Участие тандема «тучная клетка – нейрон» в регуляции работы сердца при сердечно-сосудистых патологиях

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Аннотация

Данный обзор посвящен изложению новых данных об участии тучных клеток (ТК) в регуляции работы сердца при развитии некоторых сердечно-сосудистых патологий. В норме содержание ТК в сердце невелико по сравнению с их количеством в барьерных тканях. Они отвечают за гомеостаз сердечной ткани и обеспечение взаимодействия органа с нервной и эндокринной системами на протяжении всей жизни организма.

Патологические процессы в сердце сопровождаются развитием реакции воспаления, в формировании всех этапов которой значительная роль принадлежит ТК. На фоне развития инфаркта миокарда, фибротического поражения сердца и атеросклероза сосудов число ТК существенно возрастает. Их вклад в патогенез заболевания неоднозначен, поскольку с одной стороны направлен на адаптацию ткани к повреждению, а с другой – лавинообразный синтез и высвобождение медиаторов из активированных ТК усугубляет течение процесса. В результате ТК меняют свой секреторный профиль, вмешиваются в реализацию функций сердца на фоне воспаления, но вместе с тем и модулируют афферентный поток информации от сердца и эфферентные влияния нервной системы. Слаженная работа системы теряет свою устойчивость, что может привести к тяжелым последствиям для жизнедеятельности всего организма.

Анализ современного состояния проблемы свидетельствует, что от функционального состояния ТК, их сложного взаимодействия с нервной системой зависит деятельность сердца как в норме, так и, особенно, на фоне развития патологических процессов.

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М. П. Морозова

Российский национальный исследовательский медицинский университет им. Н.И. Пирогова

Автор, ответственный за переписку.
Email: mormasha@gmail.com
Россия, Москва

А. Д. Куренкова

Институт регенеративной медицины, Первый МГМУ им. И.М. Сеченова Минздрава России (Сеченовский университет)

