Skip to main content
SpringerLink
Log in

Excitation-contraction coupling of the developing rat heart

  • Part I: Cardiac Development and Regulation
  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Postnatal maturation of rat heart is characterized by increases in force production, velocity of shortening and heart rate. Simultaneously with the enhanced cardiac power production the size of ventricular myocytes markedly increases. Parallel increase in cardiac rate functions and cells size would be expected to require reorganization of cardiac Ca regulation so that adequate rate of Ca release and uptake can be maintained. In accordance with this the source of activator Ca shifts from extracellular space to intracellular stores within the first four or five weeks of postnatal life. Calcium handling of sarcoplasmic reticulum and sarcolemma change in complementary manner so that diminishing sarcolemmal Ca transport is compensated with enhanced Ca release and sequestration by the sarcoplasmic reticulum during the early postnatal development of rat heart. These functional changes are partly due to reciprocal alterations in surface area of sarcolemma and sarcoplasmic reticulum, partly due to age-dependent changes in the expression of different transport systems and their kinetic properties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Hopkins SF, McCutcheon EP, Wekstein DR: Postnatal changes in rat ventricular function. Circ Res 32: 685–691, 1973

    PubMed  Google Scholar 

  2. Cappelli V, Bottinelli R, Poggesi C, Moggio R, Reggiani C: Shortening velocity and myosin and myofibrillar ATPase activity related to myosin isoenzyme composition during postnatal development in rat myocardium. Circ Res 65: 446–457, 1989

    PubMed  Google Scholar 

  3. Wekstein DR: Heart rate of the preweanling rat and its autonomic control. Am J Physiol 208: 1259–1262, 1965

    PubMed  Google Scholar 

  4. Lompré AM, Nadal-Ginard B, Mahdavi V: Expression of the cardiac ventricular α- and β-myosin heavy chain genes is developmentally and hormonally regulated. J Biol Chem 259: 6437–6446, 1984

    PubMed  Google Scholar 

  5. Reiser PJ, Westfall MV, Schiaffino S, Solaro RJ: Tension production and thin-filament protein isoforms in developing rat myocardium. Am J Physiol 267: H1589-H1596, 1994

    PubMed  Google Scholar 

  6. Fabiato A, Fabiato F: Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat and frog hearts and from fetal and new-born rat ventricles. Ann NY Acad Sci 307: 491–522, 1978

    PubMed  Google Scholar 

  7. Vornanen M: Regulation of contractility by cellular membrane systems in ventricular muscle of neonatal and adult rat heart: studies with isolated cells and intact tissue. (PhD Thesis), University of Joensuu Publications in Sciences No 6: 1–58, 1985

  8. Clubb FJ, Bishop SP: Formation of binucleated myocardial cells in the neonatal rat. An index for growth hypertrophy. Lab Invest 50: 571–577, 1984

    PubMed  Google Scholar 

  9. Vornanen M: Contribution of Ca current to total cellular Ca in postnatally developing rat heart. Cardiovasc Res (in press), 1996

  10. Vornanen M: Force-frequency relationship, contraction duration and recirculating fraction of calcium in postnatally developing rat heart ventricle: correlation with heart rate. Acta Physiol Scand 145: 311–321, 1992

    PubMed  Google Scholar 

  11. Sham JSK, Cleeman L, Morad M: Functional coupling of Ca2+ channels and ryanodine receptors in cardiac myocytes. Proc Natl Acad Sci USA 92:121–125, 1995

    PubMed  Google Scholar 

  12. Negretti N, O'Neill SC, Eisner DA: The relative contributions of different intracellular and sarcolemmal systems to relaxation in rat ventricular myocytes. Cardiovasc Res 27: 1826–1830, 1993

    PubMed  Google Scholar 

  13. Bassani JWM, Bassani RA, Bers DM: Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476: 279–293, 1994

    PubMed  Google Scholar 

  14. Negretti N, Varro A, Eisner DA: Estimate of net calcium fluxes and sarcoplasmic reticulum calcium content during systole in rat ventricular myocytes. J Physiol 486.3: 581–591, 1995

    Google Scholar 

  15. Olivetti G, Anversa P, Loud AV: Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. II. Tissue composition, capillary growth, and sarcoplasmic alterations. Circ Res 46: 503–512, 1980

