stepanova V, Lebedeva T, Kuo A, Yarovoi S, Tkachuk S, Zaitsev S, Bdeir K, Dumler I, Marks MS, Parfyonova Y, Tkachuk VA, Higazi AA, Cines DB. Nuclear translocation of urokinase-type plasminogen activator. Blood. 2008;112:100-10. doi: 10.1182/blood-2007-07-104455
19. Stepanova V, Jayaraman PS, Zaitsev SV, Lebedeva T, Bdeir K, Kershaw R, Holman KR, Parfyonova YV, Semina EV, Beloglazova IB, Tkachuk VA, Cines DB. Urokinase-type plasminogen activator (uPA) promotes angiogenesis by attenuating proline-rich homeodomain protein (PRH) transcription factor activity and de-repressing vascular endothelial growth factor (VEGF) receptor expression. J Biol Chem. 2016;291(29):15029-45. doi: 10.1074/jbc.M115.678490
20. Van Weel V, van Tongeren RB, van Hinsbergh VW, van Bockel JH, Quax PH. Vascular growth in ischemic limbs: a review of mechanisms and possible therapeutic stimulation. Ann Vasc Surg. 2008;22:582-97. doi: 10.1016/j.avsg.2008.02.017
21. Beloglazova IB, Zubkova ES, Stambol'skii DV, Plekhanova OS, Men'shikov MY, Akopyan ZhA, Bibilashvili RSh, Parfenova EV, Tkachuk VA. Proteolytically inactive recombinant forms of urokinase suppress migration of endothelial cells. Bull Exp Biol Med. 2014;156(6):756-9. doi: 10.1007/s10517-014-2442-z
22. Парфенова Е.В., Плеханова О.С., Меньшиков М.Ю., Степанова В.В., Ткачук В.А. Регуляция роста и ремоделирования кровеносных сосудов: уникальная роль урокиназы. Российский физиологический журнал им. И.М. Сеченова. 2009;95(5):442-64 [Parfenova EV, Plekhanova OS, Men'shikov MIu, Stepanova VV, Tkachuk VA. Regulation of growth and remodeling of blood vessels: the unique role of urokinase. Ross Fiziol Zh Im IM Sechenova. 2009;95(5):442-64 (In Russ.)].
23. Traktuev DO, Tsokolaeva ZI, Shevelev AA, Talitskiy KA, Stepanova VV, Johnstone BH, Rahmat-Zade TM, Kapustin AN, Tkachuk VA, March KL, Parfyonova YV. Urokinase gene transfer augments angiogenesis in ischemic skeletal and myocardial muscle. Mol Ther. 2007;15:1939-46. doi: 10.1038/sj.mt.6300262
24. Semina E, Rubina K, Sysoeva V, Rysenkova K, Klimovich P, Plekhanova O, Tkachuk V. Urokinase and urokinase receptor participate in regulation of neuronal migration, axon growth and branching. Eur J Cell Biol. 2016 Sep;95(9):295-310. doi: 10.1016/j.ejcb.2016.05.003
25. Семина Е.В., Рубина К.А., Сысоева В.Ю., Макаревич П.И., Парфенова Е.В., Ткачук В.А. Участие урокиназной системы в миграции сосудистых клеток и в регуляции роста и ветвления капилляров. Цитология. 2015;57(10):689-98 [Semina EV, Rubina KA, Sysoeva VYu, Makarevich PI, Parfenova EV, Tkachuk VA. Participation of the urokinase system in the migration of vascular cells and in the regulation of growth and branching of capillaries. Citologia. 2015;57(10):689-98 (In Russ.)].
26. Рубина К.А., Семина Е.В., Ткачук В.А. Навигационные молекулы и хемокины в процессах роста и ремоделирования сосудов. Журнал эволюционной биохимии и физиологии. 2017;5:313-27 [Rubina KA, Semina EV, Tkachuk VA. Navigation molecules and chemokines in the processes of growth and remodeling of blood vessels. J Evolutionary Biochemistry and Physiology. 2017;5:313-27 (In Russ.)].
