RAS PhysiologyЖурнал эволюционной биохимии и физиологии Journal of Evolutionary Biochemistry and Physiology

  • ISSN (Print) 0044-4529
  • ISSN (Online) 3034-5529

Mechanical alternancies in cardiomycytes of the myocardial sleeves of the superior vena cava and pulmonary veins as a potential source of ectopic activity of the atria

PII
S0044452925020044-1
DOI
10.31857/S0044452925020044
Publication type
Article
Status
Published
Authors
Volume/ Edition
Volume 61 / Issue number 2
Pages
108-118
Abstract
The myocardium of the right and left atria (RA and LA) continues into the superior vena cava (SVC) and pulmonary veins (PV) and forms myocardial sleeves, which are sources of ectopic activity causing atrial fibrillation. We compared the sarcomere dynamics of single cardiomyocytes from the myocardial sleeves of the SVC and PV and guinea pig atria. SVC cardiomyocytes were characterized by a longer time to peak sarcomere shortening and time to 50% relaxation than cardiomyocytes of other groups. In cardiomyocytes of the SVC, PV and right atrium, there was no correlation between the amplitude of sarcomere shortening and the length of the cardiomyocytes. The sarcomere shortening alternans was found in cardiomyocytes of the SVC and PV. The mechanical alternans and the lack of correlation between the amplitude of the sarcomere shortening and the cell size in the myocardial sleeves of the SVC and PV may point to a mechanical substrate that provokes arrhythmia.
Keywords
миокардиальные рукава кардиомиоциты верхней полой вены кардиомиоциты легочной вены укорочение-расслабление саркомеров механические альтернансы фибрилляция предсердий
Date of publication
18.09.2025
Year of publication
2025
Number of purchasers
0
Views
3

