Цитокиновые факторы роста в регуляции ангиогенеза и атерогенного воспаления в сосудистой стенке. Аналитический обзор. Часть 1
https://doi.org/10.52727/2078-256X-2025-21-1-60-91
Аннотация
Целью обзора является оценка терапевтических возможностей локальной активации ангиогенеза и прерывания атерогенного воспаления при реконструкции слоев артериальной стенки методом введения полисахаридных полимеров в пара-адвентициальную зону кровеносных сосудов. Концепция обзора строится на гипотезе восстановления баланса провоспалительных и атеропротекторных цитокиновых факторов роста при использовании биополимеров. Согласно данным литературы реконструкция адвентициального слоя артериальной стенки с применением гидрогелей полисахаридного ряда, обладающих высоким сродством к холестерину, обусловливает формирование дополнительного внеклеточного матрикса за пределами интимальной и средней зон магистральной артерии и перехода холестериновой массы из интимальной зоны в околоадвентициальное пространство. Создание продуктивного воспаления в зоне адвентиции с помощью биополимеров может служить одним из эффективных способов деградации ранних мягких атеросклеротических бляшек. Рассматривается возможность удаления мягких атеросклеротических бляшек из интимального пространства магистральных артерий методом обширной имплантации в фасциальный футляр сосудов полисахаридных гидрогелей, образующих внеклеточный матрикс второго уровня. Анализ литературы, соответствующей концепции, проводился с использованием баз данных WoS, Scopus, PubMed, DOAJ, Embase, Ei Compendex, преимущественно за последние 8 лет. Обзор позволяет составить представление о молекулярных процессах, протекающих в стенке сосуда при развитии атерогенного воспаления и выявить признаки реконструкции сосудистой стенки при экзогенной имплантации биополимеров. В сосудистой стенке цитокиновые факторы роста сопряжены с природными или синтетическими биоматериалами. Иммобилизованные факторы доступны для клеток, которые вступают в контакт с матрицей, и обеспечивают точно локализованный сигнал для контроля судьбы клеток. Многообещающим подходом для стимулирования ангиогенеза являются биополимерные инъекционные каркасы. Клеточная миграция из интимы и медии может быть активирована благодаря электростатическому градиенту в присутствии сульфатированного полимера, образующего аффинные комплексы с холестерином и липопротеинами низкой плотности (ЛПНП). Высокая аффинность полисахаридных полимеров к холестерину и ЛПНП, а также активная васкуляризация дополнительного экстраклеточного матрикса провоцируют концентрационный градиент холестерина, направленный в сторону гидрогелевой «рубашки». Эффект оттока холестерина может стать основой нового подхода в терапии патологии магистральных сосудов.
Ключевые слова
Об авторах
И. Н. БольшаковРоссия
Игорь Николаевич Большаков, д-р мед. наук, проф. кафедры оперативной хирургии и топографической анатомии
660022, г. Красноярск, ул. Партизана Железняка, 1
Д. В. Шиндякин
Россия
Дмитрий Васильевич Шиндякин, студент педиатрического факультета
660022, г. Красноярск, ул. Партизана Железняка, 1
А. К. Кириченко
Россия
Андрей Константинович Кириченко, д-р мед. наук, проф. кафедры патологической анатомии
660022, г. Красноярск, ул. Партизана Железняка, 1
В. А. Бахшян
Россия
Валентина Артуровна Бахшян, студент лечебного факультета
660022, г. Красноярск, ул. Партизана Железняка, 1
С. В. Архипкин
Россия
Сергей Викторович Архипкин, старший преподаватель кафедры оперативной хирургии и топографической анатомии
660022, г. Красноярск, ул. Партизана Железняка, 1
Список литературы
1. Abu Dabrh A.M., Steffen M.W., Undavalli C., Asi N., Wang Z., Elamin M.B., Conte M.S., Murad M.H. The natural history of untreated severe or critical limb ischemia. J. Vasc. Surg., 2015; 62 (6): 1642–1651. doi: 10.1016/j.jvs.2015.07.065
2. Han J., Luo L., Marcelina O., Kasim V., Wu S. Therapeutic angiogenesis-based strategy for peripheral artery disease. Theranostics, 2022; 12 (11): 5015–5033. doi: 10.7150/thno.74785
3. Riley C.M., Fuegy P.W., Firpo M.A., Shu X.Z., Prestwich G.D., Peattie R.A. Stimulation of in vivo angiogenesis using dual growth factor-loaded cross-linked glycosaminoglycan hydrogels. Biomaterials, 2006; 27 (35): 5935–5943. doi: 10.1016/j.biomaterials.2006.08.029
4. Chiu L.L., Radisic M. Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues. Biomaterials, 2010; 31 (2): 226–241. doi: 10.1016/j.biomaterials.2009.09.039
5. Layman H., Li X., Nagar E., Vial X., Pham S.M., Andreopoulos F.M. Enhanced angiogenic efficacy through controlled and sustained delivery of FGF-2 and G-CSF from fibrin hydrogels containing ionic-albumin microspheres. J. Biomater. Sci. Polym. Ed., 2012; 23 (1-4): 185–206. doi: 10.1163/092050610X546417
6. Roberts J.J., Farrugia B.L., Green R.A., Rnjak-Kovacina J., Martens P.J. In situ formation of poly(vinyl alcohol)-heparin hydrogels for mild encapsulation and prolonged release of basic fibroblast growth factor and vascular endothelial growth factor. J. Tissue Eng., 2016; 7: 2041731416677132. doi: 10.1177/2041731416677132
7. Zieris A., Chwalek K., Prokoph S., Levental K.R., Welzel P.B., Freudenberg U., Werner C. Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels. J. Control. Release, 2011; 156 (1): 28–36. doi: 10.1016/j.jconrel.2011.06.042
8. Yancopoulos G.D., Davis S., Gale N.W., Rudge J.S., Wiegand S.J., Holash J. Vascular-specific growth factors and blood vessel formation. Nature, 2000; 407 (6801): 242–248. doi: 10.1038/35025215
9. Li B., Xiu R. Angiogenesis: from molecular mechanisms to translational implications. Clin. Hemorheol. Microcirc., 2013; 54 (4): 345–355. doi: 10.3233/CH-121647
10. Jansen P.L., Rosch R., Jansen M., Binnebösel M., Junge K., Alfonso-Jaume A., Klinge U., Lovett D.H., Mertens P.R. Regulation of MMP-2 gene transcription in dermal wounds. J. Invest. Dermatol., 2007; 127 (7): 1762–1767. doi: 10.1038/sj.jid.5700765
11. Zhang J., Kasim V., Xie Y.D., Huang C., Sisjayawan J., Dwi Ariyanti A., Yan X.S., Wu X.Y., Liu C.P., Yang L., Miyagishi M., Wu S.R. Inhibition of PHD3 by salidroside promotes neovascularization through cell-cell communications mediated by muscle-secreted angiogenic factors. Sci. Rep., 2017; 7: 43935. doi: 10.1038/srep43935
