Study of the influence of long-dependent changes in myosin bridge kinetics on calcium transient in the myocardium of the right atrium and right ventricle of rats

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Дәйексөз келтіру

Толық мәтін

Ашық рұқсат Ашық рұқсат
Рұқсат жабық Рұқсат берілді
Рұқсат жабық Тек жазылушылар үшін

Аннотация

Heterometric regulation of myocardial contractility is the most important property regulating the pumping function of the heart. Calcium ions play a key role in the activation and regulation of muscle contraction. In addition to changes in the degree of actin-myosin filament overlap, one consequence of myocardial stretch is a length-dependent change in the shape and duration of the intracellular calcium transient (CaT). As the degree of myocardial stretch increases, the duration of the CaT decreases in the upper half of the CaT decline and increases in the lower half. To determine the contribution of myosin bridge kinetics to CaT changes, length-dependent changes in CaT were assessed in three states of myosin bridge kinetics; (1) intact, (2) slowed under the influence of omecamtiv mecarbil 1 µM (OM), and (3) blocked under the influence of blebbistatin 10 µM (BB). It was found that length-dependent multidirectional changes in CaT decay (CaT crossover phenomenon) were pronounced in the right ventricular (RV) myocardium and weak in the right atrial (RA) myocardium of intact male nine-week-old Wistar rats. OM significantly slows the rate of tension development and decline in myocardium of RA and RV rats; enhances length-dependent changes in CaT duration; OM decreases the duration of CaT at 80% of its amplitude and increases the duration of CaT at 20% of its amplitude in both RA and RV. BB almost completely abolishes the ability of the myocardium to develop tension; length-dependent changes in CaT duration are monotonous, CaT crossover in RV myocardium disappears. The phenomenon of CaT crossover in the myocardium of the RV is a consequence of the attachment and detachment of myosin bridges to the thin filament. The absence of length-dependent changes in CaT in rat RA myocardium seems to be associated with a more developed calcium sequestering system in RA, in comparison with the calcium sequestering system in RV.

Авторлар туралы

R. Lisin

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: lisin.ruslan@gmail.com
Ресей, Yekaterinburg

