Journal of Comparative Physiology B

, Volume 187, Issue 2, pp 291–313 | Cite as

Characterization of the functional and anatomical differences in the atrial and ventricular myocardium from three species of elasmobranch fishes: smooth dogfish (Mustelus canis), sandbar shark (Carcharhinus plumbeus), and clearnose skate (Raja eglanteria)

  • Julie Larsen
  • Peter Bushnell
  • John Steffensen
  • Morten Pedersen
  • Klaus Qvortrup
  • Richard Brill
Original Paper

Abstract

We assessed the functional properties in atrial and ventricular myocardium (using isolated cardiac strips) of smooth dogfish (Mustelus canis), clearnose skate (Raja eglanteria), and sandbar shark (Carcharhinus plumbeus) by blocking Ca2+ release from the sarcoplasmic reticulum (SR) with ryanodine and thapsigargin and measuring the resultant changes in contraction–relaxation parameters and the force–frequency relationship at 20 °C and 30 °C. We also examined ultrastructural differences with electron microscopy. In tissues from smooth dogfish, net force (per cross-sectional area) and measures of the speeds of contraction and relaxation were all higher in atrial than ventricular myocardium at both temperatures. Atrial-ventricular differences were evident in the other two species primarily in measures of the rates of contraction and relaxation. Ryanodine-thapsigargin treatment reduced net force and its maximum positive first derivative (i.e., contractility), and increased time to 50 % relaxation in atrial tissue from smooth dogfish at 30 °C. It also increased times to peak force and half relaxation in clearnose skate atrial and ventricular tissue at both temperatures, but only in atrial tissue from sandbar shark at 30 °C; indicating that SR involvement in excitation–contraction (EC) coupling is species- and temperature-specific in elasmobranch fishes, as it is in teleost fishes. Atrial and ventricular myocardium from all three species displayed a negative force–frequency relationship, but there was no evidence that SR involvement in EC coupling was influenced by heart rate. SR was evident in electron micrographs, generally located in proximity to mitochondria and intercalated discs, and to a lesser extent between the myofibrils; with mitochondria being more numerous in ventricular than atrial myocardium in all three species.

Keywords

Atria Cardiac Force–frequency Heart Temperature Ventricle 

Abbreviations

CICR

Ca2+-induced Ca2+-release

+dF/dtmax

Maximum rate of force development (mN mm−2 s−1)

−dF/dtmin

Maximum rate of relaxation (mN mm−2 s−1)

DMSO

Dimethyl sulfoxide

EC

Excitation–contraction

ECG

Electrocardiogram

G

Glycogen storage granules

h

Hours

Hz

Hertz

ICD

Intercalated discs

kHz

Kilohertz

M

Mitochondria

min

Minutes

mm

Millimeter

mN

MilliNewtons

ms

Millisecond

MHC

Myosin heavy chains

NCX

Na+–Ca2+ exchanger

nm

Nanometers

P

Probability

s

Seconds

SL

Sarcolemma

SERCA

SR Ca2+-ATPase

SR

Sarcoplasmic reticulum

Z

Z-line

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Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2016

Authors and Affiliations

  • Julie Larsen
    • 1
  • Peter Bushnell
    • 2
  • John Steffensen
    • 1
  • Morten Pedersen
    • 3
  • Klaus Qvortrup
    • 4
  • Richard Brill
    • 5
    • 6
  1. 1.Marine Biological SectionUniversity of CopenhagenHelsingørDenmark
  2. 2.Department of BiologyIndiana University South BendSouth BendUSA
  3. 3.Department of Science and EnvironmentRoskilde UniversityRoskildeDenmark
  4. 4.Department of Biomedical Sciences/CFIMUniversity of CopenhagenCopenhagenDenmark
  5. 5.Behavioral Ecology Branch, Ecosystems Processes DivisionNortheast Fisheries Science Center, National Marine Fisheries Service, NOAASandy HookUSA
  6. 6.Virginia Institute of Marine ScienceGloucester PointUSA

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