Email: mormasha@gmail.com
Россия, Москва

Б. А. Умарова

Московский государственный университет им. М.В. Ломоносова

Email: mormasha@gmail.com
Россия, Москва

Список литературы

  1. Varricchi G, Rossi FW, Galdiero MR, Granata F, Criscuolo G, Spadaro G, de Paulis A, Marone G (2019) Physiological Roles of Mast Cells: Collegium Internationale Allergologicum Update 2019. Int Arch Allergy Immunol 179(4): 247–261. https://doi.org/10.1159/000500088
  2. Elieh Ali Komi D, Wohrl S, Bielory L (2020) Mast Cell Biology at Molecular Level: a Comprehensive Review. Clin Rev Allergy Immunol 58(3): 342–365. https://doi.org/10.1007/s12016-019-08769-2
  3. Zhang Z, Ernst PB, Kiyono H, Kurashima Y (2022) Utilizing mast cells in a positive manner to overcome inflammatory and allergic diseases. Front Immunol 13: 937120. https://doi.org/10.3389/fimmu.2022.937120
  4. Nilsson G, Dahlin JS (2019) New insights into the origin of mast cells. Allergy 74(4): 844–845. https://doi.org/10.1111/all.13668
  5. Dahlin JS, Maurer M, Metcalfe DD, Pejler G, Sagi-Eisenberg R, Nilsson G (2022) The ingenious mast cell: Contemporary insights into mast cell behavior and function. Allergy 77(1): 83–99. https://doi.org/10.1111/all.14881
  6. Григорьев ИП, Коржевский ДЭ (2021) Современные технологии визуализации тучных клеток для биологии и медицины (обзор). Совр технол в мед 13(4): 93–109. [Grigorev IP, Korzhevskii DE (2021) Modern imaging technologies of mast cell for biology and medicine (review). Modern Technol Med 13(4): 93–109. (In Russ)]. https://doi.org/10.17691/stm2021.13.4.10
  7. Jin J, Jiang Y, Chakrabarti S, Su Z (2022) Cardiac Mast Cells: A Two-Head Regulator in Cardiac Homeostasis and Pathogenesis Following Injury. Front Immunol 13: 963444. https://doi.org/10.3389/fimmu.2022.963444
  8. Da Silva EZ, Jamur MC, Oliver C (2014) Mast cell function: a new vision of an old cell. J Histochem Cytochem 62(10): 698–738. https//doi.org/ 10.1369/0022155414545334
  9. Vukman KV, Forsonits A, Oszvald A, Tуth EA, Buzas EI (2017) Mast cell secretome: Soluble and vesicular components. Semin Cell Dev Biol 67: 65–73. https://doi.org/10.1016/j.semcdb.2017.02.002
  10. Levick SP, Brower GL, Janicki J (2019) Substance P-mediated cardiac mast cell activation: An in vitro study. Neuropeptides 74: 52–59. https://doi.org/10.1016/j.npep.2019.01.002
  11. Levick SP, Widiapradja A (2018) Mast Cells: Key Contributors to Cardiac Fibrosis. Int J Mol Sci 19(1): 231. https://doi.org/10.3390/ijms19010231
  12. He A, Fang W, Zhao K, Wang Y, Li J, Yang C, Benadjaoud F, Shi GP (2019) Mast cell-deficiency protects mice from streptozotocin-induced diabetic cardiomyopathy. Transl Res 208: 1–14. https://doi.org/10.1016/j.trsl.2019.01.005
  13. He G, Hu J, Li T, Ma X, Meng J, Jia M, Lu J, Ohtsu H, Chen Z, Luo X (2012) Arrhythmogenic effect of sympathetic histamine in mouse hearts subjected to acute ischemia. Mol Med 18(1): 1–9. https://doi.org/10.2119/molmed.2011.00225
  14. Ahmad S, Wright KN, Sun X, Groban L, Ferrario CM (2019) Mast cell peptidases (carboxypeptidase A and chymase)-mediated hydrolysis of human angiotensin-(1-12) substrate. Biochem Biophys Res Commun 518(4): 651–656. https://doi.org/10.1016/j.bbrc.2019.08.098
  15. Zhang X, Shao C, Cheng S, Zhu Y, Liang B, Gu N (2021) Effect of Guanxin V in animal model of acute myocardial infarction. BMC Complement Med Ther 21(1): 72. https://doi.org/10.1186/s12906-021-03211-7
  16. Kritas SK, Caraffa A, Antinolfi P, Saggini A, Pantalone A, Rosati M, Tei M, Speziali A, Saggini R, Pandolfi F, Cerulli G, Conti P (2014) Nerve growth factor interactions with mast cells. Int J Immunopathol Pharmacol 27(1): 15–19. https://doi.org/10.1177/039463201402700103
