The role of interleukin-27 in atherosclerotic cardiovascular diseases: A review

Cover Page

Cite item

Full Text

Abstract

The main cause of many cardiovascular diseases is atherosclerosis. The atherosclerotic process, manifested by acute vascular accidents, such as myocardial and/or cerebral infarction, or chronic ischemic conditions, such as coronary heart disease and cerebrovascular disease, is essentially a systemic inflammatory process. The significant role of T-cells, macrophages, neutrophils and cytokines in this pathological process has been proven. The presented literature review indicates the potentially important diagnostic and prognostic value of the interleukin-27 assessment. It is expected that further scientific and clinical studies will demonstrate the possibility of using this cytokine as an additional laboratory tool for the diagnosis, risk stratification and prediction of cardiovascular events in patients with a cardiac profile.

About the authors

Amina M. Alieva

Pirogov Russian National Research Medical University

Author for correspondence.
Email: amisha_alieva@mail.ru
ORCID iD: 0000-0001-5416-8579

Cand. Sci. (Med.)

Russian Federation, Moscow

Natalia V. Teplova

Pirogov Russian National Research Medical University

Email: editor@omnidoctor.ru
ORCID iD: 0000-0002-7181-4680

D. Sci. (Med.), Prof.

Russian Federation, Moscow

Elena V. Reznik

Pirogov Russian National Research Medical University

Email: elenaresnik@gmail.com
ORCID iD: 0000-0001-7479-418X

D. Sci. (Med.), Assoc. Prof.

Russian Federation, Moscow

Leyla R. Sarakaeva

Almazov National Medical Research Center

Email: editor@omnidoctor.ru

Graduate Student, pediatric endocrinologist

Russian Federation, Saint Petersburg

Alik M. Rahaev

Berbekov Kabardino-Balkarian State University

Email: alikrahaev@yandex.ru
ORCID iD: 0000-0001-9601-1174

D. Sci. (Med.)

Russian Federation, Nalchik

Dzhannet A. Elmurzaeva

Berbekov Kabardino-Balkarian State University

Email: jannet.elmurzaeva@yandex.ru
ORCID iD: 0000-0002-5640-6638

Cand. Sci. (Med.)