12. Luo L.L., Han J.X., Wu S.R., Kasim V. Intramuscular injection of sotagliflozin promotes neovascularization in diabetic mice through enhancing skeletal muscle cells paracrine function. Acta Pharmacol. Sin., 2022; 43 (10): 2636–2650. doi: 10.1038/s41401-022-00889-4
13. Liu C., Han J., Marcelina O., Nugrahaningrum D.A., Huang S., Zou M., Wang G., Miyagishi M., He Y., Wu S., Kasim V. Discovery of salidroside-derivated glycoside analogues as novel angiogenesis agents to treat diabetic hind limb ischemia. J. Med. Chem., 2022; 65 (1): 135–162. doi: 10.1021/acs.jmedchem.1c00947
14. Davidson S.M. FAM3A – A mitochondrial route to the stimulation of angiogenesis? EBioMedicine, 2019; 43: 3–4. doi: 10.1016/j.ebiom.2019.04.033
15. Chapanian R., Amsden B.G. Combined and sequential delivery of bioactive VEGF165 and HGF from poly(trimethylene carbonate) based photo-crosslinked elastomers. J. Control. Release, 2010; 143 (1): 53–63. doi: 10.1016/j.jconrel.2009.11.025
16. Fagiani E., Christofori G. Angiopoietins in angiogenesis. Cancer Lett., 2013, 328 (1): 18–26. doi: 10.1016/j.canlet.2012.08.018
17. Sakurai T., Kudo M. Signaling pathways governing tumor angiogenesis. Oncology, 2011; 81, Suppl 1: 24– 29. doi: 10.1159/000333256
18. Payne L.B., Tewari B.P., Dunkenberger L., Bond S., Savelli A., Darden J., Zhao H., Willi C., Kanodia R., Gude R., Powell M.D., Oestreich K.J., Sontheimer H., Dal-Pra S., Chappell J.C. Pericyte progenitor coupling to the emerging endothelium during vasculogenesis via connexin 43. Arterioscler. Thromb. Vasc. Biol., 2022; 42 (4): 96–114. doi: 10.1161/ATVBAHA.121.317324
19. Kruse K., Lee Q.S., Sun Y., Klomp J., Yang X., Huang F., Sun M.Y., Zhao S., Hong Z., Vogel S.M., Shin J.W., Leckband D.E., Tai L.M., Malik A.B., Komarova Y.A. N-cadherin signaling via Trio assembles adherens junctions to restrict endothelial permeability. J. Cell. Biol., 2019; 218 (1): 299–316. doi: 10.1083/jcb.201802076
20. Moccia F., Negri S., Shekha M., Faris P., Guerra G. Endothelial Ca2+ signaling, angiogenesis and vasculogenesis: just what it takes to make a blood vessel. Int. J. Mol. Sci., 2019; 20 (16): 3962. doi: 10.3390/ijms20163962
21. Annex B.H. Therapeutic angiogenesis for critical limb ischaemia. Nat. Rev. Cardiol., 2013; 10 (7): 387–396. doi: 10.1038/nrcardio.2013.0
22. Hoeben A., Landuyt B., Highley M.S., Wildiers H., van Oosterom A.T., de Bruijn E.A. Vascular endothelial growth factor and angiogenesis. Pharmacol. Rev., 2004; 56 (4): 549–580. doi: 10.1124/pr.56.4.3
23. Braghirolli D.I., Helfer V.E., Chagastelles P.C., Dalberto T.P., Gamba D., Pranke P. Electrospun scaffolds functionalized with heparin and vascular endothelial growth factor increase the proliferation of endothelial progenitor cells. Biomed. Mater., 2017; 12 (2): 025003. doi: 10.1088/1748-605X/aa5bbc
24. Chung A.S., Lee J., Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat. Rev. Cancer, 2010; 10 (7): 505–514. doi: 10.1038/nrc2868
25. Cadenas S. ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection. Free Radic. Biol. Med., 2018; 117: 76–89. doi: 10.1016/j.freeradbiomed.2018.01.024
26. Kivelä R., Bry M., Robciuc M.R., Räsänen M., Taavitsainen M., Silvola J.M., Saraste A., Hulmi J.J., Anisimov A., Mдyränpää M.I., Lindeman J.H., Eklund L., Hellberg S., Hlushchuk R., Zhuang Z.W., Simons M., Djonov V., Knuuti J., Mervaala E., Alitalo K. VEGF-B-induced vascular growth leads to metabolic reprogramming and ischemia resistance in the heart. EMBO Mol. Med., 2014; 6 (3): 307–321. doi: 10.1002/emmm.201303147
27. Groppa E., Brkic S., Bovo E., Reginato S., Sacchi V., di Maggio N., Muraro M.G., Calabrese D., Heberer M., Gianni-Barrera R., Banfi A. VEGF dose regulates vascular stabilization through Semaphorin3A and the Neuropilin-1+ monocyte/TGFβ1 paracrine axis. EMBO Mol. Med., 2015; 7 (10): 1366–1384. doi: 10.15252/emmm.201405003
28. Grunewald M., Kumar S., Sharife H., Volinsky E., Gileles-Hillel A., Licht T., Permyakova A., Hinden L., Azar S., Friedmann Y., Kupetz P., Tzuberi R., Anisimov A., Alitalo K., Horwitz M., Leebhoff S., Khoma O.Z., Hlushchuk R., Djonov V., Abramovitch R., Tam J., Keshet E. Counteracting age-related VEGF signaling insufficiency promotes healthy aging and extends life span. Science, 2021; 373 (6554): eabc8479. doi: 10.1126/science.abc8479
29. Rissanen T.T., Markkanen J.E., Gruchala M., Heikura T., Puranen A., Kettunen M.I., Kholová I., Kauppinen R.A., Achen M.G., Stacker S.A., Alitalo K., Ylä-Herttuala S. VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ. Res., 2003; 92 (10): 1098–1106. doi: 10.1161/01.RES.0000073584.46059.E3
30. Wu M., Pokreisz P., Swinnen M., Caluwe E., Gillijns H., Vanden Driessche N., Casazza A., Verbeken E., Collen D., Janssens S. Sustained placental growth factor-2 treatment does not aggravate advanced atherosclerosis in ischemic cardiomyopathy. J. Cardiovasc. Transl. Res., 2017; 10 (4): 348–358. doi: 10.1007/s12265-017-9742-4
31. Goonoo N., Bhaw-Luximon A. Mimicking growth factors: role of small molecule scaffold additives in promoting tissue regeneration and repair. RSC Adv., 2019; 9 (32): 18124–18146. doi: 10.1039/c9ra02765c
32. Risau W. Angiogenic growth factors. Prog. Growth. Factor Res., 1990; 2 (1): 71–79. doi: 10.1016/0955-2235(90)90010-h
33. Chung J.C., Shum-Tim D. Neovascularization in tissue engineering. Cells, 2012; 1 (4): 1246–1260. doi: 10.3390/cells1041246
34. Nikol S., Baumgartner I., van Belle E., Diehm C., Visoná A., Capogrossi M.C., Ferreira-Maldent N., Gallino A., Graham Wyatt M., Dinesh Wijesinghe L., Fusari M., Stephan D., Emmerich J., Pompilio G., Vermassen F., Pham E., Grek V., Coleman M., Meyer F. Therapeutic angiogenesis with intramuscular nv1fgf improves amputation-free survival in patients with critical limb ischemia. Mol. Ther., 2008; 16 (5): 972–978. doi: 10.1038/mt.2008.33
35. Mukherjee S., Patra C.R. Therapeutic application of anti-angiogenic nanomaterials in cancers. Nanoscale, 2016; 8 (25): 12444–12470. doi: 10.1039/c5nr07887c
36. Morishita R., Shimamura M., Takeya Y., Nakagami H., Chujo M., Ishihama T., Yamada E., Rakugi H. Combined analysis of clinical data on HGF gene therapy to treat critical limb ischemia in Japan. Curr. Gene Ther., 2020; 20 (1): 25–35. doi: 10.2174/1566523220666200516171447
37. Sanada F., Fujikawa T., Shibata K., Taniyama Y., Rakugi H., Morishita R. Therapeutic angiogenesis using HGF plasmid. Ann. Vasc. Dis., 2020; 13 (2): 109–115. doi: 10.3400/avd.ra.20-00035.