  17. Forsythe P (2019) Mast Cells in Neuroimmune Interactions. Trends Neurosci 42(1): 43–55. https://doi.org/10.1016/j.tins.2018.09.006
  18. Carthy E, Ellender T (2021) Histamine, Neuroinflammation and Neurodevelopment: A Review. Front Neurosci 15: 680214. https://doi.org/10.3389/fnins.2021.680214
  19. Li F, Yu R, Sun X, Chen X, Xu P, Huang Y, Huang S, Xue Y, Fu T, Liu J, Li Z (2022) Autonomic nervous system receptor-mediated regulation of mast cell degranulation modulates the inflammation after corneal epithelial abrasion. Exp Eye Res 219: 109065. https://doi.org/10.1016/j.exer.2022.109065
  20. Чумасов ЕИ, Петрова ЕС, Коржевский ДЭ (2021) Морфологические признаки нейрогенного воспаления в сердце крыс при старении. Успехи геронтол 34(6): 831–841. [Chumasov EI, Petrova ES, Korzhevskii DE (2021) Morphological signs of neurogenic inflammation in the heart of rats during aging. Uspehi gerontol 34(6): 831–841. (In Russ)].
  21. Kulka M, Sheen CH, Tancowny BP, Grammer LC, Schleimer RP (2008) Neuropeptides activate human mast cell degranulation and chemokine production. Immunology 123(3): 398–410. https://doi.org/10.1111/j.1365-2567.2007.02705.x
  22. Siiskonen H, Harvima I (2019) Mast Cells and Sensory Nerves Contribute to Neurogenic Inflammation and Pruritus in Chronic Skin Inflammation. Front Cell Neurosci 13: 422. https://doi.org/10.3389/fncel.2019.00422
  23. Suzuki A, Suzuki R, Furuno T, Teshima R, Nakanishi M (2004) N-cadherin plays a role in the synapse-like structures between mast cells and neurites. Biol Pharm Bull 27(12): 1891–1894. https://doi.org/10.1248/bpb.27.1891
  24. Wilhelm M, Silver R, Silverman AJ (2005) Central nervous system neurons acquire mast cell products via transgranulation. Eur J Neurosci 22(9): 2238–2248. https://doi.org/10.1111/j.1460-9568.2005.04429.x
  25. Greenberg G, Burnstock G (1983) A novel cell-to-cell interaction between mast cells and other cell types. Exp Cell Res147(1): 1–13. https://doi.org/10.1016/0014-4827(83)90265-3
  26. Ardell JL, Armour JA (2016) Neurocardiology: Structure-Based Function. Compr Physiol 6(4): 1635–1653. https://doi.org/10.1002/cphy.c150046
  27. Li F, Wang F (2021) TRPV1 in Pain and Itch. Adv Exp Med Biol 1349: 249–273. https://doi.org/10.1007/978-981-16-4254-8_12
  28. Morrey C, Brazin J, Seyedi N, Corti F, Silver RB, Levi R (2010). Interaction between sensory C-fibers and cardiac mast cells in ischemia/reperfusion: activation of a local renin-angiotensin system culminating in severe arrhythmic dysfunction. J Pharmacol Exp Ther 335: 76–84. https://doi.org/10.1124/jpet.110.172262
  29. Facoetti A, Fallarini S, Miserere S, Bertolotti A, Ferrero I, Tozzi R, Gatti C, Palladini G, Perlini S, Nano R (2006) Histochemical study of cardiac mast cells degranulation and collagen deposition: interaction with the cathecolaminergic system in the rat. Eur J Histochem 50(2): 133–140.
  30. Reid AC, Brazin JA, Morrey C, Silver RB, Levi R (2011) Targeting cardiac mast cells: pharmacological modulation of the local renin-angiotensin system. Curr Pharm Des 17(34): 3744–3752. https://doi.org/10.2174/138161211798357908
  31. Levick SP (2022) Histamine receptors in heart failure. Heart Fail Rev 27(4): 1355–1372. https://doi.org/10.1007/s10741-021-10166-x
  32. Li M, Luo X, Chen L, Zhang J, Hu J, Lu B (2003) Co-localization of histamine and dopamine-beta-hydroxylase in sympathetic ganglion and release of histamine from cardiac sympathetic terminals of guinea-pig. Auton Autacoid Pharmacol 23(5-6): 327–333. https://doi.org/10.1111/j.1474-8673.2004.00305.x
