Pathogenetic aspects of dishormonal cardiomyopathy

Authors: Zaytseva E.V.1, Popov V.V.1, Khidirova L.D1, 2

Company: 1 Novosibirsk State Medical University, Novosibirsk, Russian Federation
2 Novosibirsk Clinical Cardiology Dispensary, Novosibirsk, Russian Federation

For correspondence:  Sign in or register.

Type:  Reviews


DOI: https://doi.org/10.24022/1997-3187-2024-18-1-20-27

For citation: Zaytseva E.V., Popov V.V., Khidirova L.D. Pathogenetic aspects of dishormonal cardiomyopathy. Creative Cardiology. 2024; 18 (1): 20–27 (in Russ.). DOI: 0.24022/1997-3187-2024-18-1-20-271

Received / Accepted:  22.01.2024 / 09.02.2024

Keywords: dishormonal cardiomyopathy menopause menopause estrogens androgens endothelial dysfunction endothelial nitric oxide synthase sphingolipid cardiovascular diseases



Subscribe 🔒

 

Abstract

The presence of high social significance of the increase in morbidity and mortality in women with sex hormone dysfunction served as the basis for the development of recommendations for the prevention and treatment of cardiovascular diseases in this category of patients. Based on current literature data, questions about the mechanisms of development and clinical course of cardiometabolic disorders that occur during the menopause are summarized. According to recent data, in the female population, the onset of menopause is accompanied by the development of a whole complex of hormonal, metabolic and structural-functional changes, including those in the cardiovascular system, which contribute to the formation and rapid progression of cardiovascular pathology. The problem of the relationship between structural changes in the myocardium and its functional characteristics is still a subject of debate, as well as the question of the influence on the structure and function of the myocardium of genetic factors, imbalance of the renin-angiotensin-aldosterone system (RAAS) and the immune system, depending on the type of menopause, the presence and severity of postmenopausal hypertension, its duration and some other factors. The deterioration in the quality of life in patients with menopausal disorders causes a number of not only medical, but also socio-economic problems. An important issue is the creation of a specialized multidisciplinary reception for the problems of menopause, which will ensure individual selection of complex treatment for the patient, taking into account the characteristics of the pathogenetic mechanisms of dishormonal cardiomyopathy.