27. Witmer AN, van Blijswijk BC, van Noorden CJ, Vrensen GF, Schlingemann RO. In vivo angiogenic phenotype of endothelial cells and pericytes induced by vascular endothelial growth factor-A. J Histochem Cytochem. 2004;52(1):39-52. doi: 10.1177/002215540405200105
28. Семина Е.В., Рубина К.А., Степанова В.В., Ткачук В.А. Участие рецептора урокиназы и его эндогенных лигандов в развитии головного мозга и формировании когнитивных функций. Российский физиологический журнал им. И.М. Сеченова. 2016;102(8):881-903 [Semina EV, Rubina KA, Stepanova VV, Tkachuk VA. The participation of the urokinase receptor and its endogenous ligands in the development of the brain and the formation of cognitive functions. Russian physiological journal IM Sechenov. 2016;102(8):881-903 (In Russ.)].
29. Levitt P. Disruption of Interneuron Development. Epilepsia. 2005; 46(7):22-8. doi: https://doi.org/10.1111/j.1528-1167.2005.00305.x
30. Semina EV, Rubina KA, Stepanova VV, Tkachuk VA. Involvement of the Urokinase Receptor and Its Endogenous Ligands in the Development of the Brain and the Formation of Cognitive Functions. Neuroscience and Behavioral Physiology. 2018;48(1):16-27. doi: 10.1007/s11055-017-0525-9
31. Stone RC, Pastar I, Ojeh N, Chen V, Liu S, Garzon KI, Tomic-Canic M. Epithelial-mesenchymal transition in tissue repair and fibrosis. Cell Tissue Res. 2016;365(3):495-506. doi: 10.1007/s00441-016-2464-0
32. Rybinski B, Franco-Barraza J, Cukierman E. The wound healing, chronic fibrosis, and cancer progression triad. Physiol Genomics. 2014;46(7):223-44. doi: 10.1152/physiolgenomics.00158.2013
33. Weidenfeld K, Barkan D. EMT and Stemness in Tumor Dormancy and Outgrowth: Are They Intertwined Processes? Front Oncol. 2018;8:381. doi: 10.3389/fonc.2018.00381
34. Rubina KA, Sysoeva VYu, Zagorujko EI, Tsokolaeva ZI, Kurdina MI, Parfyonova YeV, Tkachuk VA. Increased expression of uPA, uPAR, andPAI-1 in psoriatic skin and in basal cell carcinomas. Archives of Dermatological Research. 2017;309(6):433-42. doi: 10.1007/s00403-017-1738-z
35. Rysenkova KD, Semina EV, Karagyaur MN, Shmakova AA, Dyikanov DT, Vasiluev PA, Rubtsov YP, Rubina KA, Tkachuk VA. CRISPR/Cas9 nickase mediated targeting of urokinase receptor gene inhibits neuroblastoma cell proliferation. Oncotarget. 2018;9(50):29414-30. doi: 10.18632/oncotarget.25647
36. Dyikanov DT, Vasiluev PA, Rysenkova KD, Aleksandrushkina NA, Tyurin-Kuzmin PA, Kulebyakin KY, Rubtsov YP, Shmakova AA, Evseeva MN, Balatskiy AV, Semina EV, Rostovtseva AI, Makarevich PI, Karagyaur MN. Optimization of CRISPR/Cas9 Technology to Knock Out Genes of Interest in Aneuploid Cell Lines. Tissue Eng Part C Methods. 2019;25(3):168-75. doi: 10.1089/ten.TEC.2018.0365
________________________________________________
2. [Chazov EI, Andreenko GV. The first experience of thrombosis therapy with domestic fibrinolysin. Kardiologiia. 1962;4:59-64 (In Russ.)].
3. [Chazov EI, Matveeva LS, Mazaev AV, Sargin KE, Sadovskaia GV, Ruda MI. Intracoronary administration of fibrinolysin in acute myocardial infarct. Therapeutic Archive.1976;48(4):8-19 (In Russ.)].