  33. Winbo A, Ashton JL, Montgomery JM (2020) Neuroscience in the heart: Recent advances in neurocardiac communication and its role in cardiac arrhythmias. Int J Biochem Cell Biol 122: 105737. https://doi.org/10.1016/j.biocel.2020.105737
  34. Hanna P, Rajendran PS, Ajijola OA, Vaseghi M, Andrew Armour J, Ardell JL, Shivkumar K (2017) Cardiac neuroanatomy – Imaging nerves to define functional control. Auton Neurosci 207: 48–58. https://doi.org/10.1016/j.autneu.2017.07.008
  35. Shi L, Xu H, Wu Y, Li X, Zou L, Gao J, Chen H (2017) Alpha7-nicotinic acetylcholine receptors involve the imidacloprid-induced inhibition of IgE-mediated rat and human mast cell activation. RSC Adv 7: 51896–51906. https://doi.org/10.1039/C7RA07862E
  36. Duraes Campos I, Pinto V, Sousa N, Pereira VH (2018) A brain within the heart: A review on the intracardiac nervous system. J Mol Cell Cardiol 119: 1–9. https://doi.org/10.1016/j.yjmcc.2018.04.005
  37. Powers MJ, Peterson BA, Hardwick JC (2001) Regulation of parasympathetic neurons by mast cells and histamine in the guinea pig heart. Auton Neurosci 87(1): 37–45. https://doi.org/10.1016/S1566-0702(00)00260-5
  38. Alfonso A, Le Sueur ANV, Geraldes SS, Guimaraes-Okamoto PTC, Tsunemi MH, Santana DF, Ribeiro VRF, Melchert A, Chiacchio SB, Lourenco MLG (2020) Heart Rate Variability and Electrocardiographic Parameters Predictive of Arrhythmias in Dogs with Stage IV Chronic Kidney Disease Undergoing Intermittent Haemodialysis. Animals (Basel) 10(10): 1829. https://doi.org/10.3390/ani10101829
  39. Pongkan W, Jitnapakarn W, Phetnoi W, Punyapornwithaya V, Boonyapakorn C (2020) Obesity-Induced Heart Rate Variability Impairment and Decreased Systolic Function in Obese Male Dogs. Animals (Basel) 10(8): 1383. https://doi.org/10.3390/ani10081383
  40. Chang YT, Huang WC, Cheng CC, Ke MW, Tsai JS, Hung YM, Huang NC, Huang MS, Wann SR (2020) Effects of epinephrine on heart rate variability and cytokines in a rat sepsis model. Bosn J Basic Med Sci 20(1): 88–98. https://doi.org/10.17305/bjbms.2018.3565
  41. Biering-Sorensen F, Biering-Sorensen T, Liu N, Malmqvist L, Wecht JM, Krassioukov A (2018) Alterations in cardiac autonomic control in spinal cord injury. Auton Neurosci 209: 4–18. https://doi.org/10.1016/j.autneu.2017.02.004
  42. Flood S, Tordoff C (2020) A new heart for organ donation after circulatory death. BJA Educ 20(4): 126–132. https://doi.org/10.1016/j.bjae.2019.12.004
  43. Morozova MP, Kurenkova AD, Volkova JuL, Berdalin AB, Banzeluk EN, Umarova BA, Lukoshkova EV, Gavrilova SA (2023) The Initial Autonomic Tone Determines the Progress of Irreversible Myocardial Ischemia in Rats. Biol Bull 50(3): 437–448. https://doi.org/10.1134/S106235902270011X
  44. Simões FC, Riley PR (2022) Immune cells in cardiac repair and regeneration. Development 149(8): dev199906. https://doi.org/10.3389/fimmu.2021.664457
  45. Janicki JS, Brower GL, Levick SP (2015) The emerging prominence of the cardiac mast cell as a potent mediator of adverse myocardial remodeling. Methods Mol Biol 1220: 121–139. https://doi.org/10.1007/978-1-4939-1568-2_8
  46. Elia A, Fossati S (2023) Autonomic nervous system and cardiac neuro-signaling pathway modulation in cardiovascular disorders and Alzheimer’s disease. Front Physiol 14: 1060666. https://doi.org/10.3389/fphys.2023.1060666
  47. Alevizos M, Karagkouni A, Panagiotidou S, Vasiadi M, Theoharides TC (2014) Stress triggers coronary mast cells leading to cardiac events. Ann Allergy Asthma Immunol 112(4): 309–316. https://doi.org/10.1016/j.anai.2013.09.017
