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Fish Physiology and Biochemistry

, Volume 40, Issue 1, pp 67–73 | Cite as

Hypoxia increases the release of salmon cardiac peptide (sCP) from the heart of rainbow trout (Oncorhynchus mykiss) under constant mechanical load in vitro

  • Olli Arjamaa
  • Olli Vuolteenaho
  • Elina Kivi
  • Mikko Nikinmaa
Article

Abstract

Our aim was to study the effects of hypoxia on the release of salmon cardiac peptide (sCP) from an isolated heart ventricle of trout during a constant mechanical load. Trout heart ventricles were studied in vitro. The ventricle was placed in an organ bath at 12 °C in which a constant mechanical load could be imposed on the ventricle while buffer solution was circulating. Ventricles were field-stimulated with a supramaximal voltage pulse at a rate of about 0.3 s−1. Samples of 1 ml were collected at an interval of 10 min for 200 min from the organ bath and assessed with a radioimmunoassay for sCP. After a control period of 20 min, ventricles were exposed to hypoxia produced with N2 gassing (n = 9) or to hypoxia with 20 mM BDM, a nonselective myosin ATPase inhibitor locking cross-bridges in a pre-power-stroke state inhibiting force production with normal electrical activity (n = 10). In this model and setup, hypoxia stimulated the release of sCP, but the interindividual variation in the response was large. At the end of hypoxia exposure, the concentration of sCP in the organ bath was about sixfold higher than at the start of the exposure (P < 0.05, one-way ANOVA for repeated measurements, followed by Dunnett’s multiple comparison test). When BDM was introduced into the bath, the ventricle still secreted sCP but the hypoxic response was smaller than in the experiments without BDM. In the trout heart ventricle, there is a hypoxia-sensitive component in the release mechanism of sCP which is independent of contraction.

Keywords

Trout heart hypoxia salmon cardiac peptide sCP 2,3-butanedione monoxime BDM 

Notes

Acknowledgments

The authors gratefully acknowledge the technical assistance Ms Tuula Lumijärvi.

Conflict of interest

None.