38. Wu J., Heemskerk J.W.M., Baaten C.C.F.M.J. Platelet membrane receptor proteolysis: implications for platelet function. Front. Cardiovasc. Med., 2021; 7: 608391. doi: 10.3389/fcvm.2020.608391
39. Burzynski L.C., Humphry M., Pyrillou K., Wiggins K.A., Chan J.N.E., Figg N., Kitt L.L., Summers C., Tatham K.C., Martin P.B., Bennett M.R., Clarke M.C.H. The coagulation and immune systems are directly linked through the activation of interleukin-1α by thrombin. Immunity, 2019; 50 (4): 1033–1042.e6. doi: 10.1016/j.immuni.2019.03.003
40. Fang X., Liao R., Yu Y., Li J., Guo Z., Zhu T. Thrombin induces secretion of multiple cytokines and expression of protease-activated receptors in mouse mast cell line. Mediators Inflamm., 2019; 2019: 4952131. doi: 10.1155/2019/4952131
41. Jaberi N., Soleimani A., Pashirzad M., Abdeahad H., Mohammadi F., Khoshakhlagh M., Khazaei M., Ferns G.A., Avan A., Hassanian S.M. Role of thrombin in the pathogenesis of atherosclerosis. J. Cell. Biochem., 2019; 120 (4): 4757–4765. doi: 10.1002/jcb.27771
42. Bea F., Kreuzer J., Preusch M., Schaab S., Isermann B., Rosenfeld M.E., Katus H., Blessing E. Melagatran reduces advanced atherosclerotic lesion size and may promote plaque stability in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol., 2006; 26 (12): 2787–2792. doi: 10.1161/01.ATV.0000246797.05781.ad
43. Grebe A., Hoss F., Latz E. NLRP3 inflammasome and the IL-1 pathway in atherosclerosis. Circ. Res., 2018; 122 (12): 1722–1740. doi: 10.1161/CIRCRESAHA.118.311362
44. Latz E., Xiao T.S., Stutz A. Activation and regulation of the inflammasomes. Nat. Rev. Immunol., 2013; 13 (6): 397–411. doi: 10.1038/nri3452
45. Galea J., Armstrong J., Gadsdon P., Holden H., Francis S.E., Holt C.M. Interleukin-1 beta in coronary arteries of patients with ischemic heart disease. Arterioscler. Thromb. Vasc. Biol., 1996; 16 (8): 1000– 1006. doi: 10.1161/ 01.atv.16.8.1000
46. Weber A., Wasiliew P., Kracht M. Interleukin-1beta (IL-1beta) processing pathway. Sci. Signal, 2010; 3 (105): cm2. doi: 10.1126/scisignal.3105cm2
47. Weber A., Wasiliew P., Kracht M. Interleukin-1 (IL-1) pathway. Sci. Signal, 2010; 3 (105): cm1. doi: 10.1126/scisignal.3105cm1
48. Beltrami-Moreira M., Vromman A., Sukhova G.K., Folco E.J., Libby P. Redundancy of IL-1 isoform signaling and its implications for arterial remodeling. PLoS One, 2016; 11 (3): e0152474. doi: 10.1371/journal.pone.0152474
49. Libby P. Collagenases and cracks in the plaque. J. Clin. Invest., 2013; 123 (8): 3201–3203. doi: 10.1172/JCI67526
50. Libby P. Interleukin-1 beta as a target for atherosclerosis therapy: biological basis of CANTOS and beyond. J. Am. Coll. Cardiol., 2017; 70 (18): 2278–2289. doi: 10.1016/j.jacc.2017.09.028
51. Vromman A., Ruvkun V., Shvartz E., Wojtkiewicz G., Santos Masson G., Tesmenitsky Y., Folco E., Gram H., Nahrendorf M., Swirski F.K., Sukhova G.K., Libby P. Stage-dependent differential effects of interleukin-1 isoforms on experimental atherosclerosis. Eur. Heart J., 2019; 40 (30): 2482–2491. doi: 10.1093/eurheartj/ehz008
52. Kamari Y., Shaish A., Shemesh S., Vax E., Grosskopf I., Dotan S., White M., Voronov E., Dinarello C.A., Apte R.N., Harats D. Reduced atherosclerosis and inflammatory cytokines in apolipoprotein-E-deficient mice lacking bone marrow-derived interleukin1α. Biochem. Biophys. Res. Commun., 2011; 405 (2): 197–203. doi: 10.1016/j.bbrc.2011.01.008
53. Tsioufis P., Theofilis P., Tsioufis K., Tousoulis D. The impact of cytokines in coronary atherosclerotic plaque: current therapeutic approaches. Int. J. Mol. Sci., 2022; 23 (24): 15937. doi: 10.3390/ijms232415937
54. Dinarello C.A. Overview of the IL-1 family in innate inflammation and acquired immunity. Immunol. Rev., 2018; 281 (1): 8–27. doi: 10.1111/imr.12621
55. Herder C., de Las Heras Gala T., Carstensen-Kirberg M., Huth C., Zierer A., Wahl S., Sudduth-Klinger J., Kuulasmaa K., Peretz D., Ligthart S., Bongaerts B.W.C., Dehghan A., Ikram M.A., Jula A., Kee F., Pietilä A., Saarela O., Zeller T., Blankenberg S., Meisinger C., Peters A., Roden M., Salomaa V., Koenig W., Thorand B. Circulating levels of interleukin 1-receptor antagonist and risk of cardiovascular disease: meta-analysis of six population-based cohorts. Arterioscler. Thromb. Vasc. Biol., 2017; 37 (6): 1222–1227. doi: 10.1161/ATVBAHA.117.309307
56. Mai W., Liao Y. Targeting IL-1β in the treatment of atherosclerosis. Front. Immunol., 2020; 11: 589654. doi: 10.3389/fimmu.2020.589654
57. Lee Y.W., Hirani A.A. Role of interleukin-4 in atherosclerosis. Arch. Pharm. Res., 2006; 29 (1): 1–15. doi: 10.1007/BF02977462
58. Ali M., Girgis S., Hassan A., Rudick S., Becker R.C. Inflammation and coronary artery disease: from pathophysiology to Canakinumab Anti-Inflammatory Thrombosis Outcomes Study (CANTOS). Coron. Artery Dis., 2018; 29 (5): 429–437. doi: 10.1097/MCA.0000000000000625
59. Silveira A., McLeod O., Strawbridge R.J., Gertow K., Sennblad B., Baldassarre D., Veglia F., Deleskog A., Persson J., Leander K., Gigante B., Kauhanen J., Rauramaa R., Smit A.J., Mannarino E., Giral P., Gustafsson S., Söderberg S., Öhrvik J., Humphries S.E., Tremoli E., de Faire U., Hamsten A. Plasma IL-5 concentration and subclinical carotid atherosclerosis. Atherosclerosis, 2015; 239 (1): 125–130. doi: 10.1016/j.atherosclerosis.2014.12.046
60. Ishigami T., Abe K., Aoki I., Minegishi S., Ryo A., Matsunaga S., Matsuoka K., Takeda H., Sawasaki T., Umemura S., Endo Y. Anti-interleukin-5 and multiple autoantibodies are associated with human atherosclerotic diseases and serum interleukin-5 levels. FASEB J., 2013; 27 (9): 3437–3445. doi: 10.1096/fj.12-222653
61. Zhao W., Lei T., Li H., Sun D., Mo X., Wang Z., Zhang K., Ou H. Macrophage-specific overexpression of interleukin-5 attenuates atherosclerosis in LDL receptor-deficient mice. Gene Ther., 2015; 22 (8): 645–652. doi: 10.1038/gt.2015.33
62. Ren W., Wang Z., Wang J., Wu Z., Ren Q., Yu A., Ruan Y. IL-5 overexpression attenuates aortic dissection by reducing inflammation and smooth muscle cell apoptosis. Life Sci., 2020; 241: 117144. doi: 10.1016/j.lfs.2019.117144
63. Reiss A.B., Siegart N.M., de Leon J. Interleukin-6 in atherosclerosis: Atherogenic or atheroprotective? Clin. Lipidol., 2017; 12: 14–23. doi: 10.1080/17584299.2017.1319787
64. Schaper F., Rose-John S. Interleukin-6: biology, signaling and strategies of blockade. Cytokine Growth. Factor Rev., 2015; 26 (5): 475–487. doi: 10.1016/j.cytogfr.2015.07.004
65. Rose-John S. IL-6 trans-signaling via the soluble IL-6 receptor: importance for the pro-inflammatory activities of IL-6. Int. J. Biol. Sci., 2012; 8 (9): 1237–1247. doi: 10.7150/ijbs.4989
66. Tzoulaki I., Murray G.D., Lee A.J., Rumley A., Lowe G.D.O., Fowkes F.G.R. C-reactive protein, interleukin-6, and soluble adhesion molecules as predictors of progressive peripheral atherosclerosis in the general population: Edinburgh Artery Study. Circulation, 2005; 112: 976–983. doi: 10.1161/CIRCULATIONAHA.104.513085
67. Li R., Paul A., Ko K.W., Sheldon M., Rich B.E., Terashima T., Dieker C., Cormier S., Li L., Nour E.A., Chan L., Oka K. Interleukin-7 induces recruitment of monocytes/macrophages to endothelium. Eur. Heart J., 2012; 33 (24): 3114–3123. doi: 10.1093/eurheartj/ehr245
68. Standiford T.J., Strieter R.M., Allen R.M., Burdick M.D., Kunkel S.L. IL-7 up-regulates the expression of IL-8 from resting and stimulated human blood monocytes. J. Immunol., 1992; 149: 2035–2039.
