Skip to main content
Log in

Sarcoplasmic reticulum: a key factor in cardiac contractility of sea bass Dicentrarchus labrax and common sole Solea solea during thermal acclimations

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

This study investigated the effects of acclimation temperature upon (i) contractility of ventricular strips (ii) calcium movements in ventricular cardiomyocytes during excitation–contraction coupling (ECC), and (iii) the role of the sarcoplasmic reticulum (SR) in myocardial responses, in two marine teleosts, the sea bass (Dicentrarchus labrax) and the common sole (Solea solea). Because of the different sensitivities of their metabolism to temperature variation, both species were exposed to different thermal ranges. Sea bass were acclimated to 10, 15, 20, and 25 °C, and common sole to 6, 12, 18, and 24 °C, for 1 month. Isometric tension developed by ventricular strips was recorded over a range of physiological stimulation frequencies, whereas the depolarization-induced calcium transients were recorded on isolated ventricular cells through hyperpotassic solution application (at 100 mM). The SR contribution was assessed by ryanodine (RYAN) perfusion on ventricular strips and by caffeine application (at 10 mM) on isolated ventricular cells. Rates of contraction and relaxation of ventricular strip, in both species, increased with increasing acclimation temperature. At a low range of stimulation frequency, ventricular strips of common sole developed a positive force–frequency relationship at high acclimation temperature. In both the species, SR Ca2+-cycling was dependent on fish species, acclimation temperature and pacing frequency. The SR contribution was more important to force development at low acclimation temperatures in sea bass but at high acclimation temperatures in common sole. The results also revealed that high acclimation temperature causes an increase in the maximum calcium response amplitude on ventricular cells in both the species. Although sea bass and common sole occupy similar environments and tolerate similar environmental temperatures, this study indicated that sea bass and common sole can acclimatize to new thermal conditions, adjusting their cellular process in a different manner.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

BSA:

Bovine serum albumin

CICR:

Ca2+-induced Ca2+-release

DMSO:

Dimethyl sulfoxide

ECC:

Excitation-contraction coupling

EGTA:

Ethylene glycol tetraacetic acid

ICaL:

L-type Ca2+-current

NCX:

Na+/Ca2+exchanger

PMCA:

Sarcolemmal Ca2+-ATPase pump

RYAN:

Ryanodine

SERCA:

SR Ca2+-ATPase pumps

SL:

Sarcolemma

SR:

Sarcoplasmic reticulum

References

  • Aho E, Vornanen M (1998) Ca2+ -ATPase activity and Ca2+ uptake by the sarcoplasmic reticulum in fish heart: effects of thermal acclimation. J Exp Biol 201:525–532

    PubMed  CAS  Google Scholar 

  • Aho E, Vornanen M (1999) Contractile properties of atrial and ventricular tissue of the rainbow trout (Oncorhynchus mykiss) heart: effects of thermal acclimation. J Exp Biol 202:2663–2677

    PubMed  Google Scholar 

  • Bassani JW, Weilong Y, Bers DM (1995) Fractional SR Ca release is regulated by trigger Ca and SR Ca content in cardiac myocytes. Am J Physiol 268:C1313–C1329

    PubMed  CAS  Google Scholar 

  • Birkedal R, Christopher J, Thistlethwaite A, Shiels H (2009) Temperature acclimation has no effect on ryanodine receptor expression or subcellular localization in rainbow trout heart. J Comp Physiol B 179:961–969

    Article  PubMed  CAS  Google Scholar 

  • Bowler K, Tirri R (1990) Temperature dependence of the heart isolated from the cold or warm acclimated perch (Perca fluviatilis). Comp Biochem Physiol A 96:177–180

    Article  Google Scholar 

  • Castilho PC, Landeira-Fernandez AM, Block BA (2007) Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: comparative aspects of temperature dependence. Comp Biochem Physiol A 148:124–132

    Google Scholar 

  • Chatelier A, Imbert N, Zambonino Infante JL, McKenzie DJ, Bois P (2006) Effects of oleic acid on the high threshold barium current in sea bass (Dicentrarchus labrax) ventricular myocytes. J Exp Biol 209:4033–4039

    Article  PubMed  CAS  Google Scholar 

  • Claireaux G, Lagardere JP (1999) Influence of temperature, oxygen and salinity on the metabolism of European sea bass. J Sea Res 42:157–168

    Article  CAS  Google Scholar 

  • Cohen O, Kanana H, Zoizner R, Gross C, Meiri U, Stern M, Gerstenblith G, Horowitz M (2006) Altered Ca2_ handling and myofilament desensitization underlie cardiomyocyte performance in normothermic and hyperthermic heat-acclimated rat hearts. J Appl Physiol 103:266–275

    Article  Google Scholar 

  • Driedzic WR, Bailey JR, Septon DH (1996) Cardiac adaptations to low temperature in non-polar teleost fish. J Exp Zool 275:186–195

    Article  Google Scholar 

  • Erickson JR, Sidell BD, Moerland TM (2005) Temperature sensitivity of calcium binding for parvalbumins from Antarctic and temperate zone teleost fishes. Comp Biochem Physiol A 140:179–185