References

  1. Arjamaa O, Nikinmaa M (2009) Natriuretic peptides in hormonal regulation of hypoxia responses. Am J Physiol 296:R257–R264Google Scholar
  2. Arjamaa O, Nikinmaa M (2011) Hypoxia regulates the natriuretic peptide system. Int J Physiol Pathophysiol Pharmacol 3:191–201PubMedCentralPubMedGoogle Scholar
  3. Arjamaa O, Sormunen R, Lehto V-P, Vuolteenaho O (2000) Localization of salmon cardiac peptide (sCP) in the heart of salmon (Salmo salar L.). Gen Comp Endocrinol 120:276–282PubMedCrossRefGoogle Scholar
  4. Baertschi AJ, Hausmaninger C, Walsh RS, Mentzer RM Jr, Wyatt DA, Pence RA (1986) Hypoxia-induced release of atrial natriuretic factor (ANF) from the isolated rat and rabbit heart. Biochem Biophys Res Commun 140:427–433PubMedCrossRefGoogle Scholar
  5. Blanchard EM, Smith GL, Allen DG, Alpert NR (1990) The effects of 2,3-butanedione monoxime on initial heat, tension, and aequorin light output of ferret papillary muscles. Pflugers Arch 416:219–221PubMedCrossRefGoogle Scholar
  6. Chen YF (2005) Atrial natriuretic peptide in hypoxia. Peptides 26:1068–1077PubMedCrossRefGoogle Scholar
  7. Chen YF, Durand J, Claycomb WC (1997) Hypoxia stimulates atrial natriuretic peptide gene expression in cultured atrial cardiocytes. Hypertension 29:75–82PubMedCrossRefGoogle Scholar
  8. Chun YC, Hyun JY, Kwak YG, Kim CH, Choi E, Kim MS, Park JW (2003) Hypoxic activation of the atrial natriuretic peptide gene promoter through direct and indirect actions of hypoxia-inducible factor-1. Biochem J 370:149–157PubMedCrossRefGoogle Scholar
  9. Dietz JR (1984) Release of natriuretic factor from rat heart-lung preparation by atrial distension. Am J Physiol 247:R1093–R1096PubMedGoogle Scholar
  10. Focaccio A, Ambrosio G, Enea I, Russo R, Balestrieri P, Chiariello M, Volpe M (1995) Influence of O2 deprivation, reduced flow, and temperature on release of ANP from rabbit hearts. Am J Physiol 268:H2352–H2357PubMedGoogle Scholar
  11. Goetze JP, Gore A, Moller CH, Steinbruchel DA, Rehfeld JF, Nielsen LB (2004) Acute myocardial hypoxia increases BNP gene expression. FASEB 15:1928–1930Google Scholar
  12. Greenwood FC, Hunter WM, Glover JS (1963) The preparation of I131-labelled human growth hormone of high specific radioactivity. Biochem J 89:114–123PubMedGoogle Scholar
  13. Klinger JR, Pietras L, Warburton R, Hill NS (2001) Reduced oxygen tension increases atrial natriuretic peptide release from atrial cardiocytes. Exp Biol Med 226:847–853Google Scholar
  14. Kokkonen K, Vierimaa H, Bergström S, Tervonen V, Arjamaa O, Ruskoaho H, Järvilehto M, Vuolteenaho O (2000) Novel salmon cardiac peptide hormone is released from the ventricle by regulated secretory pathway. Am J Physiol 278:E285–E292Google Scholar
  15. Laine M, Weckström M, Vuolteenaho O, Arjamaa O (1994) Effect of ryanodine on atrial natriuretic peptide secretion by contracting and quiescent rat atrium. Pfluegers Arch 426:276–283CrossRefGoogle Scholar
  16. Lang RE, Tholken H, Ganten D, Luft FC, Ruskoaho H, Unger T (1985) Atrial natriuretic factor—a circulating hormone stimulated by volume loading. Nature 314:264–266PubMedCrossRefGoogle Scholar
  17. Laurent P, Holmgren S, Nilsson S (1983) Nervous and humoral control of the fish heart: structure and function. Comp Biochem Physiol 76A:525–542CrossRefGoogle Scholar
  18. Lew RA, Baertschi AJ (1989) Mechanisms of hypoxia-induced atrial natriuretic factor release from rat hearts. Am J Physiol 257:H147–H156PubMedGoogle Scholar
  19. Ljusegren ME, Andersson RG (1994) Hypoxia induces release of atrial natriuretic peptide in rat atrial tissue: a role for this peptide during low oxygen stress. Naunyn Schmiedebergs Arch Pharmacol 350:189–193PubMedCrossRefGoogle Scholar
  20. Majalahti-Palviainen T, Hirvinen M, Tervonen V, Ilves M, Ruskoaho H, Vuolteenaho O (2000) Gene structure of a new cardiac peptide hormone: a model for heart-specific gene expression. Endocrinology 141:731–740PubMedGoogle Scholar