4. [Патент RF for the invention №1692151 Bull. №13. Belogurov AA, Bibilashvili RSh, Goryunova LE, Delver EP, Domkin VD, Efimova EP, Rybalkin IN, Savochkina LP, Sidorov MA, Skamrov AV, Chenchik AA, Shevelev AI, Yuzhakov AA. Rekombinantnaya plazmidnaya DNK ruavs, kodiruyushchaya aktivator plazminogena urokinaznogo tipa, sposob yeye konstruirovaniya i shtamm bakteriy escherichia coli produtsent aktivatora plazminogena urokinaznogo tipa (In Russ.)].
5. [Chazov EI. The role of fundamental science achievements in raising treatment efficacy. Therapeutic Archive. 2005;77(8):5-9 (In Russ.)].
6. Nicholl SM, Roztocil E, Davies MG. Plasminogen activator system and vascular disease. Curr Vasc Pharmacol. 2006;4:101-16. doi: 10.2174/ 157016106776359880
7. Blasi F. The urokinase receptor: a cell surface, regulated chemokine. APMIS. 1999;107:96-101. doi: https://doi.org/10.1111/j.1699-0463.1999. tb01531.x
8. Tkachuk VA, Plekhanova OS, Parfyonova YV. Regulation of arterial remodeling and angiogenesis by urokinase-type plasminogen activator. Can J Physiol Pharmacol. 2009;87(4):231-51. doi: 10.1139/Y08-113
9. Cui K, Lyu S, Song X, Yuan F, Xu F, Zhang M, Wang W, Zhang D, Dai J. Drug-eluting balloon versus bare-mental stent and drug-eluting stent for de novo coronary artery disease: A systematic review and meta-analysis of 14 randomized controlled trials. PLoS One. 2017;12(4):e0176365. doi: 10.1371/journal.pone.0176365. eCollection 2017
10. Araújo PV, Ribeiro MS, Dalio MB, Rocha LA, Viaro F, Dellalibera Joviliano R, Piccinato CE, Évora PR, Joviliano EE. Interleukins and inflammatory markers in in-stent restenosis after femoral percutaneous transluminal angioplasty. Ann Vasc Surg. 2015;29(4):731-7. doi: 10.1016/ j.avsg.2014.12.006
11. Plekhanova O, Parfyonova Ye, Bibilashvily R, Domogatskii S, Stepanova V, Gulba DC, Agrotis A, Bobik A, Tkachuk V. Urokinase plasminogen activator augments cell proliferation and neointima formation in injured arteries via proteolytic mechanisms. Atherosclerosis. 2001;159(2):297-306. doi: https://doi.org/10.1016/S0021-9150(01)00511-1
12. Plekhanova O, Parfyonova Ye, Bibilashvily R, Stepanova V, Bobik A, Tkachuk V. Urokinase plasminogen activator enhances intima and media growth and reduces lumen size in carotid arteries. J Hypertension. 2000;18(8):1065-9. doi: 10.1097/00004872-200018080-00011
13. Plekhanova O, Stepanova V, Ratner E, Bobik A, Tkachuk V, Parfyonova Ye. Urokinase plasminogen activator in injured adventitia increases the number of myofibroblasts and augments early proliferation. J Vasc Res. 2006;43(5):437-46. doi: 10.1159/000094906
14. [Plekhanova OS, Solomatina MA, Domogatskii SP, Naumov VG, Tkachuk VA, Parfenova EV, Chazov EI. Urokinase stimulates whereas tissue plasminogen activator attenuates blood vessel stenosis. Ross Fiziol Zh Im IM Sechenova. 2001;87(5):584-93 (In Russ.)].