69. An Z., Li J., Yu J., Wang X., Gao H., Zhang W., Wei Z., Zhang J., Zhang Y., Zhao J., Liang X.. Neutrophil extracellular traps induced by IL-8 aggravate atherosclerosis via activation NF-κB signaling in macrophages. Cell. Cycle, 2019; 18: 2928–2938. doi: 10.1080/15384101.2019.1662678
70. Zhang W., Tang T., Nie D., Wen S., Jia C., Zhu Z., Xia N., Nie S., Zhou S., Jiao J., Dong W., Lv B., Xu T., Sun B., Lu Y., Li Y., Cheng L., Liao Y., Cheng X. IL-9 aggravates the development of atherosclerosis in ApoE-/mice. Cardiovasc. Res., 2015; 106 (3): 453–464. doi: 10.1093/cvr/cvv110
71. Mittal S.K., Cho K.J., Ishido S., Roche P.A. Interleukin 10 (IL-10)-mediated immunosuppression: march-I induction regulates antigen presentation by macrophages but not dendritic cells. J. Biol. Chem., 2015; 290 (45): 27158–27167. doi: 10.1074/jbc.M115.682708
72. Han X., Boisvert W.A. Interleukin-10 protects against atherosclerosis by modulating multiple atherogenic macrophage function. Thromb. Haemost., 2015; 113 (3): 505–512. doi: 10.1160/TH14-06-0509
73. Abu El-Asrar A.M., Ahmad A., Allegaert E., Siddiquei M.M., Gikandi P.W., de Hertogh G., Opdenakker G. Interleukin-11 overexpression and M2 macrophage density are associated with angiogenic activity in proliferative diabetic retinopathy. Ocul. Immunol. Inflamm., 2020; 28 (4): 575–588. doi: 10.1080/09273948.2019.1616772
74. Roger I., Estornut C., Ballester B., Milara J., Cortijo J. Role of IL-11 in vascular function of pulmonary fibrosis patients. Eur. Respir. J., 2019; 54 (suppl 63): PA1424. doi: 10.1183/13993003.congress-2019.PA1424
75. Elshabrawy H.A., Volin M.V., Essani A.B., Chen Z., McInnes I.B., van Raemdonck K., Palasiewicz K., Arami S., Gonzalez M., Ashour H.M., Kim S.J., Zhou G., Fox D.A., Shahrara S. IL-11 facilitates a novel connection between RA joint fibroblasts and endothelial cells. Angiogenesis, 2018; 21 (2): 215–228. doi: 10.1007/s10456-017-9589-y
76. Guo Y.T., Lu Y.Y., Lu X., He S., Li S.J., Shao S., Zhou H.D., Wang R.Q., Li X.D., Gao P.J. Krüppellike factor 15/interleukin 11 axis-mediated adventitial remodeling depends on extracellular signal-regulated kinases 1 and 2 activation in angiotensin ii-induced hypertension. J. Am. Heart Assoc., 2021; 10 (16): e020554. doi: 10.1161/JAHA.120.020554
77. Widjaja A.A., Viswanathan S., Jinrui D., Singh B.K., Tan J., Wei Ting J.G., Lamb D., Shekeran S.G., George B.L., Schafer S., Carling D., Adami E., Cook S.A. Molecular dissection of pro-fibrotic IL11 signaling in cardiac and pulmonary fibroblasts. Front. Mol. Biosci., 2021; 8: 740650. doi: 10.3389/fmolb.2021.740650
78. Ye J., Wang Y., Wang Z., Liu L., Yang Z., Wang M., Xu Y., Ye D., Zhang J., Lin Y., Ji Q., Wan J. Roles and mechanisms of interleukin-12 family members in cardiovascular diseases: opportunities and challenges. Front. Pharmacol., 2020; 11: 129. doi: 10.3389/fphar.2020.00129
79. Bobryshev Y.V., Sobenin I.A., Orekhov A.N., Chistiakov D.A. Novel anti-inflammatory interleukin-35 as an emerging target for antiatherosclerotic therapy. Curr. Pharm. Des., 2015 ;21: 1147–1151. doi: 10.2174/1381612820666141014123810
80. Kan X., Wu Y., Ma Y., Zhang C., Li P., Wu L., Zhang S., Li Y., Du J. Deficiency of IL-12p35 improves cardiac repair after myocardial infarction by promoting angiogenesis. Cardiovasc. Res., 2016; 109 (2): 249–259. doi: 10.1093/cvr/cvv255
81. Фатхуллина А.Р., Пешкова Ю.О., Кольцова Е.К. Роль цитокинов в развитии атеросклероза. Биохимия, 2016: 81 (11): 1614–1627. doi: 10.1134/S0006297916110134
82. Rossol M., Heine H., Meusch U., Quandt D., Klein C., Sweet M.J., Hauschildt S. LPS-induced cytokine production in human monocytes and macrophages. Crit. Rev. Immunol., 2011; 31 (5): 379– 446. doi: 10.1615/critrevimmunol.v31.i5.20
83. McGeachy M.J., Cua D.J., Gaffen S.L. The IL-17 family of cytokines in health and disease. Immunity, 2019; 50 (4): 892–906. doi: 10.1016/j.immuni.2019.03.021
84. Kidani Y., Bensinger S.J. Reviewing the impact of lipid synthetic flux on Th17 function. Curr. Opin. Immunol., 2017; 46: 121–126. doi: 10.1016/j.coi.2017.03.012
85. Danzaki K., Matsui Y., Ikesue M., Ohta D., Ito K., Kanayama M., Kurotaki D., Morimoto J., Iwakura Y., Yagita H., Tsutsui H., Uede T. Interleukin-17A deficiency accelerates unstable atherosclerotic plaque formation in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2012; 32 (2): 273–280. doi: 10.1161/ATVBAHA.111.229997
86. Erbel C., Dengler T.J., Wangler S., Lasitschka F., Bea F., Wambsganss N., Hakimi M., Böckler D., Katus H.A., Gleissner C.A. Expression of IL-17A in human atherosclerotic lesions is associated with increased inflammation and plaque vulnerability. Basic Res. Cardiol., 2011; 106 (1): 125–134. doi: 10.1007/s00395-010-0135-y
87. González L., Rivera K., Andia M.E., Rodriguez G.M. The IL-1 family and its role in atherosclerosis. Int. J. Mol. Sci., 2022; 24 (1): 17. doi: 10.3390/ijms24010017
88. Gallagher G. Interleukin-19: multiple roles in immune regulation and disease. Cytokine Growth. Factor Rev., 2010; 21 (5): 345–352. doi: 10.1016/j.cytogfr.2010.08.005
89. Gabunia K., Ellison S., Kelemen S., Kako F., Cornwell W.D., Rogers T.J., Datta P.K., Ouimet M., Moore K.J., Autieri M.V. IL-19 halts progression of atherosclerotic plaque, polarizes, and increases cholesterol uptake and efflux in macrophages. Am. J. Pathol., 2016; 186 (5): 1361–1374. doi: 10.1016/j.aj-path.2015.12.023
90. Francis A.A., Pierce G.N. An integrated approach for the mechanisms responsible for atherosclerotic plaque regression. Exp. Clin. Cardiol., 2011; 16 (3): 77–86.