  48. Xiong W, Zhou R, Qu Y, Yang Y, Wang Z, Song N, Liang R, Qian J (2021) Dexmedetomidine preconditioning mitigates myocardial ischemia/reperfusion injury via inhibition of mast cell degranulation. Biomed Pharmacother 141: 111853. https://doi.org/10.1016/j.biopha.2021.111853
  49. Galagudza MM, Sonin DL, Pochkaeva EI (2018) The no-reflow phenomenon: mechanisms and therapeutic targets. Region Вlood Сirculat and Microcirculat 17(1): 5–12. https://doi.org/10.24884/1682-6655-2018-17-1-5-12
  50. He GH, Xu GL, Cai WK, Zhang J (2016) Is Histamine H2 Receptor a Real Promising Target for Prevention or Treatment of Heart Failure? J Am Coll Cardiol 68(18): 2029. https://doi.org/10.1016/j.jacc.2016.06.078
  51. Huang YH, Cai WK, Yin SJ, Wang P, Li ZR, Yang Q, Zhou T, Meng R, Yang M, Guo Y, He GH (2022) Histamine H2 receptor antagonist exposure was related to decreased all-cause mortality in critical ill patients with heart failure: a cohort study. Eur J Prev Cardiol 29(14): 1854–1865. https://doi.org/10.1093/eurjpc/zwac122
  52. Meng R, Chen LR, Zhang ML, Cai WK, Yin SJ, Fan YX, Zhou T, Huang YH, He GH (2023) Effectiveness and Safety of Histamine H2 Receptor Antagonists: An Umbrella Review of Meta-Analyses. J Clin Pharmacol 63(1): 7–20. https://doi.org/10.1002/jcph.2147
  53. Levick SP, Meléndez GC, Plante E, McLarty JL, Brower GL, Janicki JS (2011) Cardiac mast cells: the centrepiece in adverse myocardial remodelling. Cardiovasc Res 89(1): 12–19. https://doi.org/10.1093/cvr/cvq272
  54. Ngkelo A, Richart A, Kirk JA, Bonnin P, Vilar J, Lemitre M, Marck P, Branchereau M, Le Gall S, Renault N, Guerin C, Ranek MJ, Kervadec A, Danelli L, Gautier G, Blank U, Launay P, Camerer E, Bruneval P, Menasche P, Heymes C, Luche E, Casteilla L, Cousin B, Rodewald HR, Kass DA, Silvestre JS (2016) Mast cells regulate myofilament calcium sensitization and heart function after myocardial infarction. J Exp Med 213(7): 1353–1374. https://doi.org/10.1084/jem.20160081
  55. Wei CC, Chen Y, Powell LC, Zheng J, Shi K, Bradley WE, Powell PC, Ahmad S, Ferrario CM, Dell’Italia LJ (2012) Cardiac kallikrein-kinin system is upregulated in chronic volume overload and mediates an inflammatory induced collagen loss. PLoS One 7(6): e40110. https://doi.org/10.1371/journal.pone.0040110
  56. Sharma JN (2005) The kallikrein-kinin system: from mediator of inflammation to modulator of cardioprotection. Inflammopharmacology 12(5-6): 591–596. https://doi.org/10.1163/156856005774382760
  57. Li Y, Sun X, Juan Z, Guan X, Wang M, Meng Y, Ma R (2022) Propofol pretreatment alleviates mast cell degranulation by inhibiting SOC to protect the myocardium from ischemia-reperfusion injury. Biomed Pharmacother 150: 113014. https://doi.org/10.1016/j.biopha.2022.113014
  58. Goldberger JJ, Arora R, Buckley U, Shivkumar K (2019) Autonomic Nervous System Dysfunction: JACC Focus Seminar. J Am Coll Cardiol 73(10): 1189–1206. https://doi.org/10.1016/j.jacc.2018.12.064
  59. Stoyek MR, Hortells L, Quinn TA (2021) From Mice to Mainframes: Experimental Models for Investigation of the Intracardiac Nervous System. J Cardiovasc Dev Dis 8(11): 149. https://doi.org/10.3390/jcdd8110149
  60. Frangogiannis NG (2019) Cardiac fibrosis: Cell biological mechanisms, molecular pathways and therapeutic opportunities. Mol Aspects Med 65: 70–99. https://doi.org/10.1016/j.mam.2018.07.001
  61. Kologrivova I, Shtatolkina M, Suslova T, Ryabov V (2021) Cells of the Immune System in Cardiac Remodeling: Main Players in Resolution of Inflammation and Repair After Myocardial Infarction. Front Immunol 12: 664457. https://doi.org/10.3389/fimmu.2021.664457