    PubMed  Google Scholar 

  16. Page E, Early J, Power B: Normal growth of ultrastructures in rat left ventricular myocardial cells. Circ Res 34–35 (Suppl. II): 12–16, 1974

    Google Scholar 

  17. Page E: Quantitative ultrastructural analysis in cardiac membrane physiology. Am J Physiol 235: C147-C158, 1978

    PubMed  Google Scholar 

  18. Schiebler TH, Wolf HH: Elektronenmikroskopische Untersuchungen am Herzmuskel der Ratte während der Entwicklung. Z Zellforsch 69: 22–40, 1966

    PubMed  Google Scholar 

  19. Sommer JR: Comparative anatomy: in praise of a powerful approach to elucidate mechanisms translating cardiac excitation into purposeful contraction. J Mol Cell Cardiol 27: 19–35, 1995

    PubMed  Google Scholar 

  20. Stern MD: Theory of excitation-contraction coupling in cardiac muscle. Biophys J 63: 497–517, 1992

    PubMed  Google Scholar 

  21. Rousseau E, Smith JS, Meissner G: Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol 253: C364-C368, 1987

    PubMed  Google Scholar 

  22. Jorgensen AO, Shen AC-Y, Arnold W, McPherson PS, Campbell KP: The Ca 2+ channel/ryanodine receptor is localized in junctional and corbular sarcoplasmic reticulum in cardiac muscle. J Cell Biol 120: 969–980, 1993

    PubMed  Google Scholar 

  23. Fabiato A: Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245: C1-C14, 1983

    PubMed  Google Scholar 

  24. Levi AJ, Brooksby P, Hancox JC: A role for depolarization induced calcium entry on the Na-Ca exchange in triggering intracellular calcium release and contraction in rat ventricular myocytes. Cardiovasc Res 27: 1677–1690, 1993

    PubMed  Google Scholar 

  25. Page E, Surdyk-Droske M: Distribution, surface density, and membrane area of diadic junctional contacts between plasma membrane and terminal cisterns in mammalian ventricle. Circ Res 45: 260–267, 1979

    PubMed  Google Scholar 

  26. Wohlfart B: Relationship between peak force, action potential duration and stimulus interval in rabbit myocardium. Acta Physiol Scand 106: 395–409, 1979

    PubMed  Google Scholar 

  27. Urthaler F, Walker AA, Reeves RC, Hefner LL: Estimates of beat to beat handling of activator calcium using measurements of [Ca2+]i in aequorin loaded ferret cardiac muscle. Cardiovasc Res 28: 40–46, 1994

    PubMed  Google Scholar 

  28. Kojima S, Wu ST, Wikman-Coeffelt J, Parmley WW: Contractile and intracellular Ca2+ decay in potentiated contractions following multiple extrasystolic beats. Cell Calcium 18: 155–164, 1995

    Article  PubMed  Google Scholar 

  29. Shattock MJ, Bers DM: Rat vs. rabbit ventricle: Ca flux and intracellular Na assessed by ion-selective microelectrodes. Am J Physiol 256: C813-C822, 1989

    PubMed  Google Scholar 

  30. Vomanen M: Effects of caffeine on the mechanical properties of developing rat heart ventricles. Comp Biochem Physiol 78C: 239–334, 1984

    Google Scholar 

  31. Vornanen M: Postnatal changes in the inotropic effect of ouabain on the rat heart ventricle. Basic Res Cardiol 82: 82–91, 1987

    PubMed  Google Scholar 

  32. Ramesch V, Kresch MJ, Katz AM, Kim DH: Characterization of Ca2+-release in fetal and adult rat heart. Am J Physiol 269: H778-H782, 1995

    PubMed  Google Scholar 

  33. Agata N, Tanaka H, Shigenobu K: Possible action of cyclopiazonic acid on myocardial sarcoplasmic reticulum: inotropic effects on neonatal and adult rat heart. Br J Pharmac 108: 571–572, 1993

    Google Scholar 

  34. Chiesi M, Wrzosek A, Grueninger S: The role of the sarcoplasmic reticulum in various types of cardiomyocytes. Mol Cell Biochem 130: 159–171, 1994

    PubMed  Google Scholar 

  35. Tanaka H, Shigenobu K: Effect of ryanodine on neonatal and adult rat heart: Developmental increase in sarcoplasmic reticulum function. J Mol Cell Cardiol 21: 1305–1313, 1989