91. Khallou-Laschet J., Varthaman A., Fornasa G., Compain C., Gaston A.T., Clement M., Dussiot M., Levillain O., Graff-Dubois S., Nicoletti A., Caligiuri G. Macrophage plasticity in experimental atherosclerosis. PLoS One, 2010; 5 (1): e8852. doi: 10.1371/journal.pone.0008852
92. Ellison S., Gabunia K., Kelemen S.E., England R.N., Scalia R., Richards J.M., Orr A.W., Traylor J.G. Jr, Rogers T., Cornwell W., Berglund L.M., Goncalves I., Gomez M.F., Autieri M.V. Attenuation of experimental atherosclerosis by interleukin-19. Arterioscler. Thromb. Vasc. Biol., 2013; 33 (10): 2316–2324. doi: 10.1161/ATVBAHA.113.301521
93. Commins S., Steinke J.W., Borish L. The extended IL-10 superfamily: IL-10, IL-19, IL-20, IL-22, IL-24, IL-26, IL-28, and IL-29. J. Allergy Clin. Immunol., 2008; 121 (5): 1108–1111. doi: 10.1016/j.jaci.2008.02.026
94. Hsieh M.Y., Chen W.Y., Jiang M.J., Cheng B.C., Huang T.Y., Chang M.S. Interleukin-20 promotes angiogenesis in a direct and indirect manner. Genes Immun., 2006; 7 (3): 234–242. doi: 10.1038/sj.gene.6364291
95. Xia Q., Xiang X., Patel S., Puranik R., Xie Q., Bao S. Characterisation of IL-22 and interferon-gamma-inducible chemokines in human carotid plaque. Int. J. Cardiol., 2012; 154 (2): 187–189. doi: 10.1016/j.ijcard.2011.10.093
96. Rattik S., Hultman K., Rauch U., Söderberg I., Sundius L., Ljungcrantz I., Hultgеrdh-Nilsson A., Wigren M., Björkbacka H., Fredrikson G.N., Nilsson J. IL-22 affects smooth muscle cell phenotype and plaque formation in apolipoprotein E knockout mice. Atherosclerosis, 2015; 242 (2): 506–514. doi: 10.1016/j.atherosclerosis.2015.08.006
97. Luo J.W., Hu Y., Liu J., Yang H., Huang P. Inter-leukin-22: a potential therapeutic target in atherosclerosis. Mol. Med., 2021; 27: 88. doi: 10.1186/s10020-021-00353-9
98. Che Y., Su Z., Xia L. Effects of IL-22 on cardiovascular diseases. Int. Immunopharmacol., 2020; 81: 106277. doi: 10.1016/j.intimp.2020.106277
99. Evans B.R., Yerly A., van der Vorst E.P.C., Baumgartner I., Schindewolf S.M.B., Döring Y. Inflammatory mediators in atherosclerotic vascular remodeling. Front. Cardiovasc. Med., 2022; 9: 868934. doi: 10.3389/fcvm.2022.868934
100. Shi L., Ji Qi., Liu L., Shi Y., Lu Z., Ye J., Zeng T., Xue Y., Yang Z., Liu Y., Lu J., Huang Xi., Qin Qi., Li T., Lin Y.-Z. IL-22 produced by Th22 cells aggravates atherosclerosis development in ApoE-/-mice by enhancing DC-induced Th17 cell proliferation. J. Cell. Mol. Med., 2020; 24: 3064–3078. doi: 10.1111/jcmm.14967
101. Wang J., Zhao P., Gao Y., Zhang F., Yuan X., Jiao Y., Gong K. The effects of anti-IL-23p19 therapy on atherosclerosis development in ApoE-/-mice. J. Interferon Cytokine Res., 2019; 39 (9): 564–571. doi: 10.1089/jir.2019.0050
102. Subramanian M., Thorp E., Tabas I. Identification of a non-growth factor role for GM-CSF in advanced atherosclerosis: promotion of macrophage apoptosis and plaque necrosis through IL-23 signaling. Circ. Res., 2015; 116 (2): e13–e24. doi: 10.1161/CIRCRESAHA.116.304794
103. Fatkhullina A.R., Peshkova I.O., Dzutsev A., Aghayev T., McCulloch J.A., Thovarai V., Badger J.H., Vats R., Sundd P., Tang H.Y., Kossenkov A.V., Hazen S.L., Trinchieri G., Grivennikov S.I., Koltsova E.K. An interleukin-23-interleukin-22 axis regulates intestinal microbial homeostasis to protect from diet-induced atherosclerosis. Immunity, 2018; 49 (5): 943–957.e9. doi: 10.1016/j.immuni.2018.09.011
104. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med., 2008; 14: 282–289.