A. Balakin

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences

Email: lisin.ruslan@gmail.com
Ресей, Yekaterinburg

A. Zudova

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences

Email: lisin.ruslan@gmail.com
Ресей, Yekaterinburg

Yu. Protsenko

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences

Email: lisin.ruslan@gmail.com
Ресей, Yekaterinburg

Әдебиет тізімі

  1. Kosta S, Dauby PC (2021) Frank-Starling mechanism, fluid responsiveness, and length-dependent activation: Unravelling the multiscale behaviors with an in silico analysis. PLoS Comput Biol 17: e1009469. https://doi.org/10.1371/journal.pcbi.1009469
  2. Reda SM, Gollapudi SK, Chandra M (2019) Developmental increase in β-MHC enhances sarcomere length-dependent activation in the myocardium. J Gen Physiol 151: 635–644. https://doi.org/10.1085/jgp.201812183
  3. Hofmann PA, Fuchs F (1987) Effect of length and cross-bridge attachment on Ca2+ binding to cardiac troponin C. Am J Physiol 253: C90–С96. https://doi.org/10.1152/ajpcell.1987.253.1.C90
  4. Fuchs F, Smith SH (2001) Calcium, cross-bridges, and the Frank-Starling relationship. News Physiol Sci 16: 5–10. https://doi.org/10.1152/physiologyonline.2001.16.1.5
  5. Moss RL, Fitzsimons DP (2002) Frank-Starling Relationship. Circ Res 90: 11–13. https://doi.org/10.1161/res.90.1.11
  6. Ait-Mou Y, Hsu K, Farman GP, Kumar M, Greaser ML, Irving TC, de Tombe PP (2016) Titin strain contributes to the Frank-Starling law of the heart by structural rearrangements of both thin- and thick-filament proteins. Proc Natl Acad Sci USA 113: 2306–2311. https://doi.org/10.1073/pnas.1516732113
  7. Wijnker PJM, Sequeira V, Foster DB, Li Y, Dos Remedios CG, Murphy AM, Stienen GJM, van der Velden J (2014) Length-dependent activation is modulated by cardiac troponin I bisphosphorylation at Ser23 and Ser24 but not by Thr143 phosphorylation. Am J Physiol Heart Circ Physiol 306: H1171–H1181. https://doi.org/10.1152/ajpheart.00580.2013
  8. 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
  9. Morimoto S, Ohtsuki I (1994) Ca2+ binding to cardiac troponin C in the myofilament lattice and its relation to the myofibrillar ATPase activity. Eur J Biochem 226: 597–602. https://doi.org/10.1111/j.1432-1033.1994.tb20085.x
  10. Lisin R, Balakin A, Mukhlynina E, Protsenko Y (2023) Differences in Mechanical, Electrical and Calcium Transient Performance of the Isolated Right Atrial and Ventricular Myocardium of Guinea Pigs at Different Preloads (Lengths). Int J Mol Sci 24: 15524. https://doi.org/10.3390/ijms242115524
  11. Lookin O, Balakin A, Protsenko Y (2023) Differences in Effects of Length-Dependent Regulation of Force and Ca2+ Transient in the Myocardial Trabeculae of the Rat Right Atrium and Ventricle. Int J Mol Sci 24: 8960. https://doi.org/10.3390/ijms24108960
  12. Lookin O (2020) The use of Ca-transient to evaluate Ca2+ utilization by myofilaments in living cardiac muscle. Clin Exp Pharmacol Physiol 47: 1824–1833. https://doi.org/10.1111/1440-1681.13376
  13. Chizzonite RA, Everett AW, Prior G, Zak R (1984) Comparison of myosin heavy chains in atria and ventricles from hyperthyroid, hypothyroid, and euthyroid rabbits. J Biol Chem 259: 15564–15571.
  14. Narolska NA, van Loon RB, Boontje NM, Zaremba R, Penas SE, Russell J, Spiegelenberg SR, Huybregts JM, Visser FC, de Jong JW, van der Velden J, Stienen GJM (2005) Myocardial contraction is 5-fold more economical in ventricular than in atrial human tissue. Cardiovasc Res 65: 221–229. https://doi.org/10.1016/j.cardiores.2004.09.029
  15. Gerzen OP, Lisin RV, Balakin AA, Mukhlynina EA, Kuznetsov DA, Nikitina LV, Protsenko YL (2023) Characteristics of the right atrial and right ventricular contractility in a model of monocrotaline-induced pulmonary arterial hypertension. J Muscle Res Cell Motil 44(4): 299–309. https://doi.org/10.1007/s10974-023-09651-7
  16. Smyrnias I, Mair W, Harzheim D, Walker SA, Roderick HL, Bootman MD (2010) Comparison of the T-tubule system in adult rat ventricular and atrial myocytes, and its role in excitation-contraction coupling and inotropic stimulation. Cell Calcium 47: 210–223. https://doi.org/10.1016/j.ceca.2009.10.001
  17. Bootman MD, Smyrnias I, Thul R, Coombes S, Roderick HL (2011) Atrial cardiomyocyte calcium signalling. Biochim Biophys Acta 1813: 922–934. https://doi.org/10.1016/j.bbamcr.2011.01.030
  18. Maxwell JT, Blatter LA (2017) A novel mechanism of tandem activation of ryanodine receptors by cytosolic and SR luminal Ca2+ during excitation-contraction coupling in atrial myocytes. J Physiol 595: 3835–3845. https://doi.org/10.1113/JP273611
  19. Walden AP, Dibb KM, Trafford AW (2009) Differences in intracellular calcium homeostasis between atrial and ventricular myocytes. J Mol Cell Cardiol 46: 463–473. https://doi.org/10.1016/j.yjmcc.2008.11.003
  20. Jiang Y, Patterson MF, Morgan DL, Julian FJ (1998) Basis for late rise in fura 2 R signal reporting [Ca2+]i during relaxation in intact rat ventricular trabeculae. Am J Physiol 274: C1273–C1282. https://doi.org/10.1152/ajpcell.1998.274.5.C1273