    Article  PubMed  Google Scholar 

  36. Pucelik P, Jezek K, Bartak F: Postnatal development of electrophysiological manifestation of the working ventricular myocardium of albino rats. Physiol Bohemosl 31: 217–224, 1982

    Google Scholar 

  37. Wahler GM, Dollinger S, Smith JM, Flemal KL: Time course of postnatal changes in rat heart action potential and in transient outward current is different. Am J Physiol 267: H1157-H1166, 1994

    PubMed  Google Scholar 

  38. Moorman AFM, Lamers WH: Molecular anatomy of the developing heart. Trends Cardiovasc Med 4: 257–264, 1994

    Article  Google Scholar 

  39. Lompré AM, Lambert F, Lakatta EG, Schwartz K: Expression of sarcoplasmic reticulum Ca2+-ATPase and calsequestrin genes in rat heart during ontogenetic development and aging. Circ Res 69: 1380–1388, 1991

    PubMed  Google Scholar 

  40. Komuro I, Kurabayashi M, Shibazaki Y, Takaku F, Yazaki Y: Molecular cloning and characterization of a Ca2+ Mg2+-dependent adenosine triphosphatase from rat cardiac sarcoplasmic reticulum. J Clin Invest 83: 1102–1108, 1989

    PubMed  Google Scholar 

  41. Feher JJ, LeBolt WR: Stabilization of rat cardiac sarcoplasmic reticulum Ca2+ activity and isolation of vesicles with improved calcium uptake activity. Mol Cell B 99: 41–52, 1990

    Google Scholar 

  42. Simonides WS, Van Hardeveld C: An assay for sarcoplasmic reticulum Ca2+-ATPase activity in muscle homogenates. Anal Biochem 191: 321–331, 1990

    PubMed  Google Scholar 

  43. Kirby MS, Sagara Y, Gaa S, Inesi G, Lederer WJ, Rogers TB: Thapsigargin inhibits contraction and Ca 2+ transient in cardiac cells by specific inhibition of the sarcoplasmic reticulum Ca2+ pump. J Biol Chem 267:12545–12551, 1992

    PubMed  Google Scholar 

  44. Vetter R, Studer R, Reinecke M, Kolar F, Ostadalova I, Drexler H: Reciprocal changes in the postnatal expression of the sarcolemmal Na+-Ca2+-exchanger and SERCA2 in rat heart. J Mol Cell Cardiol 27: 1689–1701, 1995

    Article  PubMed  Google Scholar 

  45. Skovranek J, Ostadal B, Pelouch V, Prochazka J: Ontogenetic differences in cardiac sensitivity to verapamil in rats. Pediatr Cardiol 7: 25–29, 1986

    PubMed  Google Scholar 

  46. Masuda H, Sumii K, Sperelakis N: Long openings of calcium channels in fetal rat ventricular cardiomyocytes. Pflugers Archiv 429: 595–597, 1995

    PubMed  Google Scholar 

  47. Gao W, Backx PH, Azan-Backx M, Marban E: Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle. Circ Res 74: 408–415, 1994

    PubMed  Google Scholar 

  48. Berlin JR, Bassani JWM, Bers DM: Intrinsic cytosolic calcium buffering properties of single rat cardiac myocytes. Biophys J 67: 1775–1787, 1994

    PubMed  Google Scholar 

  49. Gomez J-P, Potreau D, Raymond G: Intracellular calcium transients from newborn rat cardiomyocytes in primary culture. Cell Calcium 15:265–275, 1994

    Article  PubMed  Google Scholar 

  50. Vetter R, Kemsies C, Schulze W: Sarcolemmal Na+-Ca2+ exchange and sarcoplasmic reticulum Ca2+ uptake in several cardiac preparations. Biomed Biochim Acta 46: 375–381, 1987

    Google Scholar 

  51. Boerth SR, Zimmer DB, Artman M: Steady-state mRNA levels of the sarcolemmal Na+-Ca2+ exchanger peak near birth in developing rabbit and rat hearts. Circ Res 74: 354–359, 1994

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Joensuu, P.O. Box 111 80101, Joensuu, Finland

    Matti Vornanen

Authors
  1. Matti Vornanen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vornanen, M. Excitation-contraction coupling of the developing rat heart. Mol Cell Biochem 163, 5–11 (1996). https://doi.org/10.1007/BF00408635

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00408635

Key words

Search

Navigation