105. Lee K.-M., Kang H.A., Park M., Lee H.Y., Song M.J., Ko K., Oh J.W., Kang H.S. Interleukin-24 suppresses the growth of vascular smooth muscle cells by inhibiting H(2)O(2)-induced reactive oxygen species production. Pharmacology, 2012; 90 (5-6): 332–341. doi: 10.1159/000343242
106. Mantani P.T., Dunér P., Bengtsson E., Ljungcrantz I., Sundius L., To F., Nilsson J., Björkbacka H., Fredrikson G.N. Interleukin-25 (IL-25) has a protective role in atherosclerosis development in the aortic arch in mice. J. Biol. Chem., 2018; 293 (18): 6791–6801. doi: 10.1074/jbc.RA117.000292
107. Mantani P.T., Dunér P., Bengtsson E., Alm R., Ljungcrantz I., Söderberg I., Sundius L., To F., Nilsson J., Björkbacka H., Fredrikson G.N. IL-25 inhibits atherosclerosis development in apolipoprotein E deficient mice. PLoS One, 2015; 10 (1): e0117255. doi: 10.1371/journal.pone.0117255
108. Yoshida H., Hunter C.A. The immunobiology of interleukin-27. Annu. Rev. Immunol., 2015; 33: 417– 443. doi: 10.1146/annurev-immunol-032414-112134
109. Koltsova E.K., Kim G., Lloyd K.M., Saris C.J., von Vietinghoff S., Kronenberg M., Ley K. Interleukin-27 receptor limits atherosclerosis in Ldlr-/-mice. Circ. Res., 2012; 111 (10): 1274–1285. doi: 10.1161/CIRCRESAHA.112.277525
110. Hirase T., Hara H., Miyazaki Y., Ide N., Nishimoto-Hazuku A., Fujimoto H., Saris C.J., Yoshida H., Node K. Interleukin 27 inhibits atherosclerosis via immunoregulation of macrophages in mice. Am. J. Physiol. Heart Circ. Physiol., 2013; 305 (3): H420– Н429. doi: 10.1152/ajpheart.00198.2013
111. Park M.H., Song M.J., Cho M.C., Moon D.C., Yoon D.Y., Han S.B., Hong J.T. Interleukin-32 enhances cytotoxic effect of natural killer cells to cancer cells via activation of death receptor 3. Immunology, 2012; 135 (1): 63–72. doi: 10.1111/j.1365-2567.2011.03513.x
112. Zheng C., Zheng L., Yoo J.K., Guo H., Zhang Y., Guo X., Kang B., Hu R., Huang J.Y., Zhang Q., Liu Z., Dong M., Hu X., Ouyang W., Peng J., Zhang Z. Landscape of infiltrating T cells in liver cancer revealed by single-cell sequencing. Cell, 2017; 169 (7): 1342–1356. doi: 10.1016/j.cell.2017.05.035
113. Nold-Petry C.A., Nold M.F., Zepp J.A., Kim S.H., Voelkel N.F., Dinarello C.A. IL-32-dependent effects of IL-1beta on endothelial cell functions. Proc. Natl. Acad. Sci. USA, 2009; 106 (10): 3883–3888. doi: 10.1073/pnas.0813334106
114. Hong J.T., Son D.J., Lee C.K., Yoon D.Y., Lee D.H., Park M.H. Interleukin 32, inflammation and cancer. Pharmacol. Ther., 2017; 174: 127–137. doi: 10.1016/j.pharmthera.2017.02.025
115. Zaidan S.M., Leyre L., Bunet R., Larouche-Anctil E., Turcotte I., Sylla M., Chamberland A., Chartrand-Lefebvre C., Ancuta P., Routy J.P., Baril J.G., Trottier B., MacPherson P., Trottier S., Harris M., Walmsley S., Conway B., Wong A., Thomas R., Kaplan R.C., Landay A.L., Durand M., Chomont N., Tremblay C.L., El-Far M.; Canadian HIV and Aging Cohort Study. Upregulation of IL-32 isoforms in virologically suppressed HIV-infected individuals: potential role in persistent inflammation and transcription from stable HIV-1 reservoirs. J. Acquir. Immune Defic Syndr., 2019; 82 (5): 503–513. doi: 10.1097/QAI.0000000000002185
116. Mohammad-Rezaei M., Ahmadi R., Rafiei A., Khaledifar A., Fattahi S., Samiei-Sefat A., Emami S., Bagheri N. Serum levels of IL-32 in patients with coronary artery disease and its relationship with the serum levels of IL-6 and TNF-α. Mol. Biol. Rep., 2021; 48 (5): 4263–4271. doi: 10.1007/s11033-021-06441-7
117. Yang Z., Shi L., Xue Y., Zeng T., Shi Y., Lin Y., Liu L. Interleukin-32 increases in coronary arteries and plasma from patients with coronary artery disease. Clin .Chim. Acta, 2019; 497: 104–109. doi: 10.1016/j.cca.2019.07.019
118. Heinhuis B., Popa C.D., van Tits B.L., Kim S.H., Zeeuwen P.L., van den Berg W.B., van der Meer J.W., van der Vliet J.A., Stalenhoef A.F., Dinarello C.A., Netea M.G., Joosten L.A. Towards a role of interleukin-32 in atherosclerosis. Cytokine, 2013; 64 (1): 433–440. doi: 10.1016/j.cyto.2013.05.002
119. Choi Y.S., Choi H.J., Min J.K., Pyun B.J., Maeng Y.S., Park H., Kim J., Kim Y.M., Kwon Y.G. Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production. Blood, 2009; 114 (14): 3117– 3126. doi: 10.1182/blood-2009-02-203372
120. Cao K., Liao X., Lu J., Yao S., Wu F., Zhu X., Shi D., Wen S., Liu L., Zhou H. IL-33/ST2 plays a critical role in endothelial cell activation and microglia-mediated neuroinflammation modulation. J. Neuroinflammation., 2018; 15 (1): 136. doi: 10.1186/s12974-018-1169-6
121. McLaren J.E., Michael D.R., Salter R.C., Ashlin T.G., Calder C.J., Miller A.M., Liew F.Y., Ramji D.P. IL-33 reduces macrophage foam cell formation. J. Immunol., 2010; 185 (2): 1222–1229. doi: 10.4049/jimmunol.1000520
122. Zhang H.F., Wu M.X., Lin Y.Q., Xie S.L., Huang T.C., Liu P.M., Nie R.Q., Meng Q.Q., Luo N.S., Chen Y.X., Wang J.F. IL-33 promotes IL-10 production in macrophages: a role for IL-33 in macrophage foam cell formation. Exp. Mol. Med., 2017; 49 (11): e388. doi: 10.1038/emm.2017.183
123. Zheng X., Gong L., Zhang S., Wu W. Epicardial adipose tissue thickness and plasma interleukin-35 predict acute myocardial infarction in patients with coronary artery disease. Int. J. Clin. Exp. Med., 2018; 11: 13456–13467.
124. Jia D., Jiang H., Weng X., Wu J., Bai P., Yang W., Wang Z., Hu K., Sun A., Ge J. Interleukin-35 promotes macrophage survival and improves wound healing after myocardial infarction in mice. Circ. Res., 2019; 124 (9): 1323–1336. doi: 10.1161/CIRCRESAHA
125. Liu J., Lin J., He S., Wu C., Wang B., Liu J., Duan Y., Liu T., Shan S., Yang K., Dong N., Ji Q., Huang K., Li D. Transgenic overexpression of IL-37 protects against atherosclerosis and strengthens plaque stability. Cell. Physiol. Biochem., 2018; 45 (3): 1034– 1050. doi: 10.1159/000487344
126. McCurdy S., Liu C.A., Yap J., Boisvert W.A. Potential role of IL-37 in atherosclerosis. Cytokine, 2017; 122: 154169. doi: 10.1016/j.cyto.2017.09.025
127. Chai M., Ji Q., Zhang H., Zhou Y., Yang Q., Zhou Y., Guo G., Liu W., Han W., Yang L., Zhang L., Liang J., Liu Y., Shi D., Zhao Y. The protective effect of interleukin-37 on vascular calcification and atherosclerosis in apolipoprotein E-deficient mice with diabetes. J. Interferon Cytokine Res., 2015; 35 (7): 530–539. doi: 10.1089/jir.2014.0212
128. Flusberg D.A., Sorger P.K. Surviving apoptosis: life-death signaling in single cells. Trends Cell. Biol., 2015; 25 (8): 446–458. doi: 10.1016/j.tcb.2015.03.003
129. Ślebioda T.J., Kmieć Z. Tumour necrosis factor superfamily members in the pathogenesis of inflammatory bowel disease. Mediators Inflamm., 2014; 2014: 325129. doi: 10.1155/2014/325129