15. Plekhanova O, Berk BC, Bashtrykov P, Brooks A, Tkachuk V, Parfyonova Ye. Oligonucleotide microarrays reveal regulated genes related to inward arterial remodeling induced by urokinase plasminogen activator. J Vasc Res. 2009;46(3):177-87. doi: 10.1159/000156703
16. Plekhanova O, Parfyonova Y, Beloglazova I, Berk BC and Tkachuk V. Oligonucleotide microarrays identified potential regulatory genes related to early outward arterial remodeling induced by tissue plasminogen activator. Front Physiol. 2019;10:493. doi: 10.3389/fphys.2019.00493
17. Menshikov M, Plekhanova O, Cai H, Chalupsky K, Parfyonova Y, Bashtrikov P, Tkachuk V, Berk BC. Urokinase plasminogen activator stimulates vascular smooth muscle cell proliferation via redox-dependent pathways. Arterioscler Thromb Vasc Biol. 2006;26:801-7. doi: 10.1161/0 1.ATV.0000207277.27432.15
18. Stepanova V, Lebedeva T, Kuo A, Yarovoi S, Tkachuk S, Zaitsev S, Bdeir K, Dumler I, Marks MS, Parfyonova Y, Tkachuk VA, Higazi AA, Cines DB. Nuclear translocation of urokinase-type plasminogen activator. Blood. 2008;112:100-10. doi: 10.1182/blood-2007-07-104455
19. Stepanova V, Jayaraman PS, Zaitsev SV, Lebedeva T, Bdeir K, Kershaw R, Holman KR, Parfyonova YV, Semina EV, Beloglazova IB, Tkachuk VA, Cines DB. Urokinase-type plasminogen activator (uPA) promotes angiogenesis by attenuating proline-rich homeodomain protein (PRH) transcription factor activity and de-repressing vascular endothelial growth factor (VEGF) receptor expression. J Biol Chem. 2016;291(29):15029-45. doi: 10.1074/jbc.M115.678490
20. Van Weel V, van Tongeren RB, van Hinsbergh VW, van Bockel JH, Quax PH. Vascular growth in ischemic limbs: a review of mechanisms and possible therapeutic stimulation. Ann Vasc Surg. 2008;22:582-97. doi: 10.1016/j.avsg.2008.02.017
21. Beloglazova IB, Zubkova ES, Stambol'skii DV, Plekhanova OS, Men'shikov MY, Akopyan ZhA, Bibilashvili RSh, Parfenova EV, Tkachuk VA. Proteolytically inactive recombinant forms of urokinase suppress migration of endothelial cells. Bull Exp Biol Med. 2014;156(6):756-9. doi: 10.1007/s10517-014-2442-z
22. [Parfenova EV, Plekhanova OS, Men'shikov MIu, Stepanova VV, Tkachuk VA. Regulation of growth and remodeling of blood vessels: the unique role of urokinase. Ross Fiziol Zh Im IM Sechenova. 2009;95(5):442-64 (In Russ.)].
23. Traktuev DO, Tsokolaeva ZI, Shevelev AA, Talitskiy KA, Stepanova VV, Johnstone BH, Rahmat-Zade TM, Kapustin AN, Tkachuk VA, March KL, Parfyonova YV. Urokinase gene transfer augments angiogenesis in ischemic skeletal and myocardial muscle. Mol Ther. 2007;15:1939-46. doi: 10.1038/sj.mt.6300262
24. Semina E, Rubina K, Sysoeva V, Rysenkova K, Klimovich P, Plekhanova O, Tkachuk V. Urokinase and urokinase receptor participate in regulation of neuronal migration, axon growth and branching. Eur J Cell Biol. 2016 Sep;95(9):295-310. doi: 10.1016/j.ejcb.2016.05.003
25. [Semina EV, Rubina KA, Sysoeva VYu, Makarevich PI, Parfenova EV, Tkachuk VA. Participation of the urokinase system in the migration of vascular cells and in the regulation of growth and branching of capillaries. Citologia. 2015;57(10):689-98 (In Russ.)].
