The Role of Mast Cell-Neuron Tandem in the Regulation of Cardiac Function in Cardiovascular Pathologies
- Авторлар: Morozova M.P.1, Kurenkova A.D.2, Umarova B.A.3
-
Мекемелер:
- Pirogov Russian National Research Medical University
- Institute of Regenerative Medicine, Sechenov First Moscow Medical University
- Lomonosov Moscow State University
- Шығарылым: Том 110, № 3 (2024)
- Беттер: 349-374
- Бөлім: REVIEW
- URL: https://cardiosomatics.ru/0869-8139/article/view/651660
- DOI: https://doi.org/10.31857/S0869813924030031
- EDN: https://elibrary.ru/CPYNFR
- ID: 651660
Дәйексөз келтіру
Аннотация
This review is consisted of new data about participation of mast cells (MCs) in the regulation of cardiac function in the development of some cardiovascular pathologies. In norm the number of MCs in the heart is very small compared to their number in barrier tissues. They are responsible for homeostasis of cardiac tissue and ensuring the interaction of the organ with the nervous and endocrine systems throughout the life of the organism.
Pathological processes in the heart are accompanied by the development of inflammation reaction. MCs fulfil a significant role in the all stages of inflammation. The number of MCs significantly increases against the background of myocardial infarction development, fibrotic heart disease and vascular atherosclerosis. Their contribution to the pathogenesis of the disease is ambiguous, because on the one hand it is aimed at tissue adaptation to damage, and on the other hand - avalanche-like synthesis and release of mediators from activated MCs aggravates the course of the process. As a result, MCs change their secretory profile, interfere in the realization of cardiac functions against the background of inflammation, but at the same time modulate afferent information flow from the heart and efferent influences of the nervous system. The coordinated work of the system loses its stability, which can lead to severe consequences for the vital activity of the whole organism.
The analysis of the current state of the problem indicates that the heart activity depends on the functional state of MCs, their complex interaction with the nervous system both in the norm and, especially, against the background of pathological processes development.
Негізгі сөздер
Толық мәтін

Авторлар туралы
M. Morozova
Pirogov Russian National Research Medical University
Хат алмасуға жауапты Автор.
Email: mormasha@gmail.com
Ресей, Moscow
A. Kurenkova
Institute of Regenerative Medicine, Sechenov First Moscow Medical University
Email: mormasha@gmail.com
Ресей, Moscow
B. Umarova
Lomonosov Moscow State University
Email: mormasha@gmail.com
Ресей, Moscow
Әдебиет тізімі
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Forsythe P (2019) Mast Cells in Neuroimmune Interactions. Trends Neurosci 42(1): 43–55. https://doi.org/10.1016/j.tins.2018.09.006
- Carthy E, Ellender T (2021) Histamine, Neuroinflammation and Neurodevelopment: A Review. Front Neurosci 15: 680214. https://doi.org/10.3389/fnins.2021.680214
- 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
- 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)].
- 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
- 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
- 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
- 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
- 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
- Ardell JL, Armour JA (2016) Neurocardiology: Structure-Based Function. Compr Physiol 6(4): 1635–1653. https://doi.org/10.1002/cphy.c150046
- 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
- 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
- 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.
- 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
- Levick SP (2022) Histamine receptors in heart failure. Heart Fail Rev 27(4): 1355–1372. https://doi.org/10.1007/s10741-021-10166-x
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Simões FC, Riley PR (2022) Immune cells in cardiac repair and regeneration. Development 149(8): dev199906. https://doi.org/10.3389/fimmu.2021.664457
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
Қосымша файлдар