130. Nash M., McGrath J.P., Cartland S.P., Patel S., Kavurma M.M. Tumour necrosis factor superfamily members in ischaemic vascular diseases. Cardiovasc. Res., 2019; 115 (4): 713–720. doi: 10.1093/cvr/cvz042
131. Mackesy D.Z., Goalstone M.L. Extracellular signal-regulated kinase-5: Novel mediator of insulin and tumor necrosis factor α-stimulated vascular cell adhesion molecule-1 expression in vascular cells. J. Diabetes, 2014; 6 (6): 595–602. doi: 10.1111/1753-0407.12132
132. Hashizume M., Mihara M. Atherogenic effects of TNF-α and IL-6 via up-regulation of scavenger receptors. Cytokine, 2012; 58 (3): 424–430. doi: 10.1016/j.cyto.2012.02.010
133. Boshuizen M.C., de Winther M.P. Interferons as essential modulators of atherosclerosis. Arterioscler. Thromb. Vasc. Biol., 2015; 35 (7): 1579–1588. doi: 10.1161/ATVBAHA.115.305464
134. Zhou Q.D., Chi X., Lee M.S., Hsieh W.Y., Mkrtchyan J.J., Feng A.C., He C., York A.G., Bui V.L., Kronenberger E.B., Ferrari A., Xiao X., Daly A.E., Tarling E.J., Damoiseaux R., Scumpia P.O., Smale S.T., Williams K.J., Tontonoz P., Bensinger S.J. Interferon-mediated reprogramming of membrane cholesterol to evade bacterial toxins. Nat. Immunol., 2020; 21 (7): 746–755. doi: 10.1038/s41590-020-0695-4
135. Ranjbaran H., Sokol S.I., Gallo A., Eid R.E., Iakimov A.O, D’Alessio A., Kapoor J.R., Akhtar S., Howes C.J., Aslan M., Pfau S., Pober J.S., Tellides G. An inflammatory pathway of IFN-gamma production in coronary atherosclerosis. J. Immunol., 2007; 178: 592–604. doi: 10.4049/jimmunol.178.1.592
136. Serralheiro P., Soares A., Costa Almeida C.M., Verde I. TGF-β1 in vascular wall pathology: unraveling chronic venous insufficiency pathophysiology. Int. J. Mol. Sci., 2017; 18 (12): 2534. doi: 10.3390/ijms18122534
137. Chen P.Y., Qin L., Li G., Wang Z., Dahlman J.E., Malagon-Lopez J., Gujja S., Cilfone N.A., Kauffman K.J., Sun L., Sun H., Zhang X., Aryal B., Canfran-Duque A., Liu R., Kusters P., Sehgal A., Jiao Y., Anderson D.G., Gulcher J., Fernandez-Hernando C., Lutgens E., Schwartz M.A., Pober J.S., Chittenden T.W., Tellides G., Simons M.. Endothelial TGF-β signalling drives vascular inflammation and atherosclerosis. Nat. Metab., 2019; 1: 912–926. doi: 10.1038/s42255-019-0102-3
138. Ligi D., Croce L., Mosti G., Raffetto J.D., Mannello F. chronic venous insufficiency: transforming growth factor-β isoforms and soluble endoglin concentration in different states of wound healing. Int. J. Mol. Sci., 2017; 18 (10): 2206. doi: 10.3390/ijms18102206
139. Serralheiro P., Soares A., Costa Almeida C.M., Verde I. TGF-β1 in vascular wall pathology: unraveling chronic venous insufficiency pathophysiology. Int. J. Mol. Sci., 2017; 18: 2534. doi: 10.3390/ijms18122534
140. Gong D., Shi W., Yi S.-ju, Chen H., Groffen J., Heisterkamp N. TGFβ signaling plays a critical role in promoting alternative macrophage activation BMC. Immunology, 2012; 13: 31. doi: 10.1186/1471-2172-13-31
141. Ramji D.P., Davies T.S. Cytokines in atherosclerosis: Key players in all stages of disease and promising therapeutic targets. Cytokine Growth Factor Rev., 2015; 26 (6): 673–685. doi: 10.1016/j.cytogfr.2015.04.003
142. Adela R., Banerjee S.K. GDF-15 as a target and biomarker for diabetes and cardiovascular diseases: a translational prospective. J. Diabetes Res., 2015; 2015: 490842. doi: 10.1155/2015/490842
143. Wischhusen J., Melero I., Fridman W.H. Growth/differentiation factor-15 (GDF-15): from biomarker to novel targetable immune checkpoint. Front. Immunol., 2020; 11: 951. doi: 10.3389/fimmu.2020.00951
144. Fredriksson L., Li H., Eriksson U. The PDGF family: four gene products form five dimeric isoforms. Cytokine Growth Factor Reviews, 2004; 115: 97–204. doi: 10.1016/j.cytogfr.2004.03.007
145. Battegay E. J., Rupp J., Iruela-Arispe L., Sage E.H., Pech M. PDGF-BB modulates endothelial proliferation and angiogenesis in vitro via PDGF beta-receptors. J. Cell. Biol., 1994; 125: 917–928. doi: 10.1083/jcb.125.4.917
146. Hellberg C., Ostman A., Heldin C.H. PDGF and vessel maturation. Recent Results Cancer Res., 2010; 180: 103–114. doi: 10.1007/978-3-540-78281-0_7
147. Martino M.M., Brkic S., Bovo E., Burger M., Schaefer D.J., Wolff T., Gürke L., Briquez P.S., Larsson H.M., Gianni-Barrera R., Hubbell J.A., Banfi A. Extracellular matrix and growth factor engineering for controlled angiogenesis in regenerative medicine. Front. Bioeng. Biotechnol., 2015; 3: 45. doi: 10.3389/fbioe.2015.00045
148. Kalra K., Eberhard J., Farbehi N., Chong J.J., Xaymardan M. Role of PDGF-A/B ligands in cardiac repair after myocardial infarction. Front. Cell Dev. Biol., 2021; 9: 669188. doi: 10.3389/fcell.2021.669188
149. Martínez C.E., Smith C., Palma Alvarado V.A. The influence of platelet-derived products on angiogenesis and tissue repair: A concise update. Front. Physiol., 2015; 6: 159973. doi: 10.3389/fphys.2015.00290
150. Kemp S.S., Lin P.K., Sun Z., Castaсo M.A., Yrigoin K., Penn M.R., Davis G.E. Molecular basis for pericyte-induced capillary tube network assembly and maturation. Front. Cell Dev. Biol., 2022; 10: 943533. doi: 10.3389/fcell.2022.943533
151. Stratman A.N., Davis G.E. Endothelial cell-pericyte interactions stimulate basement membrane matrix assembly: influence on vascular tube remodeling, maturation, and stabilization. Microsc. Microanal., 2012; 18 (1): 68–80. doi: 10.1017/S1431927611012402
152. Goumans M.J., Ten Dijke P. TGF-β signaling in control of cardiovascular function. Cold Spring. Harb. Perspect. Biol., 2018; 10 (2): a022210. doi: 10.1101/cshperspect.a022210
153. Shah P., Keppler L., Rutkowski J. A review of platelet derived growth factor playing pivotal role in bone regeneration. J. Oral Implantol., 2014; 40 (3): 330–340. doi: 10.1563/AAID-JOI-D-11-00173
154. Bolshakov I.N., Gornostaev L.M., Fominykh O.I., Svetlakov A.V. Synthesis, chemical and biomedical aspects of the use of sulfated chitosan. Polymers (Basel), 2022; 14 (16): 3431. doi: 10.3390/polym14163431
155. Калинин Р.Е., Грязнов С.В., Никифоров А.А., Камаев А.А., Швальб А.П., Слепнев А.А. Полиморфизм гена синтазы азота и эндотелина-1 при хронической венозной недостаточности. Российский медико-биологический вестник имени академика И.П. Павлова, 2015; 16 (4): 97–102. doi: 10.17816/PAVLOVJ2015497-102
156. Pavlides S., Gutierrez-Pajares J.L., Katiyar S., Jasmin J.F., Mercier I., Walters R., Pavlides C., Pestell R.G., Lisanti M.P., Frank P.G. Caveolin-1 regulates the anti-atherogenic properties of macrophages. Cell. Tissue Res., 2014; 358 (3): 821–831. doi: 10.1007/s00441-014-2008-4
157. Bednarska-Chabowska D., Adamiec R., Pawlikowski A., Adamiec J. Selected problems of endothelial functions. II. The role of the selectines in the damage of vascular endothelium. Pol. Merkur. Lekarski, 2002; 12: 329–332.