Russian Federation, Nalchik

Makhty I. Akkiev

Berbekov Kabardino-Balkarian State University

Email: editor@omnidoctor.ru

Assistant

Russian Federation, Nalchik

Madina Ya. Shavaeva

Berbekov Kabardino-Balkarian State University

Email: editor@omnidoctor.ru

Deputy Director of the Medical College

Russian Federation, Nalchik

Maryana A. Akkieva

Center of Allergology and Immunology

Email: marakkieva@mail.ru

Deputy Chief doctor

Russian Federation, Nalchik

Igor G. Nikitin

Pirogov Russian National Research Medical University

Email: igor.nikitin.64@mail.ru

D. Sci. (Med.), Prof.

Russian Federation, Moscow

References

  1. Шляхто E.В., Звартау Н.Э., Виллевальде C.В. и др. Система управления сердечно-сосудистыми рисками: предпосылки к созданию, принципы организации, таргетные группы. Российский кардиологический журнал. 2019;24(11):69-82 [Shlyakhto EV, Zvartau NE, Villevalde SV, et al. Cardiovascular risk management system: prerequisites for developing, organization principles, target groups. Russian Journal of Cardiology. 2019;24(11):69-82 (in Russian)]. doi: 10.15829/1560-4071-2019-11-69-82
  2. GBD 2015 Risk Factors Collaborators. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990–2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388(10053):1659-724. doi: 10.1016/S0140-6736(16)31679-8
  3. Li H, Zou J, Yu XH, et al. Zinc finger E-box binding homeobox 1 and atherosclerosis: New insights and therapeutic potential. J Cell Physiol. 2021;236(6):4216-30. doi: 10.1002/jcp.30177
  4. Фадеев Г.А, Фатыхов Р.Г., Цибулькин Н.А., и др. Воспалительные механизмы в генезе атеросклероза. Вестник современной клинической медицины. 2020;13(6):62-7 [Fadeev GA, Fatykhov RG, Tsibulkin NA, et al. Inflammatory mechanisms in genesis of atherosclerosis. The Bulletin of Contemporary Clinical Medicine. 2020;13(6):62-7 (in Russian)]. doi: 10.20969/VSKM.2020.13(6).62-67
  5. Jafarizade M, Kahe F, Sharfaei S, et al. The role of interleukin-27 in atherosclerosis: A contemporary review. Cardiology. 2021;146(4):517-30. doi: 10.1159/000515359
  6. Witztum JL, Lichtman AH. The influence of innate and adaptive immune responses on atherosclerosis. Annu Rev Pathol. 2014;9:73-102. doi: 10.1146/annurev-pathol-020712-163936
  7. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med. 2011;17(11):1410-22. doi: 10.1038/nm.2538
  8. Posadas-Sanchez R, Perez-Hernandez N, Rodriguez-Perez JM, et al. Interleukin-27 polymorphisms are associated with premature coronary artery disease and metabolic parameters in the Mexican population: the genetics of atherosclerotic disease (GEA) Mexican study. Oncotarget. 2017;8(38):64459-70. doi: 10.18632/oncotarget.16223
  9. Pflanz S, Timans JC, Cheung J, et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4+ T cells. Immunity. 2002;16(6):779-90. doi: 10.1016/s1074-7613(02)00324-2
  10. Meka RR, Venkatesha SH, Dudics S, et al. IL-27-induced modulation of autoimmunity and its therapeutic potential. Autoimmun Rev. 2015;14(12):1131-41. doi: 10.1016/j.autrev.2015.08.001
  11. Vargas-Alarcon G, Perez-Hernández N, Rodríguez-Perez JM, et al. Interleukin 27 polymorphisms, their association with insulin resistance and their contribution to subclinical atherosclerosis. The GEA Mexican study. Cytokine. 2019;114:32-7. doi: 10.1016/j.cyto.2018.11.028
  12. Caveney NA, Glassman CR, Jude KM, et al. Structure of the IL-27 quaternary receptor signaling complex. Elife. 2022;11:e78463. doi: 10.7554/eLife.78463
  13. Han L, Chen Z, Yu K, et al. Interleukin 27 signaling in rheumatoid arthritis patients: Good or evil? Front Immunol. 2022;12:787252. doi: 10.3389/fimmu.2021.787252
  14. Miteva K, Baptista D, Montecucco F, et al. Cardiotrophin-1 deficiency abrogates atherosclerosis progression. Sci Rep. 2020;10(1):5791. doi: 10.1038/s41598-020-62596-6
  15. Chen Y, Zeng J, Zhang R, et al. Effect of interleukin-27 genetic variants on atrial fibrillation susceptibility. Genet Test Mol Biomarkers. 2017;21(2):97-101. doi: 10.1089/gtmb.2016.0219
  16. Ye J, Wang Y, Wang Z, et al. 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
  17. Hibbert L, Pflanz S, De Waal Malefyt R, et al. IL-27 and IFN-alpha signal via Stat1 and Stat3 and induce T-bet and IL-12Rbeta2 in naive T cells. J Interferon Cytokine Res. 2003;23(9):513-22. doi: 10.1089/10799900360708632