    Article  Google Scholar 

  • Farrell AP (1997) Effects of temperature on cardiovascular performance. In: Wood CM, MacDonald DG (eds) Global warming implications for freshwater and marine fish, society for experimental biology, seminar series 61. Cambridge University Press, Cambridge, pp 135–153

    Chapter  Google Scholar 

  • Galli GL, Lipnick MS, Block BA (2009) Effect of thermal acclimation on action potentials and sarcolemmal K+ channels from Pacific bluefin tuna cardiomyocytes. Am J Physiol 297(2):R502–509

    Google Scholar 

  • Galli GL, Lipnick MS, Shiels HA, Block BA (2011) Temperature effects on Ca2 + cycling in scombrid cardiomyocytes: a phylogenetic comparison. J Exp Biol 214:1068–1076

    Article  PubMed  CAS  Google Scholar 

  • Gamperl AK, Wilkinson M, Boutilier RG (1994) β-Adrenoreceptors in the trout (Oncorhynchus mykiss) heart: characterization, quantification and effects of repeated catecholamine exposure. Gen Comp Endocr 95:259–272

    Article  PubMed  CAS  Google Scholar 

  • Gomez JP, Potreau D, Raymond G (1994) Intracellular calcium transients from newborn rat cardiomyocytes in primary culture. Cell Calcium 15:265–275

    Article  PubMed  CAS  Google Scholar 

  • Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved florescence properties. J Biol Chem 260:3440–3450

    PubMed  CAS  Google Scholar 

  • Györke S, Terentyev D (2008) Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res 77:245–255

    Article  PubMed  Google Scholar 

  • Harwood CL, Howarth FC, Altringham JD, White ED (2000) Rate-dependant changes in cell shortening, intracellular Ca2+ levels and membrane potential in single, isolated rainbow trout (Onchorhynchus mykiss) ventricular myocytes. J Exp Biol 203:493–504

    PubMed  CAS  Google Scholar 

  • Haverinen J, Vornanen M (2009) Comparison of sarcoplasmic reticulum calcium content in atrial and ventricular myocytes of three fish species. Am J Physiol 297:R1180–R1187

    CAS  Google Scholar 

  • Hove-Madsen L (1992) The influence of temperature on ryanodine sensitivity and the force–frequency relationship in the myocardium of rainbow trout. J Exp Biol 167:47–60

    PubMed  CAS  Google Scholar 

  • Hove-Madsen L, Llach A, Tort L (1998) Quantification of Ca2+ uptake in the sarcoplasmic reticulum of trout ventricular myocytes. Am J Physiol 275:R2070–R2080

    PubMed  CAS  Google Scholar 

  • Keen JE, Farrell AP, Tibbits GF, Brill RW (1992) Cardiac physiology in tunas. II. Effect of ryanodine, calcium, and adrenaline on force–frequency relationships in atrial strips from skipjack tuna, Katsuwonus Pelamis. Can J Zool 70:1211–1217

    Article  CAS  Google Scholar 

  • Keen JE, Viazon DM, Farrell AP, Tibbits GF (1994) Effect of temperature acclimation on the ryanodine sensitivity of the trout myocardium. J Comp Physiol B 164:438–443

    Article  CAS  Google Scholar 

  • Landeira-Fernandez AM, Morrissette JM, Blank JM, Block BA (2004) Temperature dependence of the Ca2+-ATPase (SERCA2) in the ventricles of tuna and mackerel. Am J Physiol 286:R398–R404

    Article  CAS  Google Scholar 

  • Larsson D, Larsson B, Lundgren T, Sundell K (1999) The effect of pH and temperature on the dissociation constant for Fura-2 and their effects on [Ca2+]i in enterocytes from a poikilothermic animal, Atlantic cod (Gadus morhua). Anat Biochem 273:60–65

    Article  CAS  Google Scholar 

  • Lefrançois C, Claireaux G (2003) Influence of ambient oxygenation and temperature on metabolic scope and heart rate of common sole (Solea solea). Mar Ecol Prog Ser 259:273–284

    Article  Google Scholar 

  • Matikainen N, Vornanen M (1992) Effect of season and temperature acclimation on the function of crucian carp (Carassius carassius) heart. J Exp Biol 167:203–220

    Google Scholar 

  • Mercier C, Axelsson M, Imbert N, Claireaux G, Lefrançois C, Altimiras J, Farrell AP (2002) In vitro cardiac performance in triploid brown trout at two acclimation temperatures. J Fish Biol 50:117–133

    Article  Google Scholar 

  • Moller-Nielsen T, Gesser H (1992) Sarcoplasmic reticulum and excitation-contraction coupling at 10 and 20 °C in rainbow trout myocardium. J Comp Physiol B 162:526–534

    Article  Google Scholar 

  • Orchard CH, Lakatta EG (1985) Intracellular calcium transients and developed tension in rat heart muscle. J Gen Physiol 86:637–651

    Article  PubMed  CAS  Google Scholar 

  • Pelouch V, Vornanen M (1996) Effects of thermal acclimation on ventricle size, protein composition, and contractile properties of crucian carp heart. J Therm Biol 2(I):1–9