158. Signorelli S.S., Anzaldi M., Libra M., Navolanic P.M., Malaponte G., Mangano K., Quattrocchi C., di Marco R., Fiore V., Neri S. Plasma levels of inflammatory biomarkers in peripheral arterial disease: results of a cohort study. Angiology, 2016; 67 (9): 870–874. doi: 10.1177/0003319716633339
159. Al-Ghurabi M.E., Muhi A.A., Al-Mudhafar D.H. Vascular cell adhesion molecule-1 and endothelial leukocyte adhesion molecule-1 as markers of atherosclerosis of NIDDM. Amer. J. Life Sci., 2015; 3 (1): 22–26. doi: 10.11648/j.ajls.20150301.15
160. Tsai M.K., Hsieh C.C., Kuo H.F., Lee M.S., Huang M.Y., Kuo C.H., Hung C.H. Effect of prostaglandin I2 analogs on monocyte chemoattractant protein-1 in human monocyte and macrophage. Clin. Exp. Med., 2015; 15 (3): 245–253. doi: 10.1007/s10238-014-0304-7
161. Qiao J.H., Tripathi J., Mishra N.K., Cai Y., Tripathi S., Wang X.P., Imes S., Fishbein M.C., Clinton S.K., Libby P., Lusis A.J., Rajavashisth T.B. Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am. J. Pathol., 1997; 150: 1687–1699.
162. Kleinbongard P., Heusch G., Schulz R. TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol. Ther., 2010; 127: 295–314. doi: 10.1016/j.pharmthera.2010.05.002
163. Cossette É., Cloutier I., Tardif K., DonPierre G., Tanguay J.F. Estradiol inhibits vascular endothelial cells pro-inflammatory activation induced by C-reactive protein. Mol. Cell. Biochem., 2013; 373 (1-2): 137–147. doi: 10.1007/s11010-012-1482-9.
164. Wang L., Tang C. Targeting platelet in atherosclerosis plaque formation: current knowledge and future perspectives. Int. J. Mol. Sci., 2020; 21: 9760. doi: 10.3390/ijms21249760
165. Folco E.J., Sukhova G.K., Quillard T., Libby P. Moderate hypoxia potentiates interleukin-1β production in activated human macrophages. Circ. Res., 2014; 115 (10): 875–883. doi: 10.1161/CIRCRESA-HA.115.304437
166. Pagano P.J., Gutterman D.D. The adventitia: the outs and ins of vascular disease. Cardiovasc. Res., 2007; 75 (4): 636–639. doi: 10.1016/j.cardiores.2007.07.006
167. Edsfeldt A., Grufman H., Asciutto G., Nitulescu M., Persson A., Nilsson M., Nilsson J., Gonзalves I. Circulating cytokines reflect the expression of pro-inflammatory cytokines in atherosclerotic plaques. Atherosclerosis, 2015; 241 (2): 443–449. doi: 10.1016/j.atherosclerosis.2015.05.019
168. Voloshyna I., Littlefield M.J., Reiss A.B. Atherosclerosis and interferon-γ: new insights and therapeutic targets. Trends Cardiovasc. Med., 2014; 24 (1): 45–51. doi: 10.1016/j.tcm.2013.06.003
169. Eriksson E.E. Intravital microscopy on atherosclerosis in apolipoprotein e-deficient mice establishes microvessels as major entry pathways for leukocytes to advanced lesions. Circulation, 2011; 124 (19): 2129– 2138. doi: 10.1161/CIRCULATIONAHA.111.030627
170. Fallah A., Sadeghinia A., Kahroba H., Samadi A., Heidari H.R., Bradaran B., Zeinali S., Molavi O. Therapeutic targeting of angiogenesis molecular pathways in angiogenesis-dependent diseases. Biomed. Pharmacother., 2019; 110: 775–785. doi: 10.1016/j.biopha.2018.12.022
171. Stenmark K., Yeager M., Kasmi K.C., Nozik-Grayck E., Gerasimovskaya E.V., Li M. The adventitia: essential regulator of vascular structure and function. Ann. Rev. Pysiol., 2013; 75: 23–47. doi: 10.1146/annurev-physiol-030212-183802
172. Tang W., Liu Z., Si Y. Tunica arterial adventitia: a new exploration in intimal hyperplasia. J. Vasc. Med. Surg., 2013; 1: 108. doi:10.4172/2329-6925.1000108
173. Campbell K.A., Lipinski M.J., Doran A.C., Skaflen M.D., Fuster V., McNamara C.A. Lymphocytes and adventitial immune response in atherosclerosis. Circ. Res., 2012; 110: 889–890. doi: 10.1161/CIR-CRESAHA.111.263186
174. Ogeng’o J., Ominde B.S., Ongeti K., Olabu B., Obimbo M., Mwachaka P. Reappraisal of the structure of arterial tunica adventitia and its involvement in atherosclerosis. Anatomy Journal of Africa, 2020; 6: 824–833. doi: 10.4314/aja.v6i1.150685
175. Ogeng’o J.A., Maseghe P., Ongeti K., Obimbo M., Olabu B. Tunica adventitia of the aorta in an active vascular compartment. Anat. J. Afr., 2015; 4: 617–623
176. Mulligan-Kehoe M.J., Simons M. Vasa vasora in normal and diseased arteries. Circulation, 2014; 129:,2557– 2566. doi: 10.1161/CIRCULATIONAHA.113.007189
177. Fugundes A., Pereira A.H., Correa K., de Oliveira M.T., Rodriguez R. Effects of removal of the adventitia of the descending aorta and structural alterations in the tunica media in pigs. Rev. Col. Bras. Circ., 2012; 39: 133–138.
178. Wang J.L., Ma S.Q., Li L., Liu G.Q., Hu W.C., Ma R. Correlation of inflammatory cells in adventitia and formation and extending of atherosclerotic lesions in coronary artery of apolipoprotein E Knockout mice. Chin. J. Physiol., 2013; 56: 77–82. doi: 10.4077/CJP.2013.BAA080
179. Tian J., Hu S., Sun Y., Yu H., Han X., Cheng W., Ban X., Zhang S., Yu B., Jang I.K. Vasa vasorum and plaque progression, and responses to atorvastatin in a rabbit model of atherosclerosis: contrast enhanced ultrasound imaging and intravascular ultrasound study. Heart, 2013; 99: 48–54. doi: 10.1136/heartjnl-2012-302775
180. Fitzgibbons T.P., Czech M.P. Epicardial and perivascular adipose tissues and their influence on cardiovascular disease: basic mechanisms and clinical associations. J. Am. Heart Assoc., 2014; 3: e000582. doi: 10.1161/jaha.113.000582
181. Huh J.Y., Park Y.J., Ham M., Kim J.B. Crosstalk between adipocytes and immune cells in adipose tissue inflammation and metabolic dysregulation in obesity. Mol. Cells, 2014; 37: 365–371. doi: 10.14348/molcells.2014.0074
Рецензия
Для цитирования:
Большаков И.Н., Шиндякин Д.В., Кириченко А.К., Бахшян В.А., Архипкин С.В. Цитокиновые факторы роста в регуляции ангиогенеза и атерогенного воспаления в сосудистой стенке. Аналитический обзор. Часть 1. Атеросклероз. 2025;21(1):60-91. https://doi.org/10.52727/2078-256X-2025-21-1-60-91
For citation:
Bolshakov I.N., Shindyakin D.V., Kirichenko A.K., Bahshyan V.A., Arkhipkin S.V. Cytokine growth factors in the regulation of angiogenesis and atherogenic inflammation in the vascular wall. The role of polysaccharide polymers. Analytical review. Part 1. Ateroscleroz. 2025;21(1):60-91. (In Russ.) https://doi.org/10.52727/2078-256X-2025-21-1-60-91