  18. Hunter CA, Kastelein R. Interleukin-27: Balancing protective and pathological immunity. Immunity. 2012;37(6):960-9. doi: 10.1016/j.immuni.2012.11.003
  19. Moon SJ, Park JS, Heo YJ, et al. In vivo action of IL-27: Reciprocal regulation of Th17 and Treg cells in collagen-induced arthritis. Exp Mol Med. 2013;45(10):e46. doi: 10.1038/emm.2013.89
  20. Kurdi M, Zgheib C, Booz GW. Recent developments on the crosstalk between STAT3 and inflammation in heart function and disease. Front Immunol. 2018;9:3029. doi: 10.3389/fimmu.2018.03029
  21. Lucas S, Ghilardi N, Li J, de Sauvage FJ. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc Natl Acad Sci U S A. 2003;100(25):15047-52. doi: 10.1073/pnas.2536517100
  22. Yoshimoto T, Yoshimoto T, Yasuda K, et al. IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J Immunol. 2007;179(7):4415-23. doi: 10.4049/jimmunol.179.7.4415
  23. Bosmann M, Ward PA. Modulation of inflammation by interleukin-27. J Leukoc Biol. 2013;94(6):1159–65. doi: 10.1189/jlb.0213107
  24. Jones GW, Hill DG, Cardus A, Jones SA. IL-27: A double agent in the IL-6 family. Clin Exp Immunol. 2018;193(1):37-46. doi: 10.1111/cei.13116
  25. Ma N, Fang Y, Xu R, et al. Ebi3 promotes T- and B-cell division and differentiation via STAT3. Mol Immunol. 2019;107:61-70. doi: 10.1016/j.molimm.2019.01.009
  26. Dai L, Li Z, Tao Y, et al. Emerging roles of suppressor of cytokine signaling 3 in human cancers. Biomed Pharmacother. 2021;144:112262. doi: 10.1016/j.biopha.2021.112262
  27. Owaki T, Asakawa M, Morishima N, et al. STAT3 is indispensable to IL-27-mediated cell proliferation but not to IL-27-induced Th1 differentiation and suppression of proinflammatory cytokine production. J Immunol. 2008;180(5):2903-11. doi: 10.4049/jimmunol.180.5.2903
  28. Hirano T, Ishihara K, Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene. 2000;19(21):2548-56. doi: 10.1038/sj.onc.1203551
  29. Qiu HN, Liu B, Liu W, Liu S. Interleukin-27 enhances TNF-α-mediated activation of human coronary artery endothelial cells. Mol Cell Biochem. 2016;411(1-2):1-10. doi: 10.1007/s11010-015-2563-3
  30. Jafarzadeh A, Nemati M, Rezayati MT. Serum levels of interleukin (IL)-27 in patients with ischemic heart disease. Cytokine. 2011;56(2):153-6. doi: 10.1016/j.cyto.2011.06.014
  31. Zhu L, Lin X, Chen M. LncRNA NEAT1 correlates with Th17 cells and proinflammatory cytokines, also reflects stenosis degree and cholesterol level in coronary heart disease patients. J Clin Lab Anal. 2022;36(6):e23975. doi: 10.1002/jcla.23975
  32. Mease P, van den Bosch F. IL-23 and axial disease: Do they come together? Rheumatology (Oxford). 2021;60(Suppl. 4):iv28-iv33. doi: 10.1093/rheumatology/keab617
  33. Baldrighi M, Mallat Z, Li X. NLRP3 inflammasome pathways in atherosclerosis. Atherosclerosis. 2017;267:127-38. doi: 10.1016/j.atherosclerosis.2017.10.027
  34. Petes C, Wynick C, Guzzo C, et al. IL-27 enhances LPS-induced IL-1β in human monocytes and murine macrophages. J Leukoc Biol. 2017;102(1):83-94. doi: 10.1189/jlb.3A0316-098R
  35. Gregersen I, Sandanger O, Askevold ET, et al. Interleukin 27 is increased in carotid atherosclerosis and promotes NLRP3 inflammasome activation. PLoS One. 2017;12(11):e0188387. doi: 10.1371/journal.pone.0188387
  36. Guzzo C, Ayer A, Basta S, et al. IL-27 enhances LPS-induced proinflammatory cytokine production via upregulation of TLR4 expression and signaling in human monocytes. J Immunol. 2012;188(2):864-73. doi: 10.4049/jimmunol.1101912
  37. Jin W, Zhao Y, Yan W, et al. Elevated circulating interleukin-27 in patients with coronary artery disease is associated with dendritic cells, oxidized low-density lipoprotein, and severity of coronary artery stenosis. Mediators Inflamm. 2012;2012:506283. doi: 10.1155/2012/506283
  38. Fu H, Tang YY, Ouyang XP, et al. Interleukin-27 inhibits foam cell formation by promoting macrophage ABCA1 expression through JAK2/STAT3 pathway. Biochem Biophys Res Commun. 2014;452(4):881-7. doi: 10.1016/j.bbrc.2014.08.120
  39. Phan WL, Huang YT, Ma MC. Interleukin-27 protects cardiomyocyte-like H9c2 cells against metabolic syndrome: Role of STAT3 signaling. Biomed Res Int. 2015;2015:689614. doi: 10.1155/2015/689614
