Skip to main content
SpringerLink
Log in

Activity of Energy Metabolism Enzymes and the Adenylate System in Heart Chambers of a Black Sea Scorpionfish (Scorpaena porcus L.) under Acute Hypoxia

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

The fish heart is a unique model to compare the resistance to hypoxia of its two chambers (atrium and ventricle), which are different in the structure and functional loads. The activity of oxydoreductases malate dehydrogenase (MDH, 1.1.1.37) and lactate dehydrogenase (LDH, 1.1.1.27), as well as the parameters of the adenylate system in the heart chambers of a Black Sea scorpaena, were studied under acute hypoxia (0.9–1.2 mg O2·L–1, 90 min). Despite the leading functional role of the ventricle, MDH activity in this heart compartment tended to decrease compared to the atrium in the absence of differences in LDH activity. At the same time, the difference in the level of adenylates (ATP, ADP, AMP), total adenylate pool (AP), and adenylate energy charge (AEС) between the atrium and ventricle was statistically nonsignificant, although the absolute value of the ventricular AP was almost twice as large as the atrial AP. The AEC values of the atrium and ventricle perfused only with venous blood did not exceed ~0.7 (vs. the maximum of this parameter ~0.9–1.0), apparently reflecting the energy status of tissues initially adapted to hypoxia. Under acute hypoxia, there were found two strategies for energy metabolism transformation in the heart chambers in the form of a 2.4-fold drop in MDH activity (р < 0.05) in the atrium and a 2.2-fold increment in LDH activity (р < 0.05) in the ventricle. Probably, the decline in MDH activity in the atrial tissue was determined by a more passive function of this heart chamber in providing the blood flow. The exposure to acute hypoxia led to a decrease in the level of adenylate nucleotides and an AEC decline in the heart chambers, as pronounced most distinctly in the ventricular myocardium. When decreasing PO2, the AEC in the heart chambers shifted within quite a narrow range (from 0.7 to 0.6), indicating the retention of a certain stationary energy status achieved by inhibition of ATP consumption or demand. The putative mechanism for retaining the AEC may be based on the negative chronotropic effect of hypoxia.

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

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Driedzic WR (1992) Cardiac energy metabolism. Fish Physiology 12:219–266. https://doi.org/10.1016/S1546-5098(08)60335-0.

    Article  CAS  Google Scholar 

  2. Hochachka PW, Somero GN (2002) Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, Oxford. 356 pp.

    Google Scholar 

  3. Volosovets AP (2012) Optimization of astenia pharmacotherapy in the practice of modern pediatrics. The pediatrician practice. 2: 23–28 (in Russ.)

    Google Scholar 

  4. Soldatov AA, Golovina IV, Kolesnikova EE, Sysoeva IV, Sysoev AA, Kukhareva TA, Kladchenko ES (2020) Activity of Energy Metabolism Enzymes and ATP Content in the Brain and Gills of the Black Sea Scorpionfish Scorpaena porcus under Short-Term Hypoxia. J Evol Biochem Physiol 56(3):224–234. https://doi.org/10.31857/S0044452920010143

    Article  CAS  Google Scholar 

  5. Kolesnikova EE, Golovina IV (2020) Oxidoreductase Activities in Oxyphilic Tissues of the Black Sea Ruff Scorpaena porcus under Short-term Hydrogen Sulfide Loading. J Evol Biochem Physiol 56(5):459–470. https://doi.org/10.1134/S0022093020050099

    Article  CAS  Google Scholar 

  6. Yamauchi A (1980) Fine Structure of Fish Heart. In: Bourne GH (eds). The Hearts and Heart-like Organs. Academic Press, New York. 119–148.

    Google Scholar 

  7. Grimes AC, Kirby ML (2009) The outflow tract of the heart in fishes: anatomy, genes and evolution. Fish Biol 74(5):983-1036. https://doi.org/10.1111/j.1095-8649.2008.02125.x

    Article  CAS  Google Scholar 

  8. Garofalo F, Imbrogno S, Tota B, Amelio D (2012) Morpho-functional characterization of the goldfish (Carassius auratus L.) heart. Comp Biochem Physiol 163(2):215-22. https://doi.org/10.1016/j.cbpa.2012.05.206

    Article  CAS  Google Scholar 

  9. Holm-Hansen O, Booth CR (1966) The measurement of adenosine triphosphate in the Ocean and its ecological significance. Limnol Oceanogr 11(4):510–519. https://doi.org/10.4319/lo.1966.11.4.0510

    Article  CAS  Google Scholar 

  10. Atkinson DE (1968) The energy charge of the adenylate pools as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7(11):4030–4034. https://doi.org/10.1021/bi00851a033

    Article  CAS  PubMed  Google Scholar 

  11. Ostadal B (2014) Hypoxia and the heart of poikilotherms. Curr Res Cardiol 1(1):28-32.

    Google Scholar 

  12. Farrell AP, Jones DR (1992) The heart. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish Physiology. vol. XIIA. Academic Press, San Diego. 1–73.