  62. Palaniyandi Selvaraj S, Watanabe K, Ma M, Tachikawa H, Kodama M, Aizawa Y (2005) Involvement of mast cells in the development of fibrosis in rats with postmyocarditis dilated cardiomyopathy. Biol Pharm Bull 28(11): 2128–2132. https://doi.org/10.1248/bpb.28.2128
  63. Bradding P, Pejler G (2018) The controversial role of mast cells in fibrosis. Immunol Rev 282(1): 198–231. https://doi.org/10.1111/imr.12626
  64. Zeng Z, Shen L, Li X, Luo T, Wei X, Zhang J, Cao S, Huang X, Fukushima Y, Bin J, Kitakaze M, Xu D, Liao Y (2014) Disruption of histamine H2 receptor slows heart failure progression through reducing myocardial apoptosis and fibrosis. Clin Sci 127: 435–448. https://doi.org/10.1042/CS20130716
  65. Hooshdaran B, Kolpakov MA, Guo X, Miller SA, Wang T, Tilley DG, Rafiq K, Sabri A (2017) Dual inhibition of cathepsin G and chymase reduces myocyte death and improves cardiac remodeling after myocardial ischemia reperfusion injury. Basic Res Cardiol 112(6): 62. https://doi.org/10.1007/s00395-017-0652-z
  66. Hermans M, Lennep JRV, van Daele P, Bot I (2019) Mast Cells in Cardiovascular Disease: From Bench to Bedside. Int J Mol Sci 20(14): 3395. https://doi.org/10.3390/ijms20143395
  67. Moreno M, Puig J, Serrano M, Moreno-Navarrete JM, Ortega F, Ricart W, Fernandez-Real JM (2014) Circulating tryptase as a marker for subclinical atherosclerosis in obese subjects. PLoS One 9(5): e97014. https://doi.org/10.1371/journal.pone.0097014
  68. Kouhpeikar H, Delbari Z, Sathyapalan T, Simental-Mendía LE, Jamialahmadi T, Sahebkar A (2020) The Effect of Statins through Mast Cells in the Pathophysiology of Atherosclerosis: a Review. Curr Atheroscler Rep 22(5): 19. https://doi.org/10.1007/s11883-020-00837-9
  69. Palmiere C, Comment L, Vilarino R, Mangin P, Reggiani Bonetti L (2014) Measurement of β-tryptase in postmortem serum in cardiac deaths. J Forensic Leg Med 23: 12–18. https://doi.org/10.1016/j.jflm.2014.01.009
  70. Kareinen I, Baumann M, Nguyen SD, Maaninka K, Anisimov A, Tozuka M, Jauhiainen M, Lee-Rueckert M, Kovanen PT (2018) Chymase released from hypoxia-activated cardiac mast cells cleaves human apoA-I at Tyr192 and compromises its cardioprotective activity. J Lipid Res 59(6): 945–957. https://doi.org/10.1194/jlr.M077503
  71. Cao J, Papadopoulou N, Kempuraj D, Boucher WS, Sugimoto K, Cetrulo CL, Theoharides TC (2005) Human mast cells express corticotropin-releasing hormone (CRH) receptors and CRH leads to selective secretion of vascular endothelial growth factor. J Immunol 174(12): 7665– 7675. https://doi.org/10.4049/jimmunol.174.12.7665
  72. Bot I, de Jager SC, Bot M, van Heiningen SH, de Groot P, Veldhuizen RW, van Berkel TJ, von der Thüsen JH, Biessen EA (2018) The neuropeptide substance P mediates adventitial mast cell activation and induces intraplaque hemorrhage in advanced atherosclerosis. Circ Res 106(1): 89–92. https://doi.org/10.1161/CIRCRESAHA.109.204875
  73. Xu GZ, Wang G (2022) Acute myocardial infarction due to Kounis syndrome: A case report. World J Clin Cases 10(31): 11555–11560. https://doi.org/10.12998/wjcc.v10.i31.11555
  74. Kounis NG, Cervellin G, Koniari I, Bonfanti L, Dousdampanis P, Charokopos N, Assimakopoulos SF, Kakkos SK, Ntouvas IG, Soufras GD, Tsolakis I (2018) Anaphylactic cardiovascular collapse and Kounis syndrome: systemic vasodilation or coronary vasoconstriction? Ann Transl Med 6(17): 332. https://doi.org/10.21037/atm.2018.09.05
  75. Chen J, Hong T, Ding S, Deng L, Abudupataer M, Zhang W, Tong M, Jia J, Gong H, Zou Y, Wang TC, Ge J, Yang X (2017) Aggravated myocardial infarction-induced cardiac remodeling and heart failure in histamine-deficient mice. Sci Rep 7: 44007. https://doi.org/10.1038/srep44007

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