    Article  Google Scholar 

  • Randall DJ, Perry SF (1992) Catecholamines. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology: the cardiovascular system. Academic Press, New York, pp 255–300

    Chapter  Google Scholar 

  • Rivaroli L, Rantin FT, Kalinin AL (2006) Cardiac function of two ecologically distinct Neotropical freshwater fish: Curimbata, Prochilodus lineatus (Teleostei, Prochilodontidae), and trahira, Hoplias malabaricus (Teleostei, Erythrinidae). Comp Biochem Physiol A 145(3):322–327

    Google Scholar 

  • Rousseau E, Smith JS, Meissner G (1987) Ryanodine modifies conductance and gating behaviour of single Ca2+ release channels. Am J Physiol 253:C364–C368

    PubMed  CAS  Google Scholar 

  • Shattock MJ, Bers DM (1987) Inotropic response to hypothermia and the temperature-dependence of ryanodine action in isolated rabbit and rat ventricular muscle: implications for E-C coupling. Cir Res 61:761–771

    Article  CAS  Google Scholar 

  • Shiels HA, Farrell AP (1997) The effects of temperature and adrenaline on the relative importance of the sarcoplasmic reticulum in the contributing Ca2+ to force development in isolated ventricular trabeculae from rainbow trout. J Exp Biol 200:1607–1621

    PubMed  CAS  Google Scholar 

  • Shiels HA, Farrell AP (2000) The effect of ryanodine on isometric tension development in isolated ventricular trabeculae from Pacific mackerel (Scomber japonicus). Comp Biochem Physiol A 125:331–341

    Article  CAS  Google Scholar 

  • Shiels HA, Stevens ED, Farrell AP (1998) Effect of temperature, adrenaline and ryanodine on power production in trout (Oncorhynchus mykiss) ventricular trabeculae. J Exp Biol 201:2701–2710

    PubMed  CAS  Google Scholar 

  • Shiels HA, Freund EV, Farrell AP, Block BA (1999) The sarcoplasmic reticulum plays a major role in isometric contraction in atrial muscle of yellowfin tuna. J Exp Biol 202:881–890

    PubMed  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2002) The force–frequency relationship in fish heart. A review. Comp Biochem Physiol A 132:811–826

    Google Scholar 

  • Tiitu V, Vornanen M (2001) Cold adaptation suppresses the contractility of both atrial and ventricular muscle of the crucian carp heart. J Fish Biol 59:141–156

    Article  CAS  Google Scholar 

  • Tiitu V, Vornanen M (2003) Ryanodine and dihydropyridine receptor binding in ventricular cardiac muscle of fish with different temperature preferences. J Comp Physiol B 173(4):285–291

    Article  PubMed  CAS  Google Scholar 

  • Vornanen M (1989) Regulation of contractility of the fish (Carassius carassius L.) heart ventricle. Comp Biochem Physiol C 94:477–483

    Article  Google Scholar 

  • Vornanen M (1997) Sarcolemmal Ca influx through L-type Ca channels in the ventricular myocytes of a teleost fish. Am J Physiol 272:1432–1440

    Google Scholar 

  • Vornanen M (1998) L-type Ca2+ current in fish cardiac myocytes: effects of thermal acclimation and β-adrenergic stimulation. J Exp Biol 201:533–547

    PubMed  CAS  Google Scholar 

  • Vornanen M (1999) Na+/Ca2+ exchange current in ventricular myocytes of fish heart: contribution to sarcolemmal Ca2+ influx. J Exp Biol 202:1763–1775

    PubMed  CAS  Google Scholar 

  • Vornanen M (2006) Temperature and Ca2+- dependence of [3H]ryanodine binding in the burbot (Lota lota L.) heart. Am J Physiol 290:R345–R351

    CAS  Google Scholar 

  • Vornanen M, Shiels HA, Farrell AP (2002a) Plasticity of excitation-contraction coupling in fish cardiac myocytes. Comp Biochem Physiol A 132(4):827–846

    Article  Google Scholar 

  • Vornanen M, Ryökkynen A, Nurmi A (2002b) Temperature-dependent expression of sarcolemmal K+ currents in rainbow trout atrial and ventricular myocytes. Am J Physiol 282:R1191–R1199

    CAS  Google Scholar 

  • Yue DT (1992) Relationships between intracellular free calcium and force with changes of interval. In: Noble MI, Seed WA (eds) The interval-force relationship of the heart: bowditch revisited. Cambridge University Press., Cambridge, pp 95–109

    Google Scholar 

Download references

Acknowledgments

We are indebted to the Aquarium of La Rochelle and N.Vallee for their technical assistance. The study was funded by the Région Poitou–Charentes, the CNRS and IFREMER.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Imbert-Auvray.

Additional information

Communicated by H.V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Imbert-Auvray, N., Mercier, C., Huet, V. et al. Sarcoplasmic reticulum: a key factor in cardiac contractility of sea bass Dicentrarchus labrax and common sole Solea solea during thermal acclimations. J Comp Physiol B 183, 477–489 (2013). https://doi.org/10.1007/s00360-012-0733-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-012-0733-0

Keywords

Navigation