26.[Rubina KA, Semina EV, Tkachuk VA. Navigation molecules and chemokines in the processes of growth and remodeling of blood vessels. J Evolutionary Biochemistry and Physiology. 2017;5:313-27 (In Russ.)].
27. Witmer AN, van Blijswijk BC, van Noorden CJ, Vrensen GF, Schlingemann RO. In vivo angiogenic phenotype of endothelial cells and pericytes induced by vascular endothelial growth factor-A. J Histochem Cytochem. 2004;52(1):39-52. doi: 10.1177/002215540405200105
28. [Semina EV, Rubina KA, Stepanova VV, Tkachuk VA. The participation of the urokinase receptor and its endogenous ligands in the development of the brain and the formation of cognitive functions. Russian physiological journal IM Sechenov. 2016;102(8):881-903 (In Russ.)].
29. Levitt P. Disruption of Interneuron Development. Epilepsia. 2005; 46(7):22-8. doi: https://doi.org/10.1111/j.1528-1167.2005.00305.x
30. Semina EV, Rubina KA, Stepanova VV, Tkachuk VA. Involvement of the Urokinase Receptor and Its Endogenous Ligands in the Development of the Brain and the Formation of Cognitive Functions. Neuroscience and Behavioral Physiology. 2018;48(1):16-27. doi: 10.1007/s11055-017-0525-9
31. Stone RC, Pastar I, Ojeh N, Chen V, Liu S, Garzon KI, Tomic-Canic M. Epithelial-mesenchymal transition in tissue repair and fibrosis. Cell Tissue Res. 2016;365(3):495-506. doi: 10.1007/s00441-016-2464-0
32. Rybinski B, Franco-Barraza J, Cukierman E. The wound healing, chronic fibrosis, and cancer progression triad. Physiol Genomics. 2014;46(7):223-44. doi: 10.1152/physiolgenomics.00158.2013
33. Weidenfeld K, Barkan D. EMT and Stemness in Tumor Dormancy and Outgrowth: Are They Intertwined Processes? Front Oncol. 2018;8:381. doi: 10.3389/fonc.2018.00381
34. Rubina KA, Sysoeva VYu, Zagorujko EI, Tsokolaeva ZI, Kurdina MI, Parfyonova YeV, Tkachuk VA. Increased expression of uPA, uPAR, andPAI-1 in psoriatic skin and in basal cell carcinomas. Archives of Dermatological Research. 2017;309(6):433-42. doi: 10.1007/s00403-017-1738-z
35. Rysenkova KD, Semina EV, Karagyaur MN, Shmakova AA, Dyikanov DT, Vasiluev PA, Rubtsov YP, Rubina KA, Tkachuk VA. CRISPR/Cas9 nickase mediated targeting of urokinase receptor gene inhibits neuroblastoma cell proliferation. Oncotarget. 2018;9(50):29414-30. doi: 10.18632/oncotarget.25647
36. Dyikanov DT, Vasiluev PA, Rysenkova KD, Aleksandrushkina NA, Tyurin-Kuzmin PA, Kulebyakin KY, Rubtsov YP, Shmakova AA, Evseeva MN, Balatskiy AV, Semina EV, Rostovtseva AI, Makarevich PI, Karagyaur MN. Optimization of CRISPR/Cas9 Technology to Knock Out Genes of Interest in Aneuploid Cell Lines. Tissue Eng Part C Methods. 2019;25(3):168-75. doi: 10.1089/ten.TEC.2018.0365
Авторы
В.А. Ткачук, Е.В. Парфенова, О.С. Плеханова, В.В. Степанова, М.Ю. Меньшиков, Е.В. Семина, Р.Ш. Бибилашвили, Е.И. Чазов
ФГБУ «Национальный медицинский исследовательский центр кардиологии» Минздрава России, Москва, Россия
National Medical Research Center of Cardiology, Moscow, Russia
ФГБУ «Национальный медицинский исследовательский центр кардиологии» Минздрава России, Москва, Россия
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National Medical Research Center of Cardiology, Moscow, Russia
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