    Google Scholar 

  13. Tota B, Cerra MC, Gattuso A (2010) Catecholamines, cardiac natriuretic peptides and chromogranin A: evolution and physiopathology of a ‘whip-brake’ system of the endocrine heart. J Exp Biol 213:3081-3103. https://doi.org/10.1242/jeb.027391

    Article  CAS  PubMed  Google Scholar 

  14. Tota B, Cimini V, Salvatore G, Zummo G (1983) Comparative study of the arterial and lacunary systems of the ventricular myocardium of elasmobranchs and teleost fishes. Am J Anat 167(1):15–32. https://doi.org/10.1002/aja.1001670103

    Article  CAS  PubMed  Google Scholar 

  15. Childress JJ, Somero GN (1979) Depth-Related Enzymic Activities in Muscle, Brain and Heart of Deep-Living Pelagic Marine Teleosts. Mar Biol 52:273–283.

    Article  CAS  Google Scholar 

  16. Eddy FB (1974) Blood gases of the tench (Tinca tinca) in well aerated and oxygen-deficient waters. J Exp Biol 60:71–83.

    Article  Google Scholar 

  17. Tessadori F, van Weerd JH, Burkhard SB, Verkerk AO, de Pater E, Boukens BJ, Vink A, Christoffels VM, Bakkers J (2012) Identification and functional characterization of cardiac pacemaker cells in zebrafish. PLoS One 7(10): e47644. https://doi.org/10.1371/journal.pone.0047644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Almeida-Val VMF, Hochachka PW (1995) Air-breathing fishes: metabolic biochemistry of the first diving vertebrates. Biochemistry and Molecular Biology of Fishes 5:45–55. https://doi.org/10.1016/S1873-0140(06)80029-9

    Article  CAS  Google Scholar 

  19. Ewart HS, Driedzic WR (1987) Enzymes of energy metabolism in salmonid hearts: spongy versus cortical myocardia. Can J Zool 65(3):623–627. https://doi.org/10.1139/z87-097

    Article  CAS  Google Scholar 

  20. Filho DW (2007) Reactive Oxygen Species, Antioxidants and Fish Mitochondria. Front Biosci 12:1229–37. https://doi.org/10.2741/2141

    Article  Google Scholar 

  21. Bailey JR, Sephton DH, Driedzic WR (1990) Oxygen uptake by isolated perfused fish hearts with differing myoglobin concentrations under hypoxic conditions. J Mol Cell Cardiol 22(10):1125–34. https://doi.org/10.1016/0022-2828(90)90076-e

    Article  CAS  PubMed  Google Scholar 

  22. Bailey JR, Driedzic WR (1988) Perfusion-independent oxygen extraction in myoglobin-rich hearts. J Exp Biol 135(1):301–315.

    Article  CAS  Google Scholar 

  23. Lyzlova SN, Panteleeva NS, Yuzhakova GA (1967) Biochemical topography of adenine nucleotides in the heart. Ukrainian Biochem J 39(2):156–161 (in Russ.)

    CAS  Google Scholar 

  24. Love RM (1976) Chemical Biology of Fish. Food industry, Moscow. 349pp. (in Russ.)

    Google Scholar 

  25. Christensen M, Hartmund T, Gesser H (1994) Creatine kinase, energyrich phosphates and energy metabolism in heart muscle of different vertebrates. J Comp Physiol 164:118-23. https://doi.org/10.1007/bf00301652

    Article  CAS  Google Scholar 

  26. Kumar A, Gopesh A (2015) Effect of Hypoxia and Energy Conservation Strategies in the Air-Breathing Indian Catfish, Clarias batrachus. Natl Acad Sci Lett 38(2):135–137. https://doi.org/10.1007/s40009-014-0332-6