References

  1. Baber R.J., Panay N., Fenton A. 2016 IMS Recommendations on women's midlife health and menopause hormone therapy. Climacteric. 2018; 19 (2): 109–150. DOI: 10.3109/13697137. 2015.1129166
  2. Palma F., Volpe A., Villa P., Cagnacci A. Vaginal atrophy of women in postmenopause. Results from a multicentric observational study: The AGATA study. Maturitas. 2016; 83: 40–44. DOI: 10.1016/j.maturitas.2016.09.001
  3. Yureneva Y.S.V., Ermakova E.E.I., Glazunova G.A.V. Genitourinary syndrome of menopause in peri- and postmenopausal patients: diagnosis and therapy (short clinical guideline). Akush. Ginekol. (Sofiia). 2018; 5: 138–144. DOI: 10.18565/aig.2016.5.138-144
  4. Wood L.N., Anger J.T. Urinary incontinence in women. Br. Med. J. 2014; 349: 453. DOI: 10.1136/bmj.g4531
  5. Hotamisligil G.S., Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 2008; 8 (12): 923–934. DOI: 10.1038/nri2449
  6. Higashikuni Y., Tanaka K., Kato M., Nureki O., Hirata Y., Nagai R. et al. Toll-like receptor-2 mediates adaptive cardiac hypertrophy in response to pressure overload through interleukin1beta upregulation via nuclear factor kappaB activation. J. Am. Heart Assoc. 2013; 2 (6): e000267. DOI: 10.1161/JAHA. 113.000267
  7. Xiao F.Y., Nheu L., Komesaroff P., Ling S. Testosterone protects cardiac myocytes from superoxide injury via NF-κB signalling pathways. Life Sci. 2015; 133: 45–52. DOI: 10.1016/j.lfs. 2015.05.009
  8. Zhang L., Wu S., Ruan Y., Hong L., Xing X., Lai W. Testosterone suppresses oxidative stress via androgen receptor-independent pathway in murine cardiomyocytes. Mol. Med. Rep. 2011; 4 (6): 1183–1188. DOI: 10.3892/mmr.2011.539
  9. Vicencio J.M., Ibarra C., Estrada M., Сhoing M., Soto D., Parra V. et al. Testosterone induces an intracellular calcium increase by a nongenomic mechanism in cultured rat cardiac myocytes. Endocrinology. 2006; 147 (3): 1386–1395. DOI: 10.1210/en.2005-1139
  10. Cruz-Topete D., Dominic P., Stokes K.Y. Uncovering sexspecific mechanisms of action of testosterone and redox balance. Redox Biol. 2020; 31: 101490. DOI: 10.1016/j.redox.2020.101490
  11. Stone T., Stachenfeld N.S. Pathophysiological effects of androgens on the female vascular system. Biol. Sex. Differ. 2020; 11: 45. DOI: 10.1186/s13293-020-00323-6
  12. Zhao D., Guallar E., Ouyang P., Subramanya V., Vaidya D., Ndumele C.E. et al. Endogenous sex hormones and incident cardiovascular disease in post-menopausal women. J. Am. Coll. Cardiol. 2018; 71 (22): 2555–2566. DOI: 10.1016/j.jacc.2018.01.083
  13. Zhao D., Guallar E., Ballantyne C.M., Post W.S., Ouyang P., Vaidya D. et al. Sex hormones and incident heart failure in men and postmenopausal women: the atherosclerosis risk in communities study. J. Clin. Endoc. Metab. 2020; 105 (10): e3798–e3807. DOI: 10.1210/clinem/dgaa500
  14. Jia X., Sun C., Tang O., Gorlov O., Nambi V., Virani S.S. et al. Plasma dehydroepiandrosterone sulfate and cardiovascular disease risk in older men and women. J. Clin. Endoc. Metab. 2020; 105 (12): e4304–e4327. DOI: 10.1210/clinem/dgaa518
  15. Schaffrath G., Kische H., Gross S., Wallaschofski H., Völzke H., Dörr M. et al. Association of sex hormones with incident 10-year cardiovascular disease and mortality in women. Maturitas. 2015; 82 (4): 424–430. DOI: 10.1016/j.maturitas.2015.08.009
  16. Holmegard H.N., Nordestgaard B.G,. Jensen G.B., TybjærgHansen A., Benn M. Sex hormones and ischemic stroke: a prospective cohort study and meta-analyses. J. Clin. Endoc. Metab. 2016; 101 (1): 69–78. DOI: 10.1210/jc.2015-2687
