Skip to main content

The effects of hydrostatic pressure on signal transduction in brain membranes of deep-sea fishes of the genus Coryphaenoides

Abstract

To investigate the effects of increased hydrostatic pressure on transmembrane signaling in deep-living marine species, the A1 adenosine receptor − inhibitory G protein (Gi) − adenylyl cyclase signaling complex was examined in brain membrane preparations from four teleost fish species of the deep-sea family Macrouridae. The combined depth ranges of the adults of these species, Coryphaenoides armatus, C. cinereus, C. filifer, C. pectoralis, span several hundred meters to 5400 m. Basal adenylyl cyclase activity, determined at 5 °C, was inhibited by increased hydrostatic pressure in all four species. At the highest pressure tested, 476 atm, adenylyl cyclase activity was inhibited 60 to 70% relative to the atmospheric pressure values. Pressure inhibition did not result from denaturation or loss of protein components from the membrane due to pressure-induced shedding. Despite the pressure-inhibition of basal adenylyl cyclase activity, the responsiveness of adenylyl cyclase activity to modulation by N6-cyclopentyladenosine, an A1 adenosine receptor agonist, was retained at elevated pressures. Because the accumulation of the second messenger cAMP depends on the summation of modulatory inputs, these results indicate that the transmembrane signaling in these deep-living species is insensitive to hydrostatic pressure changes.

This is a preview of subscription content, access via your institution.

References

  • Bernhardt, G., Disteche, A., Jaenicke, R., Koch, B., Lüdemann, H.-D. and Stetter, K.-O. 1988. Effect of carbon dioxide and hydrostatic pressure on the pH of culture media and the growth of methanogens at elevated temperature. Appl. Microbiol. Biotechnol. 28: 176-181.

    Google Scholar 

  • Bruns, R.F., Lu, G.H. and Pugsley, T.A. 1986. Characterization of the A2 adenosine receptor labeled by [3H]NECA in rat striatal membranes Mol. Phamacol. 29: 331-346.

    Google Scholar 

  • Casadó, V., Cantí, Mallol, J., Canela, E.I., Lluis, C. and Franco, R. 1990. Solubilization of A1 adenosine receptor from pig brain: Characterization and evidence of the role of the cell membrane on coexistence of high-and low-affinity states. J. Neurosci. Res. 26: 461-473.

    Google Scholar 

  • Casadó, V., Mallol, J., Lluis, C., Canela, E.I. and Franco, R. 1991a. Effect of endogenous phospholipids on the [3H]R-PIA binding to A1 adenosine receptors from pig cerebral cortex. Nucleosides and Nucleotides 10: 1141-1143.

    Google Scholar 

  • Casadó, V., Mallol J., Lluis, C., Canela, E.I. and Franco, R. 1991b. Effect of phospholipases and proteases on the [3H]N6-(R)-phenylisopropyladenosine ([3H]R-PIA) binding to A1 adenosine receptors from pig cerebral cortex. J. Cell. Biochem. 47: 278-288.

    Google Scholar 

  • Casadó, V., Mallol J., Canela, E.I., Franco, R. and Lluis, C. 1992. Modulation of adenosine agonist [3H]N6-(R)-phenylisopropyladenosine binding to pig brain cortical membranes by changes to membrane fluidity and of medium physicochemical characteristics. Eur. J. Pharmacol. Mol. Pharmacol. 225: 7-14.

    Google Scholar 

  • Chong, P.L.-G., Fortes, P.A.G. and Jameson, D.M. 1985. Mechanisms of inhibition of (Na,K)-ATPase by hydrostatic pressure studied with flueorescent probes. J. Biol. Chem. 260: 14484-14490.

    Google Scholar 

  • Deckmann, M. Haimovitz, R. and Shinitzky, M. 1985. Selective release of integral proteins from human erythrocyte membranes by hydrostatic pressure. Biochim. Biophys. Acta 821: 334-340.

    Google Scholar 

  • DeLong, E.F. and Yayanos, A.A. 1987. Properties of the glucose transport system in some deep-sea bacteria. Appl. Environ. Microbiol. 53: 527-532.

    Google Scholar 

  • Gibbs, A. and Somero, G.N. 1989. Pressure adaptation of Na+/K+-ATPase in gills of marine teleosts. J. Exp. Biol. 143: 475-492.

    Google Scholar 

  • Hennessey, J.P., Jr. and Siebenaller, J.F. 1985. Pressure inactivation of tetrameric lactate dehydrogenase homologues of confamilial deep-living fishes. J. Comp. Physiol. 155: 647-652.

    Google Scholar 

  • Houslay, M.D., Dipple, I. and Gordon, D.M. 1981. Phenobarbital selectively modulates the glucagon-stimulated activity of adenylate cyclase by depressing the lipid phase separation occurring in the outer half of the bilayer of liver plasma membranes. Biochem. J. 197: 675-681.

    Google Scholar 

  • Hurley, J.H. 1999. Structure, mechanism, and regulation of mammalian adenylyl cyclase. J. Biol. Chem. 274: 7599-7602.

    Google Scholar 

  • Hubbs, C.L. 1926. The supposed intergradation of two species of Sebastolobus (a genus of scorpaenoid fishes) of western America. Am. Mus. Novitates 216: 1-9.