References

  1. 1. Mommersteeg MTM, Brown NA, Prall OWJ, De Gier-de Vries C, Harvey RP, Moorman AFM, Christoffels VM (2007) Pitx2c and Nkx2-5 are required for the formation and identity of the pulmonary myocardium. Circ Res 101: 902–909. https://doi.org/10.1161/CIRCRESAHA.107.161182
  2. 2. Mamchur S, Mamchur I, Khomenko E, Kokov A, Bokhan N, Sherbinina D (2014) Mechanical function of left atrium and pulmonary vein sleeves before and after their antrum isolation. Medicina 50: 353–359. https://doi.org/10.1016/j.medici.2014.11.008
  3. 3. Yee M, Cohen ED, Domm W, Porter GA, McDavid AN, O’Reilly MA (2018) Neonatal hyperoxia depletes pulmonary vein cardiomyocytes in adult mice via mitochondrial oxidation. Am J Physiol Lung Cell Mol Physiol 314: L846–L859. https://doi.org/10.1152/ajplung.00409.2017
  4. 4. Santangeli P, Zado ES, Hutchinson MD, Riley MP, Lin D, Frankel DS, Supple GE, Garcia FC, Dixit S, Callans DJ, Marchlinski FE (2016) Prevalence and distribution of focal triggers in persistent and long-standing persistent atrial fibrillation. Heart Rhythm 13: 374–382. https://doi.org/10.1016/j.hrthm.2015.10.023
  5. 5. Meijborg VMF, Belterman CNW, De Bakker JMT, Coronel R, Conrath CE (2017) Mechano-electric coupling, heterogeneity in repolarization and the electrocardiographic T-wave. Prog Biophys Mol Biol 130: 356–364. https://doi.org/10.1016/j.pbiomolbio.2017.05.003
  6. 6. Emig R, MacDonald EA, Quinn TA (2024) Cardiac mechano-electric crosstalk: multi-scale observations, computational integration, and clinical implications. J Physiol 602: 4335–4340. https://doi.org/10.1113/JP286706
  7. 7. Butova XA, Myachina TA, Simonova RA, Kochurova AM, Kopylova GV, Khokhlova AD, Shchepkin DV (2024) Contractile characteristics of single cardiomyocytes in the myocardial sleeves of the pulmonary veins of guinea pigs. J Evol Biochem Physiol 60: 1741–1750. https://doi.org/10.1134/S0022093024050077
  8. 8. Russell B, Curtis MW, Koshman YE, Samarel AM (2010) Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width. J Mol Cell Cardiol 48: 817–823. https://doi.org/10.1016/j.yjmcc.2010.02.016
  9. 9. Ooie T, Tsuchiya T, Ashikaga K, Takahashi N (2002) Electrical connection between the right atrium and the superior vena cava, and the extent of myocardial sleeve in a patient with atrial fibrillation originating from the superior vena cava. J Cardiovasc Electrophysiol 13: 482–485. https://doi.org/10.1046/j.1540-8167.2002.00482.x
  10. 10. Watanabe K, Nitta J, Inaba O, Sato A, Inamura Y, Kato N, Suzuki M, Goya M, Hirao K, Sasano T (2021) Predictors of non-pulmonary vein foci in paroxysmal atrial fibrillation. J Interv Card Electrophysiol 61: 71–78. https://doi.org/10.1007/s10840-020-00779-x
  11. 11. Kim D, Hwang T, Kim M, Yu HT, Kim TH, Uhm JS, Joung B, Lee MH, Pak HN (2021) Extra-pulmonary vein triggers at de novo and the repeat atrial fibrillation catheter ablation. Front Cardiovasc Med 8: 759967. https://doi.org/10.3389/fcvm.2021.759967
  12. 12. Iwamiya S, Ihara K, Nitta G, Sasano T (2024) Atrial fibrillation and underlying structural and electrophysiological heterogeneity. Int J Mol Sci 25: 10193. https://doi.org/10.3390/ijms251810193
  13. 13. Nyuta E, Takemoto M, Sakai T, Mito T, Masumoto A, Todoroki W, Yagyu K, Ueno J, Antoku Y, Koga T, Ueno T, Tsuchihashi T (2021) Importance of the length of the myocardial sleeve in the superior vena cava in patients with atrial fibrillation. J Arrhythm 37: 43–51. https://doi.org/10.1002/joa3.12494
  14. 14. Yeh HI, Lai YJ, Lee SH, Lee YN, Ko YS, Chen SA, Severs NJ, Tsai CH (2001) Heterogeneity of myocardial sleeve morphology and gap junctions in canine superior vena cava. Circulation 104: 3152–3157. https://doi.org/10.1161/hc5001.100836
  15. 15. Kugler S, Nagy N, Rácz G, Tőkés AM, Dorogi B, Nemeskéri Á (2018) Presence of cardiomyocytes exhibiting Purkinje-type morphology and prominent connexin45 immunoreactivity in the myocardial sleeves of cardiac veins. Heart Rhythm 15: 258–264. https://doi.org/10.1016/j.hrthm.2017.09.044
  16. 16. Chen YJ, Chen YC, Yeh HI, Lin CI, Chen SA (2002) Electrophysiology and arrhythmogenic activity of single cardiomyocytes from canine superior vena cava. Circulation 105: 2679–2685. https://doi.org/10.1161/01.CIR.0000016822.96362.26