  17. Xu S., Dai W., Li J. Li Y. Synergistic effect of estradiol and testosterone protects against IL-6-inducedcardiomyocyte apoptosismediated by TGF-β1. Int. J. Clin. Exp. Pathol. 2018; 11 (1): 10–26.
  18. Pruett S.T., Bushnev A., Hagedorn K., Adiga M., Haynes C.A., Sullards M.C. et al. Biodiversity of sphingoid bases (“sphingosines”) and related amino alcohols. J. Lipid Res. 2008; 49 (8): 1621–1639. DOI: 10.1194/jlr.R800012-JLR200
  19. Sasset L., Zhang Y., Dunn T.M., Lorenzo A.D. Sphingolipid de novo biosynthesis: a rheostat of cardiovascular homeostasis. Trends Endocrinol. Metab. 2016; 27 (11): 807–819. DOI: 10.1016/j.tem.2016.07.005
  20. Harrison P.J., Dunn T.M., Campopiano D.J. Sphingolipid biosynthesis in man and microbes. Nat. Prod. Rep. 2018; 35 (9): 921–954. DOI: 10.1039/c8np00019k
  21. Shu H., Peng Y., Hang W., Li N., Zhou N., Wang D.W. Emerging roles of ceramide in cardiovascular diseases. Aging Dis. 2022; 13 (1): 232–245. DOI: 10.14336/AD.2021.0710
  22. De Mello V.D., Lankinen M., Schwab U., Kolhmainen M., Lehto S. et al. Link between plasma ceramides, inflammation and insulin resistance: association with serum IL-6 concentration in patients with coronary heart disease. Diabetologia. 2009; 52 (12): 2612–2615. DOI: 10.1007/s00125-009-1482-9
  23. Spijkers L.J., van den Akker R.F., Janssen B., Debets J.J., De Mey J.G.R., Stroes E.S.G. et al. Hypertension is associated with marked alterations in sphingolipid biology: a potential role for ceramide. PLoS ONE. 2011; 6 (7): e21817. DOI: 10.1371/journal.pone.0021817
  24. Pan W., Yu J., Shi R., Yan L., Yang T., Li Y. et al. Elevation of ceramide and activation of secretory acid sphingomyelinase in patients with acute coronary syndromes. Coron. Artery Dis. 2014; 25 (3): 230–235. DOI: 10.1097/MCA.0000000000000079
  25. Havulinna A.S., Sysi-Aho M., Hilvo M., Kauhanen D., Hurme R., Ekroos K. et al. Circulating ceramides predict cardiovascular outcomes in the Population-Based FINRISK 2002 Cohort. Arterioscler. Thromb. Vasc. Biol. 2016; 36 (12): 2424–2430. DOI: 10.1161/ATVBAHA.116.307497
  26. Egom E.E., Mohamed T.M., Mamas M.A., Shi Y., Liu W., Chirico D. et al. Activation of Pak1/Akt/eNOS signaling following sphingosine-1-phosphate release as part of a mechanism protecting cardiomyocytes against ischemic cell injury. Am. J. Physiol. Heart Circ. Physiol. 2011; 301 (4): H1487–H1495. DOI: 10.1152/ajpheart.01003.2010
  27. Guo S., Yu Y., Zhang N., Cui Y., Zhai L., Li H. et al. Higher level of plasma bioactive molecule sphingosine 1-phosphate in women is associated with estrogen. Biochim. Biophys. Acta. 2014; 1841 (6): 836–846. DOI: 10.1016/j.bbalip.2014.02.005
  28. Fichtlscherer S., Zeiher A.M., Dimmeler S. Circulating microRNAs: biomarkers or mediators of cardiovascular diseases. Arterioscler. Thromb. Vasc. Biol. 2011; 31 (11): 2383–2390. DOI: 10.1161/ATVBAHA.111.226696
  29. Perez-Cremades D., Mompeon A., Vidal-Gomez X., Hermenegildo C., Novella S. Role of miRNA in the regulatory mechanisms of estrogens in cardiovascular ageing. Oxid. Med. Cell. Longev. 2018; 2018: 6082387. DOI: 10.1155/2018/6082387
  30. Vidal-Gomez X., Perez-Cremades D., Mompeon A., Dantas A.P., Novella S., Hermenegildo C. MicroRNA as crucial regulators of gene expression in estradiol-treated human endothelial сells. Cell. Physiol. Biochem. 2018; 45 (5): 1878–1892. DOI: 10.1159/000487910