  21. Pfeifer M, Wolf K, Blumberg FC, Elsner D, Muders F, Holmer SR, Riegger GA, Kurtz A (1997) ANP gene expression in rat hearts during hypoxia. Pflugers Arch 434:63–69PubMedCrossRefGoogle Scholar
  22. Renkin EM, Tucker VL (1996) Atrial natriuretic peptide as a regulator of transvascular fluid balance. News Physiol Sci 11:138–143Google Scholar
  23. Skvorak JP, Sutton ET, Rao PS, Dietz JR (1996) Mechanism of anoxia-induced atrial natriuretic peptide release in the isolated rat atria. Am J Physiol 271:R237–R243PubMedGoogle Scholar
  24. Sun JZ, Chen SJ, Li G, Chen YF (2000) Hypoxia reduces atrial natriuretic clearance receptor gene expression in ANP knockout mice. Am J Physiol 279:L511–L519Google Scholar
  25. Takei Y (2000) Structural and functional evolution of the natriuretic peptide system in vertebrates. Int Rev Cytol 194:1–66PubMedCrossRefGoogle Scholar
  26. Tervonen V (2001) Salmon cardiac peptide (sCP): a new model for natriuretic peptide biology. PhD thesis, Acta University Ouluensis D 646:1–106Google Scholar
  27. Tervonen V, Arjamaa O, Kokkonen K, Ruskoaho H, Vuolteenaho O (1998) A novel cardiac hormone related to A-, B- and C-type natriuretic peptides. Endocrinology 139:4021–4025PubMedGoogle Scholar
  28. Tervonen V, Ruskoaho H, Vuolteenaho O (2000) Novel cardiac hormone in several teleosts. J Endocrinol 166:407–418PubMedCrossRefGoogle Scholar
  29. Tervonen V, Kokkonen K, Vierimaa H, Ruskoaho H, Vuolteenaho O (2001) Temperature has a major influence on cardiac natriuretic peptide in salmon. J Physiol 536:199–209PubMedCrossRefGoogle Scholar
  30. Tervonen V, Ruskoaho H, Lecklin T, Ilves M, Vuolteenaho O (2002) Salmon cardiac natriuretic peptide is a volume-regulating hormone. Am J Physiol 283:E353–E361Google Scholar
  31. Tervonen V, Vuolteenaho O, Nikinmaa M (2006) Haemoconcentration via diuresis in short-term hypoxia: a possible role for cardiac natriuretic peptide in rainbow trout. Comp Biochem Physiol A Mol Integr Physiol 144:86–92PubMedCrossRefGoogle Scholar
  32. Toth M, Vuorinen KH, Vuolteenaho O, Hassinen IE, Uusimaa PA, Leppäluoto J, Ruskoaho H (1994) Hypoxia stimulates release of ANP and BNP from perfused rat ventricular myocardium. Am J Physiol 266:H1572–H1580PubMedGoogle Scholar
  33. Uusimaa P, Peuhkurinen KJ, Hassinen IE, Vuolteenaho O, Ruskoaho O (1992) Ischemia stimulates the release of atrial natriuretic peptide from rat cardiac ventricular myocardium in vitro. Life Sci 50:365–373PubMedCrossRefGoogle Scholar
  34. Vierimaa H, Hirvinen M, Tervonen V, Arjamaa O, Ruskoaho H, Vuolteenaho O (2002) Pronatriuretic peptide is a sensitive marker of endocrine function of teleost heart. Am J Physiol 282:E843–E850Google Scholar
  35. Vierimaa H, Ronkainen J, Ruskoaho H, Vuolteenaho O (2006) Synergistic activation of salmon cardiac function by endothelin and beta-adrenergic stimulation. Am J Physiol 291:H1360–H1370Google Scholar
  36. Vuolteenaho O, Koistinen P, Martikkala V, Takala T, Leppäluoto J (1992) Effects of physical exercise in hypobaric conditions on atrial natriuretic peptide secretion. Am J Physiol 263:R647–R652PubMedGoogle Scholar
  37. Weidemann A, Klanke B, Wagner M, Volk T, Willam C, Wiesener MS, Eckardt KU, Warnecke U (2008) Hypoxia, via stimulation of the hypoxia-inducible factor HIF-1alpha, is a direct and sufficient stimulus for brain-type natriuretic peptide induction. Biochem J 409:233–242PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Olli Arjamaa
    • 1
  • Olli Vuolteenaho
    • 2
  • Elina Kivi
    • 1
  • Mikko Nikinmaa
    • 1
  1. 1.Department of Biology, Laboratory of Animal PhysiologyUniversity of TurkuTurkuFinland
  2. 2.Department of Physiology, Biocenter OuluUniversity of OuluOuluFinland

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