  40. Tanaka T, Obana M, Mohri T, et al. Interleukin-27 induces the endothelial differentiation in Sca-1+ cardiac resident stem cells. Cytokine. 2015;75(2):365-72. doi: 10.1016/j.cyto.2015.06.009
  41. Koltsova EK, Kim G, Lloyd KM, et al. Interleukin-27 receptor limits atherosclerosis in Ldlr-/- mice. Circ Res. 2012;111(10):1274-85. doi: 10.1161/CIRCRESAHA.112.277525
  42. Hirase T, Hara H, Miyazaki Y, et al. Interleukin 27 inhibits atherosclerosis via immunoregulation of macrophages in mice. Am J Physiol Heart Circ Physiol. 2013;305(3):H420-9. doi: 10.1152/ajpheart.00198.2013
  43. Ma MC, Wang BW, Yeh TP, et al. Interleukin-27, a novel cytokine induced by ischemia-reperfusion injury in rat hearts, mediates cardioprotective effects via the gp130/STAT3 pathway. Basic Res Cardiol. 2015;110(3):22. doi: 10.1007/s00395-015-0480-y
  44. Пешкова Ю.О., Хорева М.В., Ганковская Л.В., Кольцова Е.К. Анализ количества и функциональной активности Т-клеток в аневризме брюшной аорты у мышей с отсутствием рецептора ИЛ-27. Иммунология. 2022;43(1):44-53 [Peshkova IО, Khoreva MV, Gankovskaya LV, Koltsova EK. Analysis of the number and functional activity of T cells in AAA in mice lacking the IL-27 receptor. Immunology. 2022;43(1):44-53 (in Russian)]. doi: 10.33029/0206-4952-2022-43-1-44-53
  45. Liu B, Fu Q, Yan QN, et al. Value of biochemical marker detection in risk stratification in patients with acute coronary syndrome. Nan Fang Yi Ke Da Xue Xue Bao. 2010;30(5):1015-9 (in Chinese). PMID: 20501382
  46. Lin Y, Huang Y, Lu Z, et al. Decreased plasma IL-35 levels are related to the left ventricular ejection fraction in coronary artery diseases. PLoS One. 2012;7(12):e52490. doi: 10.1371/journal.pone.0052490
  47. Wang Y, Zhou C, Yu T, Zhao F. Correlation between changes in serum RBP4, hs-CRP, and IL-27 levels and rosuvastatin in the treatment of coronary heart disease. J Healthc Eng. 2021;2021:8476592. doi: 10.1155/2021/8476592
  48. Miura K, Saita E, Suzuki-Sugihara N, et al. Plasma interleukin-27 levels in patients with coronary artery disease. Medicine (Baltimore). 2017;96(43):e8260. doi: 10.1097/MD.0000000000008260
  49. Ye J, Wang Y, Wang Z, et al. The expression of IL-12 family members in patients with hypertension and its association with the occurrence of carotid atherosclerosis. Mediators Inflamm. 2020;2020:2369279. doi: 10.1155/2020/2369279
  50. Iravani Saadi M, Salami J, Abdi H, et al. Expression of interleukin 1, interleukin 27, and TNF α genes in patients with ischemic cardiomyopathy versus idiopathic dilated cardiomyopathy: A case-control study. Health Sci Rep. 2022;5(4):e701. doi: 10.1002/hsr2.701
  51. Алиева А.М., Алмазова И.И., Пинчук Т.В., и др. Значение копептина в диагностике и прогнозе течения сердечно-сосудистых заболеваний. Клиническая медицина. 2020;98(3):203-9 [Aliyeva AM, Almazova II, Pinchuk TV, et al. The value of copeptin in the diagnosis and prognosis of cardiovascular diseases. Clinical Medicine. 2020;98(3):203-9 (in Russian)]. doi: 10.30629/0023-2149-2020-98-3-203-209
  52. Алиева А.М., Алмазова И.И., Пинчук Т.В., и др. Фракталкин и сердечно-сосудистые заболевания. Consilium Medicum. 2020;22(5):83-6 [Aliyeva AM, Almazova II, Pinchuk TV, et al. Fractalkin and cardiovascular diseases. Consilium Medicum. 2020;22(5):83-6 (in Russian)]. doi: 10.26442/20751753.2020.5.200186
  53. Алиева А.М., Байкова И.Е., Кисляков В.А., и др. Галектин-3: диагностическая и прогностическая ценность определения у пациентов с хронической сердечной недостаточностью. Терапевтический архив. 2019;91(9):145-9 [Aliyeva AM, Baykova IE, Kislyakov VA, et al. Galactin-3: diagnostic and prognostic value in patients with chronic heart failure. Ter Arkh. 2019;91(9):145-9 (In Russian)]. doi: 10.26442/00403660.2019.09.000226
  54. Алиева А.М., Пинчук Т.В., Алмазова И.И., и др. Клиническое значение определения биомаркера крови ST2 у больных с хронической сердечной недостаточностью. Consilium Medicum. 2021;23(6):522-6 [Aliyeva AM, Pinchuk TV, Almazova II, et al. Сlinical value of blood biomarker ST2 in patients with chronic heart failure. Consilium Medicum. 2021;23(6):522-6 (in Russian)]. doi: 10.26442/20751753.2021.6.200606

Copyright (c) 2023 Consilium Medicum

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies