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Ontogeny and Phylogeny of the Vertebrate Heart pp 103–124Cite as

The Sarcoplasmic Reticulum in the Vertebrate Heart

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Abstract

Excitation–contraction coupling (E–C coupling) is the ubiquitous process which drives contraction and relaxation of the working vertebrate myocardium. E–C coupling links electrical excitation of the cardiomyocyte membrane to mechanical contraction. The fundamental principles of E–C coupling are highly conserved between vertebrate species, but important morphological and functional differences exist. The role of one organelle in particular, the sarcoplasmic reticulum (SR), is highly variable among species, tissue type, age and environmental conditions, and has been linked to cardiac performance and numerous cardiac pathologies. The present review aims to update our knowledge of the role of the SR in different vertebrates, and to discuss the underlying significance of this important organelle. While SR function is well characterised in mammals and reviewed extensively (Michalak and Opas, Trends Cell Biol 19:253–259, 2009; Lanner et al., Cold Spring Harb Perspect Biol 2:a003996, 2010; Lee and Michalak, BMB Rep 43:151–157, 2010; Bers, Excitation-contraction coupling and contractile force, Kluwer Academic, 2001), ectothermic cellular cardiology is a relatively new field. Thus, this review will focus primarily on recent advances in ectothermic E–C coupling, and adult and neonatal mammalian data will only be discussed for comparative purposes. Unfortunately, there is a conspicuous lack of information on E–C coupling and the role of the SR in bird hearts. Considering the interesting position of birds in vertebrate evolution, avian cellular cardiology is undoubtedly an area ripe for future investigation.

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Abbreviations

[Ca2+]i :

Intracellular Ca2+

CASQ:

Calsequestrin

CICR:

Ca2+-induced Ca2+-release

DHPR:

L-type Ca2+ channel dihydropyridine receptor

E–C coupling:

Excitation–contraction coupling

ER:

Endoplasmic reticulum

fSR:

Free SR

jSR:

Junctional SR

NCX:

Na+/Ca2+ exchanger

RyR:

Ryanodine receptor

SERCA:

SR Ca2+ ATPase

SR:

Sarcoplasmic reticulum

References

  • Agata N, Tanaka H, Shigenobu K (1994) Inotropic effects of ryanodine and nicardipine on fetal, neonatal and adult guinea-pig myocardium. Eur J Pharm 260:47–55

    Article  CAS  Google Scholar 

  • Aho E, Vornanen M (1998) Ca2+-ATPase activity and Ca2+ uptake by 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 myocardium of the heart of rainbow trout (Oncorhynchus mykiss): effects of thermal acclimation. J Exp Biol 202:2663–2677

    PubMed  Google Scholar 

  • Anelli LC Jr, Ole CD, Costa MJ, Rantin FT, Kalinin AL (2004) Effects of temperature and calcium availability on ventricular myocardium from the neotropical teleost Piaractus mesopotamicus (Holmberg 1887—Teleostei, Serrasalmidae). J Therm Biol 29:103–113

    Article  CAS  Google Scholar 

  • Arai M, Otsu K, MacLennan DH, Periasamy M (1992) Regulation of sarcoplasmic reticulum gene expression during cardiac and skeletal muscle development. Am J Physiol 262:C614–20

    PubMed  CAS  Google Scholar 

  • Bailey JR, Val AL, Almeida-Val V, Driedzic WR (1999) Anoxic cardiac performance in Amazonian and north-temperate-zone teleosts. Can J Zool 77:683–689

    Article  Google Scholar 

  • Belke DD, Milner RE, Wang LC (1991) Seasonal variations in the rate and capacity of cardiac SR calcium accumulation in a hibernating species. Cryobiology 28:354–63

    Article  PubMed  CAS  Google Scholar 

  • Bers DM (1985) Ca influx and sarcoplasmic reticulum Ca release in cardiac muscle activation during postrest recovery. Am J Physiol 248:H366–H381

    PubMed  CAS  Google Scholar 

  • Bers DM (1989) SR Ca2+ loading in cardiac muscle preparations based on rapid-cooling contractures. Am J Physiol 256:C109–C120

    PubMed  CAS  Google Scholar 

  • Bers DM (2001) Excitation-contraction coupling and contractile force. Kluwer Academic, Dordecht

    Book  Google Scholar 

  • Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198–205

    Article  PubMed  CAS  Google Scholar 

  • Bers DM, Bridge JH (1989) Relaxation of rabbit ventricular muscle by Na-Ca exchange and sarcoplasmic reticulum calcium pump. Ryanodine and voltage sensitivity. Circ Res 65:334–342

    Article  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 

  • Bootman MD, Higazi DR, Coombes S, Roderick HL (2006) Calcium signalling during excitation-contraction coupling in mammalian atrial myocytes. J Cell Sci 119:3915–3925

    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, Morrissette J, Block BA (2007) Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: comparative aspects of temperature dependence. Comp Biochem Physiol 148:124–132

    Google Scholar 

  • Chugun A, Oyamada T, Temma K, Hara Y, Kondo H (1999) Intracellular Ca2+ storage sites in the carp heart: comparison with the rat heart. Comp Biochem Physiol 123:61–67

    Article  CAS  Google Scholar 

  • Chugun A, Taniguchi K, Murayama T, Uchide T, Hara Y, Temma K, Ogawa Y, Akera T (2003) Subcellular distribution of ryanodine receptors in the cardiac muscle of carp (Cyprinus carpio). Am J Physiol 285:R601–R609

    Google Scholar 

  • Cordeiro JM, Malone JE, Di Diego JM, Scornik FS, Aistrup GL, Antzelevitch C, Wasserstrom JA (2007) Cellular and subcellular alternans in the canine left ventricle. Am J Physiol 293: H3506–16

    CAS  Google Scholar 

  • Dan P, Lin E, Huang J, Biln P, Tibbits GF (2007) Three-dimensional distribution of cardiac Na+-Ca2+ exchanger and ryanodine receptor during development. Biophys J 93:2504–2518

    Article  PubMed  CAS  Google Scholar 

  • Di Maio A, Block BA (2008) Ultrastructure of the sarcoplasmic reticulum in cardiac myocytes from Pacific bluefin tuna. Cell Tissue Res 334:121–134

    Article  PubMed  Google Scholar 

  • Dibb KM, Hagarty CL, Loudon ASI, Trafford AW (2005) Photoperiod-dependent modulation of cardiac excitation contraction coupling in the Siberian hamster. Am J Physiol 288: R607–R614

    CAS  Google Scholar 

  • Dibb KM, Clarke JD, Horn MA, Richards MA, Graham HK, Eisner DA, Trafford AW (2009) Characterization of an extensive transverse tubular network in sheep atrial myocytes and its depletion in heart failure. Circ Heart Fail 2:482–9

    Article  PubMed  Google Scholar 

  • Endoh M (2004) Force-frequency relationship in intact mammalian ventricular myocardium: physiological and pathophysiological relevance. Eur J Pharm 500:73–86

    Article  CAS  Google Scholar 

  • Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245:1–14

    Google Scholar 

  • Fisher DJ, Tate CA, Phillips S (1992) Developmental regulation of the sarcoplasmic reticulum calcium pump in the rabbit heart. Pediatr Res 31:474–9

    Article  PubMed  CAS  Google Scholar 

  • Galli GLJ, Taylor EW, Shiels HA (2006a) Calcium flux in turtle ventricular myocytes. Am J physiol 291:R1781–R1789

    CAS  Google Scholar 

  • Galli GLJ, Gesser H, Taylor EW, Shiels HA, Wang T (2006b) The role of the sarcoplasmic reticulum in the generation of high heart rates and blood pressures in reptiles. J Exp Biol 209: 1956–1963

    Article  PubMed  Google Scholar 

  • Galli GLJ, Shiels HA, Brill R (2008) Temperature sensitivity of cardiac function in pelagic fishes with different vertical mobilities: yellowfin tuna (Thunnus albacares), bigeye tuna (T. obesus), mahimahi (Coryphaena hippurus) and swordfish (Xiphias gladius). Phys Biochem Zool 82:280–90

    Article  Google Scholar 

  • Galli GLJ, Warren DE, Shiels HA (2009) Ca2+ cycling in cardiomyocytes from a high-performance reptile, the varanid lizard (Varanus exanthematicus). Am J physiol 297:R1636–44

    CAS  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 214:1068–76

    Article  PubMed  CAS  Google Scholar 

  • Gamperl AK, Swafford BL, Rodnick KJ (2011) Elevated temperature, per se, does not limit the ability of rainbow trout to increase stroke volume. J Therm Biol 36:7–14

    Article  Google Scholar 

  • Gyorke I, Gyorke S (1998) Regulation of the cardiac ryanodine receptor channel by luminal Ca2+ involves luminal Ca2+ sensing sites. Biophys J 75:2801–10

    Article  PubMed  CAS  Google Scholar 

  • Gyorke S, Terentyev D (2008) Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res 77:245–55

    Article  PubMed  CAS  Google Scholar 

  • Haddock PS, Coetzee WA, Cho E, Porter L, Katoh H, Bers DM, Jafri MS, Artman M (1999) Subcellular [Ca2+]i gradients during excitation-contraction coupling in newborn rabbit ventricular myocytes. Circ Res 85:415–427

    Article  PubMed  CAS  Google Scholar 

  • Harrer JM, Haghighi K, Kim HW, Ferguson DG, Kranias EG (1997) Coordinate regulation of SR Ca2+-ATPase and phospholamban expression in developing murine heart. Am J Physiol 272:H57–66

    PubMed  CAS  Google Scholar 

  • Haverinen J, Vornanen M (2008) Responses of action potential and K+ currents to chronic thermal stress in fish hearts. Phylogeny or thermal preferences? Phys Biochem Zool 82:468–82

    Article  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:R1180–7

    CAS  Google Scholar 

  • Herve JC, Yamaoka K, Twist VW, Powell T, Ellory JC, Wang LC (1992) Temperature dependence of electrophysiological properties of guinea pig and ground squirrel myocytes. Am J Physiol 263:177–84

    Google Scholar 

  • Hove-Madsen L, Bers DM (1993a) Passive Ca buffering and SR Ca uptake in permeabilized rabbit ventricular myocytes. Am J Physiol 264:C677–C686

    PubMed  CAS  Google Scholar 

  • Hove-Madsen L, Bers DM (1993b) Sarcoplasmic reticulum Ca2+ uptake and thapsigargin sensitivity in permeabilized rabbit and rat ventricular myocytes. Circ Res 73:820–828

    Article  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 44:R2070–R2080

    Google Scholar 

  • Hove-Madsen L, Llach A, Tort L (2001) The function of the sarcoplasmic reticulum is not inhibited by low temperatures in trout atrial myocytes. Am J Physiol 281:R1902–R1906

    CAS  Google Scholar 

  • Huang J, Hove-Madsen L, Tibbits GF (2008) Ontogeny of Ca2+-induced Ca2+ release in rabbit ventricular myocytes. Am J Physiol 294:C516–C525

    Article  CAS  Google Scholar 

  • Huser J, Lipsius SL, Blatter LA (1996) Calcium gradients during excitation-contraction coupling in cat atrial myocytes. J Physiol 494:641–651

    PubMed  CAS  Google Scholar 

  • Keen JE, Farrell AP, Tibbits GF, Brill RW (1992) Cardiac physiology in Tunas. 2. 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, Vianzon DM, Farrell AP, Tibbits GF (1994) Effect of temperature and temperature-acclimation on the ryanodine sensitivity of the trout myocardium. J Comp Physiol 164: 438–443

    CAS  Google Scholar 

  • Korajoki H, Vornanen M (2009) Expression of calsequestrin in atrial and ventricular muscle of thermally acclimated rainbow trout. J Exp Biol 212:3403–14

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Laver DR (2007) Ca2+ stores regulate ryanodine receptor Ca2+ release channels via luminal and cytosolic Ca2+ sites. Clin Exp Pharm Physiol 34:889–96

    Article  CAS  Google Scholar 

  • Llach A, Tibbits GF, Sedarat F, Tort L, Hove-Madsen L (2001) Low temperature reduces Na+-Ca2+ exchange rate but not SR Ca2+ release in trout atrial myocytes. Biophysical J 80:585A

    Google Scholar 

  • Llach A, Molina CE, Alvarez-Lacalle E, Tort L, Benítez R and Hove-Madsen L (2011) Detection, properties and frequencies of local calcium release form the sarcoplasmic reticulum in teleost cardiomyocytes. PLOS one 6: e23708

    Google Scholar 

  • Lukyanenko V, Ziman A, Lukyanenko A, Salnikov V, Lederer WJ (2007) Functional groups of ryanodine receptors in rat ventricular cells. J Physiol 583:251–269

    Article  PubMed  CAS  Google Scholar 

  • Luss I, Boknik P, Jones LR, Kirchhefer U, Knapp J, Linck B, Luss H, Meissner A, Muller FU, Schmitz W, Vahlensieck U, Neumann J (1999) Expression of cardiac calcium regulatory proteins in atrium v ventricle in different species. J Mol Cell Cardiol 31:1299–1314

    Article  PubMed  CAS  Google Scholar 

  • Mackenzie L, Bootman MD, Berridge MJ, Lipp P (2001) Predetermined recruitment of calcium release sites underlies excitation-contraction coupling in rat atrial myocytes. J Physiol 530:417–429

    Article  PubMed  CAS  Google Scholar 

  • Mahony L, Jones LR (1986) Developmental changes in cardiac sarcoplasmic reticulum in sheep. J Biol Chem 261:15257–65

    PubMed  CAS  Google Scholar 

  • Maylie JG (1982) Excitation-contraction coupling in neonatal and adult myocardium of cat. Am J physiol 242:H834–43

    PubMed  CAS  Google Scholar 

  • Michalak M, Opas M (2009) Endoplasmic and sarcoplasmic reticulum in the heart. Trends Cell Biol 19:253–9

    Article  PubMed  CAS  Google Scholar 

  • Milner RE, Michalak M, Wang LC (1991) Altered properties of calsequestrin and the ryanodine receptor in the cardiac sarcoplasmic reticulum of hibernating mammals. Biochim Biophys Acta 1063:120–128

    Article  PubMed  CAS  Google Scholar 

  • Minajeva A, Kaasik A, Paju K, Seppet E, Lompre AM, Veksler V, Ventura-Clapier R (1997) Sarcoplasmic reticulum function in determining atrioventricular contractile differences in rat heart. Am J Physiol 273:2498–507

    Google Scholar 

  • Negretti N, Varro A, Eisner DA (1995) Estimate of net calcium fluxes and sarcoplasmic reticulum calcium content during systole in rat ventricular myocytes. J Physiol 486:581–591

    PubMed  CAS  Google Scholar 

  • Puglisi JL, Yuan WL, Bassani JWM, Bers DM (1999) Ca2+ influx through Ca2+ channels in rabbit ventricular myocytes during action potential clamp: Influence of temperature. Circ Res 85: E7–E16

    Article  PubMed  CAS  Google Scholar 

  • Ravens U, Gath J, Hussaini MA, Himmel H (1997) Mechanical restitution in atrial muscle from human and rat hearts: effects of agents that modify sarcoplasmic reticulum function. Pharmacol Toxicol 81:97–104

    Article  PubMed  CAS  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 145:322–7

    Article  Google Scholar 

  • Rocha ML, Rantin FT, Kalinin AL (2007) Importance of the sarcoplasmic reticulum and adrenergic stimulation on the cardiac contractility of the neotropical teleost Synbranchus marmoratus under different thermal conditions. J Comp Physiol B 177:713–21

    Article  PubMed  CAS  Google Scholar 

  • Rossi AE, Dirksen RT (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle Nerve 33:715–31

    Article  PubMed  CAS  Google Scholar 

  • Rossi D, Barone V, Giacomello E, Cusimano V, Sorrentino V (2008) The sarcoplasmic reticulum: an organized patchwork of specialized domains. Traffic 9:1044–9

    Article  PubMed  CAS  Google Scholar 

  • Santer RM (1974) The organization of the sarcoplasmic reticulum in teleost ventricular myocardial cells. Cell Tissue Res 151:395–402

    Article  PubMed  CAS  Google Scholar 

  • Sedarat F, Lin E, Moore EDW, Tibbits GF (2004) Deconvolution of confocal images of dihydropyridine and ryanodine receptors in developing cardiomyocytes. J Appl Physiol 97: 1098–1103

    Article  PubMed  CAS  Google Scholar 

  • Shannon TR, Guo T, Bers DM (2003) Ca2+ scraps: local depletions of free [Ca2+] in cardiac sarcoplasmic reticulum during contractions leave substantial Ca2+ reserve. Circ Res 93:40–5

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shiels HA, White E (2003) Confocal imaging of Ca 2+ transients and Ca2+ sparks in cardiac myocytes from rainbow trout. J Physiol 551P:PC8

    Google Scholar 

  • Shiels HA, White E (2005) Temporal and spatial properties of cellular Ca2+ flux in trout ventricular myocytes. Am J Physiol 288:R1756–R1766

    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 202:881–90

    PubMed  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2000) Temperature-dependence of L-type Ca2+ channel current in atrial myocytes from rainbow trout. J Exp Biol 203:2771–2780

    PubMed  CAS  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2001) Effect of temperature on Ca2+ cycling in rainbow trout myocytes. Biophysical Journal Annual Meeting Abstracts, 646a

    Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2002a) Effects of temperature on intracellular [Ca2+] in trout atrial myocytes. J Exp Biol 205:3641–3650

    PubMed  CAS  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2002b) Temperature dependence of cardiac sarcoplasmic reticulum function in rainbow trout myocytes. J Exp Biol 205:3631–3639

    PubMed  CAS  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2002c) The force-frequency relationship in fish hearts–a review. Comp Biochem Phsyiol 132:811–826

    Article  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2003) Acute temperature change modulates the response of I Ca to adrenergic stimulation in fish cardiomyocytes. Physiol Biochem Zool 76:816–24

    Article  PubMed  CAS  Google Scholar 

  • Shiels HA, Blank JM, Farrell AP, Block BA (2004) Electrophysiological properties of the L-type Ca2+ current in cardiomyocytes from bluefin tuna and Pacific mackerel. Am J Physiol 286:R659–R668

    CAS  Google Scholar 

  • Shiels HA, Paajanen V, Vornanen M (2006) Sarcolemmal ion currents and sarcoplasmic reticulum Ca2+ content in ventricular myocytes from the cold stenothermic fish, the burbot (Lota lota). J Exp Biol 209:3091–3100

    Article  PubMed  CAS  Google Scholar 

  • Shiels HA, Di Maio A, Thompson S, Block BA (2011) Warm fish with cold hearts: thermal plasticity of excitation-contraction coupling in bluefin tuna. Proc Biol Sci 278:18–27

    Article  PubMed  CAS  Google Scholar 

  • Sitsapesan R, Williams AJ (1994) Regulation of the gating of the sheep cardiac sarcoplasmic reticulum Ca2+-release channel by luminal Ca2+. J Membr Biol 137:215–226

    PubMed  CAS  Google Scholar 

  • Sitsapesan R, Williams AJ (1995) The gating of the sheep skeletal sarcoplasmic reticulum Ca2+-release channel is regulated by luminal Ca2+. J Membr Biol 146:133–144

    PubMed  CAS  Google Scholar 

  • Sitsapesan R, Montgomery RAP, Macleod KT, Williams AJ (1991) Sheep cardiac sarcoplasmic-reticulum calcium-release channels: modification of conductance and gating by temperature. J Physiol 434:469–488

    PubMed  CAS  Google Scholar 

  • Su Z, Li F, Spitzer KW, Yao A, Ritter M, Barry WH (2003) Comparison of sarcoplasmic reticulum Ca2+-ATPase function in human, dog, rabbit, and mouse ventricular myocytes. J Mol Cell Cardiol 35:761–7

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Takagi N, Shigenobu K (1995) Difference in excitation-contraction mechanisms between atrial and ventricular myocardia of hatched chicks. Gen Pharmacol Vasc Syst 26:45–49

    Article  CAS  Google Scholar 

  • Terentyev D, Viatchenko-Karpinski S, Gyorke I, Volpe P, Williams SC, Gyorke S (2003) Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: mechanism for hereditary arrhythmia. Proc Natl Acad Sci USA 100:11759–64

    Article  PubMed  CAS  Google Scholar 

  • Thomas MJ, Hamman BN, Tibbits GF (1996) Dihydropyridine and ryanodine binding in ventricles from rat; trout; dogfish and hagfish. J Exp Biol 199:1999–2009

    PubMed  CAS  Google Scholar 

  • Tibbits GF, Hovemadsen L, Bers DM (1991) Calcium-transport and the regulation of cardiac contractility in teleosts: a comparison with higher vertebrates. Can J Zool 69:2014–2019

    Article  CAS  Google Scholar 

  • Tibbits GF, Xu L, Sedarat F (2002) Ontogeny of excitation-contraction coupling in the mammalian heart. Comp Biochem Physiol A 132:691–698

    Article  Google Scholar 

  • Tiitu V, Vornanen M (2002) Regulation of cardiac contractility in a stenothermal fish, the burbot (Lota lota). J Exp Biol 205:1597–1606

    PubMed  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 173:285–291

    CAS  Google Scholar 

  • Tijskens P, Meissner G, Franzini-Armstrong C (2003) Location of ryanodine and dihydropyridine receptors in frog myocardium. Biophys J 84:1079–1092

    Article  PubMed  CAS  Google Scholar 

  • Vornanen M (1997) Sarcolemmal Ca2+ influx through L-type Ca2+ channels in ventricular myocytes of a teleost fish. Am J physiol 41:R1432–R1440

    Google Scholar 

  • Vornanen M (2005) Temperature and Ca2+ dependence of [3H]ryanodine binding in the burbot (Lota lota L.) heart. Am J Physiol 290:R345–R351

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Walden AP, Dibb KM, Trafford AW (2009) Differences in intracellular calcium homeostasis between atrial and ventricular myocytes. J Mol Cell Cardiol 46:463

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Altimiras J, Klein W, Axelsson M (2003) Ventricular haemodynamics in Python molurus: separation of pulmonary and systemic pressures. J Exp Biol 206:4241–4245

    Article  PubMed  Google Scholar 

  • Webb G, Heatwole H, De Bevay DBJ (1971) Comparative cardiac anatomy of the reptilia. I. The chambers and septa of the varanid ventricle. J Morphol 134:335–50

    Article  PubMed  CAS  Google Scholar 

  • Xue XH, Hryshko LV, Nicoll DA, Philipson KD, Tibbits GF (1999) Cloning, expression, and characterization of the trout cardiac Na+/Ca2+ exchanger. Am J Physiol 277:C693–C700

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Faculty of Medical and Health Sciences, Core Technology Facility, The University of Manchester, 46 Grafton Street, Manchester, M139NT, UK

    Gina L. J. Galli

  2. Faculty of Life Sciences, Core Technology Facility, The University of Manchester, 46 Grafton Street, Manchester, M139NT, UK

    Holly A. Shiels

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  1. Gina L. J. Galli
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Correspondence to Gina L. J. Galli .

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Editors and Affiliations

  1. , Institute of Anatomy, Charles University, U nemocnice 3, Prague, 128 00, Czech Republic

    David Sedmera

  2. Fac. Science, Inst. Biological Sciences Zoofysiology, University of Aarhus, C. F. Moellers Allé, Aarhus C, 8000, Denmark

    Tobias Wang

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Galli, G.L.J., Shiels, H.A. (2012). The Sarcoplasmic Reticulum in the Vertebrate Heart. In: Sedmera, D., Wang, T. (eds) Ontogeny and Phylogeny of the Vertebrate Heart. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3387-3_5

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