  31. Gupta A., Caffrey E., Callagy G., Gupta S. Oestrogen-dependent regulation of miRNA biogenesis: many ways to skin the cat. Biochem. Soc. Trans. 2012; 40 (4): 752–758. DOI: 10.1042/BST20110763
  32. Zhao J., Imbrie G.A., Baur W.E., Lyer L.K., Aronovitz M.J., Kershaw T.B. et al. Estrogen receptor-mediated regulation of microRNA inhibits proliferation of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2013; 33 (2): 257–265. DOI: 10.1161/ATVBAHA.112.300200 33.
  33. Mori T., Durand J., Chen Y., Thompson J.A., Bakir S., Oparil S. Effects of short-term estrogen treatment on the neointimal response to balloon injury of rat carotid artery. Am. J. Cardiol. 2000; 85 (10): 1276–1279. DOI: 10.1016/s0002-9149(00)00748-7
  34. Xing D., Nozell S., Chen Y.F., Hage F., Oparil S. Estrogen and mechanisms of vascular protection. Arterioscler. Thromb. Vasc. Biol. 2009; 29 (3): 289–295. DOI: 10.1161/ATVBAHA.108.182279
  35. Wang L., Tang Z.P., Zhao W., Cong B.H., Lu J.Q., Tang X.L. et al. MiR-22/Sp-1 links estrogens with the up-regulation of cystathionine gamma-lyase in myocardium, which contributes to estrogenic cardioprotection against oxidative stress. Endocrinology. 2015; 156 (6): 2124–2137. DOI: 10.1210/en.2014-1362
  36. Queiros A.M., Eschen C., Fliegner D., Kararigas G., Dworatzek E., Westphal C. et al. Sex- and estrogen-dependent regulation of a miRNA network in the healthy and hypertrophied heart. Int. J. Cardiol. 2013; 169 (5): 331–338. DOI: 10.1016/j.ijcard.2013.09.002
  37. Meng Y., Zong L. Estrogen stimulates the expression of SREBP2 in liver cell lines through the estrogen response element in the SREBP2 promoter. Cell. Mol. Biol. Lett. 2019; 24: 65. DOI: 10.1186/s11658-019-0194-5
  38. Mullen E., Brown R.M., Osborne T.F. Neil Sh.F. Soy isoflavones affect sterol regulatory element binding proteins (SREBPs) and SREBP-regulated genes in HepG2 cells. J. Nutr. 2004; 134 (11): 2942–2947. DOI: 10.1093/jn/134.11.2942
  39. Shin E.S., Lee H.H., Cho S.Y., Park H.W., Lee S.J., Lee T.R. Genisteindownregulates SREBP-1 regulated gene expression by inhibiting site-1protease expression in HepG2 cells. J. Nutr. 2007; 137: 1127–1131.
  40. Williams B., Mancia G., Spiering W., Rosei E.A., Azizi M., Burnier M. et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur. Heart J. 2018; 39: 3021–3104. DOI: 10.1093/eurheartj/ehy339
  41. Xue B., Johnson A.K., Hay M. Sex differences in angiotensin IIe and aldosterone-induced hypertension: the central protective effects of estrogen. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013; 305 (5): R459–R463. DOI: 10.1152/ajpregu. 00222.2013
  42. Moreau M.E., Garbacki N., Molinaro G., Brown N.J., Marceau A.A. The kallikrein-kinin system: current and future pharmacological targets. J. Pharmacol Sci. 2015; 99 (1): 6–38. DOI: 10.1254/jphs.srj05001x
  43. Xue Q., Xiao D., Zhang L. Estrogen regulates angiotensin II receptor expression patterns and protects the heart from ischemic injury in female rats. Biol. Reprod. 2015; 93 (1): 6. DOI: 10.1095/biolreprod.115.129619

About Authors

  • Ekaterina V. Zaytseva, Student; ORCID
  • Vladislav V. Popov, Student;ORCID
  • Lyudmila D. Khidirova, Dr. Med. Sci., Professor of the Department of Pharmacology, Clinical Pharmacology and Evidence-based Medicine; ORCID

Chief Editor

Leo A. Bockeria, MD, PhD, DSc, Professor, Academician of Russian Academy of Sciences, President of Bakoulev National Medical Research Center for Cardiovascular Surgery