  21. Lookin O, Protsenko Y (2019) The lack of slow force response in failing rat myocardium: role of stretch-induced modulation of Ca-TnC kinetics. J Physiol Sci 69: 345–357. https://doi.org/10.1007/s12576-018-0651-3
  22. Woody MS, Greenberg MJ, Barua B, Winkelmann DA, Goldman YE, Ostap EM (2018) Positive cardiac inotrope omecamtiv mecarbil activates muscle despite suppressing the myosin working stroke. Nat Commun 9: 3838. https://doi.org/10.1038/s41467-018-06193-2
  23. Shchepkin DV, Nabiev SR, Nikitina LV, Kochurova AM, Berg VY, Bershitsky SY, Kopylova GV (2020) Myosin from the ventricle is more sensitive to omecamtiv mecarbil than myosin from the atrium. Biochem Biophys Res Commun 528: 658–663. https://doi.org/10.1016/j.bbrc.2020.05.108
  24. Gollapudi SK, Reda SM, Chandra M (2017) Omecamtiv Mecarbil Abolishes Length-Mediated Increase in Guinea Pig Cardiac Myofiber Ca2+ Sensitivity. Biophys J 113: 880–888. https://doi.org/10.1016/j.bpj.2017.07.002
  25. Kampourakis T, Zhang X, Sun Y-B, Irving M (2018) Omecamtiv mercabil and blebbistatin modulate cardiac contractility by perturbing the regulatory state of the myosin filament. J Physiol 596: 31–46. https://doi.org/10.1113/JP275050
  26. Nakanishi T, Oyama K, Tanaka H, Kobirumaki-Shimozawa F, Ishii S, Terui T, Ishiwata S, Fukuda N (2022) Effects of omecamtiv mecarbil on the contractile properties of skinned porcine left atrial and ventricular muscles. Front Physiol 13: 947206. https://doi.org/10.3389/fphys.2022.947206
  27. Little SC, Biesiadecki BJ, Kilic A, Higgins RSD, Janssen PML, Davis JP (2012) The rates of Ca2+ dissociation and cross-bridge detachment from ventricular myofibrils as reported by a fluorescent cardiac troponin C. J Biol Chem 287: 27930–27940. https://doi.org/10.1074/jbc.M111.337295
  28. Dou Y, Arlock P, Arner A (2007) Blebbistatin specifically inhibits actin-myosin interaction in mouse cardiac muscle. Am J Physiol Cell Physiol 293: C1148–C1153. https://doi.org/10.1152/ajpcell.00551.2006
  29. Fedorov VV, Lozinsky IT, Sosunov EA, Anyukhovsky EP, Rosen MR, Balke CW, Efimov IR (2007) Application of blebbistatin as an excitation-contraction uncoupler for electrophysiologic study of rat and rabbit hearts. Heart Rhythm 4: 619–626. https://doi.org/10.1016/j.hrthm.2006.12.047
  30. Li W, Luo X, Ulbricht Y, Guan K (2021) Blebbistatin protects iPSC-CMs from hypercontraction and facilitates automated patch-clamp based electrophysiological study. Stem Cell Res 56: 102565. https://doi.org/10.1016/j.scr.2021.102565
  31. Farman GP, Tachampa K, Mateja R, Cazorla O, Lacampagne A, de Tombe PP (2008) Blebbistatin: Use as inhibitor of muscle contraction. Pflugers Arch – Eur J Physiol 455: 995–1005. https://doi.org/10.1007/s00424-007-0375-3
  32. Kossmann CE, Huxley HE (1961) The Contractile Structure of Cardiac and Skeletal Muscle. Circulation 24: 328–335. https://doi.org/10.1161/01.CIR.24.2.328
  33. Trombitás K, Tigyi-Sebes A (1984) Cross-bridge interaction with oppositely polarized actin filaments in double-overlap zones of insect flight muscle. Nature 309: 168–170. https://doi.org/10.1038/309168a0
  34. Dobesh DP, Konhilas JP, de Tombe PP (2002) Cooperative activation in cardiac muscle: Impact of sarcomere length. Am J Physiol Heart Circ Physiol 282: H1055–H1062. https://doi.org/10.1152/ajpheart.00667.2001
  35. Smith L, Tainter C, Regnier M, Martyn DA (2009) Cooperative cross-bridge activation of thin filaments contributes to the Frank-Starling mechanism in cardiac muscle. Biophys J 96: 3692–3702. https://doi.org/10.1016/j.bpj.2009.02.018
  36. Khokhlova A, Konovalov P, Iribe G, Solovyova O, Katsnelson L (2020) The Effects of Mechanical Preload on Transmural Differences in Mechano-Calcium-Electric Feedback in Single Cardiomyocytes: Experiments and Mathematical Models. Front Physiol 11: 171. https://doi.org/10.3389/fphys.2020.00171
  37. Alenezi F, Rajagopal S (2021) The right atrium, more than a storehouse. Int J Cardiol 331: 329–330. https://doi.org/10.1016/j.ijcard.2021.01.069
  38. Korakianitis T, Shi Y (2006) Effects of atrial contraction, atrioventricular interaction and heart valve dynamics on human cardiovascular system response. Med Eng Phys 28: 762–779. https://doi.org/10.1016/j.medengphy.2005.11.005
  39. Jasaityte R, Claus P, Teske AJ, Herbots L, Verheyden B, Jurcut R, Rademakers F, D’hooge J (2013) The Slope of the Segmental Stretch-Strain Relationship as a Noninvasive Index of LV Inotropy. JACC: Cardiovasc Imag 6: 419–428. https://doi.org/10.1016/j.jcmg.2012.10.022
  40. Gaynor SL, Maniar HS, Prasad SM, Steendijk P, Moon MR (2005) Reservoir and conduit function of right atrium: Impact on right ventricular filling and cardiac output. Am J Physiol Heart Circ Physiol 288: H2140–H2145. https://doi.org/10.1152/ajpheart.00566.2004

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