    Article  CAS  Google Scholar 

  27. Chippari-Gomes AR, Gomes LC, Lopes NP, Val AL, Almeida-Val VMF (2005) Metabolic adjustments in two Amazonian cichlids exposed to hypoxia and anoxia. Comp Biochem Physiol 141:347–355. https://doi.org/10.1016/j.cbpc.2005.04.006

    Article  CAS  Google Scholar 

  28. Hochachka PW, Somero GN (1984) Biochemical Adaptation. Princeton Univ Press, New Jersey, 560 pp.

    Book  Google Scholar 

  29. Sollid J, Nilsson GE (2006) Plasticity of respiratory structures—adaptive remodeling of fish gills induced by ambient oxygen and temperature. Resp Physiol Neurobiol 154:241-251. https://doi.org/10.1016/j.resp.2006.02.006

    Article  CAS  Google Scholar 

  30. Farrell AP (2007) Tribute to P.L. Lutz: A Message From the Heart—Why Hypoxic Bradycardia in Fishes? J Exp Biol 210(Pt 10):1715–25. https://doi.org/10.1242/jeb.0278

    Article  CAS  PubMed  Google Scholar 

  31. Zverev AA, Anikina TA, Iskakov NG, Leonov NV, Zefirov TL (2018) ATF inhibits spontaneous atrial contraction in rats. Scientific notes of Kazan University 160(4):558–567 (in Russ.)

    CAS  Google Scholar 

  32. Rostovtseva TK, Bezrukov SM (1998) ATP transport through a single mitochondrial channel, VDAC, studied by current fluctuation analysis. Biophys J 74:2365–2373. https://doi.org/10.1016/S0006-3495(98)77945-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kawano S, Kuruma A, Hirayama Y, Hiraoka M (1999) Anion permeability and conduction of adenine nucleotides through a chloride channel in cardiac sarcoplasmic reticulum. J Biol Chem 274:2085–2092. https://doi.org/10.1074/jbc.274.4.2085

    Article  CAS  PubMed  Google Scholar 

  34. Anikina TA, Bilalova GA, Zverev AA, Sitdikov FG (2007) Effect of ATP and its analogs on contractility of rat myocardium during ontogeny. Bull Exp Biol Med 144(1):4–7. https://doi.org/10.1007/s10517-007-0239-z

    Article  CAS  PubMed  Google Scholar 

  35. Gessi S, Merighi S, Varani K, Borea PA (2011) Adenosine receptors in health and disease. Adv Pharmacol 61:41–75. https://doi.org/10.1016/B978-0-12-385526-8.00002-3

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was implemented within a governmental assignment No. 0556-2021-0003 to the A.O. Kovalevsky Institute of Biology of the Southern Seas, and supported by the Russian Foundation for Basic Research grant No. 20-44-920001.

Author information

Authors and Affiliations

  1. A.O. Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences, Sevastopol, Russia

    E. E. Kolesnikova, А. А. Soldatov, I. V. Golovina, I. V. Sysoeva, А. А. Sysoev & Т. А. Kukhareva

Authors
  1. E. E. Kolesnikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. А. А. Soldatov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. V. Golovina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. V. Sysoeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. А. А. Sysoev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Т. А. Kukhareva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.E.K.: task setting, preparation of fish heart chambers, writing and editing the manuscript; A.A.S.: pivotal idea, task setting, experimental design, writing and editing the manuscript; I.V.G.: assaying enzyme activities, statistical data processing, preparing illustrations, writing and editing the manuscript; I.V.S. and A.A.S.: assaying adenyl nucleotides, statistical data processing; T.A.K.: participation in experiments.

Corresponding author

Correspondence to E. E. Kolesnikova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

All applicable international, national and institutional principles of handling and using experimental animals for scientific purposes were observed.

This study did not involve human subjects as research objects.

CONFLICT OF INTEREST

The authors declare that they have neither evident nor potential conflict of interest related to the publication of this article.

Additional information

Translated by A. Polyanovsky

Russian Text © The Author(s), 2021, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2021, Vol. 57, No. 5, pp. 420–429https://doi.org/10.31857/S0044452921050089.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolesnikova, E.E., Soldatov, А.А., Golovina, I.V. et al. Activity of Energy Metabolism Enzymes and the Adenylate System in Heart Chambers of a Black Sea Scorpionfish (Scorpaena porcus L.) under Acute Hypoxia. J Evol Biochem Phys 57, 1050–1059 (2021). https://doi.org/10.1134/S0022093021050070

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093021050070

Keywords:

Search

Navigation