  17. 17. Wang P, Yang XC, Liu XL, Bao RF, Ding HY, Li O, Liu TF (2021) Study of the characteristics of the pulmonary vein and superior vena cava of rabbits. J Biomater Tissue Eng 11: 112–122. https://doi.org/10.1166/jbt.2021.2585
  18. 18. Margossian SS, Lowey S (1982) Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol 85 Pt B: 55–71. https://doi.org/10.1016/0076-6879 (82)85009-x
  19. 19. Spiess M, Steinmetz MO, Mandinova A, Wolpensinger B, Aebi U, Atar D (1999) Isolation, electron microscopic imaging, and 3-D visualization of native cardiac thin myofilaments. J Struct Biol 126: 98–104. https://doi.org/10.1006/jsbi.1999.4111
  20. 20. Liu R, Feng HZ, Jin JP (2014) Physiological contractility of cardiomyocytes in the wall of mouse and rat azygos vein. Am J Physiol Cell Physiol 306: C697–C704. https://doi.org/10.1152/ajpcell.00004.2014
  21. 21. Kumar M, Govindan S, Zhang M, Khairallah RJ, Martin JL, Sadayappan S, De Tombe PP (2015) Cardiac myosin-binding protein C and troponin-I phosphorylation independently modulate myofilament length-dependent activation. J Biol Chem 290: 29241–29249. https://doi.org/10.1074/jbc.M115.686790
  22. 22. Sevrieva IR, Ponnam S, Yan Z, Irving M, Kampourakis T, Sun YB (2023) Phosphorylation-dependent interactions of myosin-binding protein C and troponin coordinate the myofilament response to protein kinase A. J Biol Chem 299: 102767. https://doi.org/10.1016/j.jbc.2022.102767
  23. 23. Lang D, Medvedev RY, Ratajczyk L, Zheng J, Yuan X, Lim E, Han OY, Valdivia HH, Glukhov AV (2022) Region-specific distribution of transversal-axial tubule system organization underlies heterogeneity of calcium dynamics in the right atrium. Am J Physiol Heart Circ Physiol 322: H269–H284. https://doi.org/10.1152/ajpheart.00381.2021
  24. 24. Cros C, Douard M, Chaigne S, Pasqualin C, Bru-Mercier G, Recalde A, Pascarel-Auclerc C, Hof T, Haïssaguerre M, Hocini M, Jaïs P, Bernus O, Brette F (2023) Regional differences in Ca2+ signaling and transverse-tubules across left atrium from adult sheep. Int J Mol Sci 24: 2347. https://doi.org/10.3390/ijms24032347
  25. 25. Wilson AJ, Schoenauer R, Ehler E, Agarkova I, Bennett PM (2014) Cardiomyocyte growth and sarcomerogenesis at the intercalated disc. Cell Mol Life Sci 71: 165–181. https://doi.org/10.1007/s00018-013-1374-5
  26. 26. Kanaporis G, Blatter LA (2015) The mechanisms of calcium cycling and action potential dynamics in cardiac alternans. Circ Res 116: 846–856. https://doi.org/10.1161/CIRCRESAHA.116.305404
  27. 27. Narayan SM, Franz MR, Clopton P, Pruvot EJ, Krummen DE (2011) Repolarization alternans reveals vulnerability to human atrial fibrillation. Circulation 123: 2922–2930. https://doi.org/10.1161/CIRCULATIONAHA.110.977827
  28. 28. Muthavarapu N, Mohan A, Manga S, Sharma P, Bhanushali AK, Yadav A, Damani DN, Jais P, Walton RD, Arunachalam SP, Kulkarni K (2023) Targeted atrial fibrillation therapy and risk stratification using atrial alternans. J Cardiovasc Dev Dis 10: 36. https://doi.org/10.3390/jcdd10020036
  29. 29. Butova X, Myachina T, Simonova R, Kochurova A, Mukhlynina E, Kopylova G, Shchepkin D, Khokhlova A (2023) The inter-chamber differences in the contractile function between left and right atrial cardiomyocytes in atrial fibrillation in rats. Front Cardiovasc Med 10: 1203093. https://doi.org/10.3389/fcvm.2023.1203093
  30. 30. Berenfeld O, Zaitsev AV, Mironov SF, Pertsov AM, Jalife J (2002) Frequency-dependent breakdown of wave propagation into fibrillatory conduction across the pectinate muscle network in the isolated sheep right atrium. Circ Res 90: 1173–1180. https://doi.org/10.1161/01.RES.0000022854.95998.5C
  31. 31. Prabhu S, Voskoboinik A, Mclellan A, Peck K, Nalliah C, Wong G, Azzopardi S, Lee G, Mariani J, Ling L, Taylor A, Kalman J, Kistler P (2017) A comparison of the electrophysiologic and electroanatomic characteristics between the right and left atrium in persistent atrial fibrillation: is the right atrium a window into the left? Heart Lung Circ 26: S176. https://doi.org/10.1016/j.hlc.2017.06.304
QR
Translate

Индексирование

Scopus

Scopus

Scopus

Crossref

Scopus

Higher Attestation Commission

At the Ministry of Education and Science of the Russian Federation

Scopus

Scientific Electronic Library