    Google Scholar 

  • Iwamoto, T. and Stein, D.L. 1974. A systematic review of the rattail fishes (Macrouridae: Gadiformes) from Oregon and adjacent waters. Bulletin of the California Academy of Sciences No. 111, 79 pp.

  • Johnson, R.A. and Salomon, Y. 1991. Assay of adenylyl cyclase catalytic activity. Methods Enzymol. 195: 3-21.

    Google Scholar 

  • Johnson, R.A. and Shoshani, I. 1990. Kinetics of 'P'-site mediated inhibition of adenylyl cyclase and the requirements for substrate. J. Biol. Chem. 265: 11595-11600.

    Google Scholar 

  • Lauth, R. R., Wilkins, M.E. and Ramore, P.A., Jr. 1997. Results of trawl surveys of groundfish resources of the West Coast upper continental slope from 1989 to 1993. U.S. Department of Commerce, NOAA Technical Memorandum NMFS-AFSC-79, 342 pp.

  • Lester, D.S. 1989. High-pressure extraction of membrane-associated protein kinase C from rat brain. J. Neurochem. 52: 1950-1953.

    Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.

    Google Scholar 

  • Marshall, N.B. 1965. Systematic and biological studies of the Macrourid fishes (Anacanthini-teleosteii). Deep-Sea Res. 299-322.

  • Marshall, N.B. 1973. Family Macrouridae. Memoir, Sears Foundation for Marine Research 1, Fishes of the western North Atlantic 6: 496-537.

    Google Scholar 

  • Muller, C.P. and Shinitzky, M. 1981. Passive shedding of erythrocyte antigens induced by membrane rigidification. Expl. Cell Res. 136: 53-62.

    Google Scholar 

  • Murray, T.F. and J.F. Siebenaller. 1987. Comparison of the binding properties of A1 adenosine receptors in brain membranes of two congeneric marine fishes living at different depths. J. Comp. Physiol. B 157: 267-277.

    Google Scholar 

  • Murray, T.F. and J.F. Siebenaller. 1993. Differential susceptibility of guanine nucleotide-binding proteins to pertussis toxin-catalyzed ADP-ribosylation in brain membranes of two congeneric marine fishes. Biol. Bull. 185: 346-354.

    Google Scholar 

  • Orr, J.W., Brown, M.A. and Baker, D.C. 1998. Guide to rockfishes (Scorpaenidae) of the genera Sebastes, Sebastolobus, and Adelosebastes of the Northeast Pacific Ocean. U.S. Department of Commerce, NOAA Technical Memorandum NMFS-AFSC-95, 46 pp.

  • Pearcy, W.G., Stein, D.L. and Carney, R.S. 1982. The deep-sea benthic fish fauna of the northeastern Pacific Ocean on Cascadia and Tufts Abyssal Plains and adjoining continental slopes. Biol. Oceanography 1: 375-428.

    Google Scholar 

  • Precht, H. 1958. Concepts of the temperature adaptation of unchanging reaction systems of cold-blooded animals. In: Physiological Adaptation, pp. 351-376. Edited by C.L. Prosser. American Association for the Advancement of Science, Washington, D.C.

    Google Scholar 

  • Rivkees, S.A., Barbhaiya, H. and IJzerman, A.P. 1999. Identification of the adenine binding site of the human A1 adenosine receptor. J. Biol. Chem. 274: 3617-3621.

    Google Scholar 

  • Salomon, Y., Londos, C. and Rodbell, M. 1974. A highly sensitive adenylate cyclase assay. Analyt. Biochem. 58: 521-548.

    Google Scholar 

  • Saunders, P.M. and Fofonoff, N.P. 1976. Conversion of pressure to depth in the ocean. Deep-Sea Res. 23: 109-111.

    Google Scholar 

  • Siebenaller, J.F. 1987. Pressure adaptations in deep-sea animals. In: Current Perspectives in High Pressure Biology. pp. 33-48. Edited by H.W. Jannasch, A.M. Zimmerman and R.E. Marquis. Academic, London.

    Google Scholar 

  • Siebenaller, J.F. 1991. Pressure as an environmental variable: magnitude and mechanisms of perturbation. In: Biochemistry and Molecular Biology of Fishes. Vol. 1, pp. 323-343. Edited by P.W. Hochachka and T.P. Mommsen Elsevier, Amsterdam.

    Google Scholar 

  • Siebenaller, J.F. and Murray, T.F. 1990. A1 adenosine receptor modulation of adenylyl cyclase of a deep-living teleost fish, Antimora rostrata. Biol. Bull. 178: 65-73.

    Google Scholar 

  • Siebenaller, J.F. and Murray, T.F. 1994a. The effects of hydrostatic pressure on the low-Km GTPase in brain membranes from two congeneric marine fishes. J. Comp. Physiol. B 163: 626-632.

    Google Scholar 

  • Siebenaller, J.F. and Murray, T.F. 1994b. The effects of hydrostatic pressure on pertussis toxin-catalyzed ribosylation of guanine nucleotide-binding proteins from two congeneric marine fishes. Comp. Biochem. Physiol. 108B: 423-430.

    Google Scholar 

  • Siebenaller, J.F. and Murray, T.F. 1994c. Membrane preparation and receptor assays-adenosine. In: Biochemistry and Molecular Biology of Fishes. Vol. 3; pp. 475-484. Edited by P.W. Hochachka and T.P. Mommsen. Elsevier Press, Amsterdam.

    Google Scholar 

  • Siebenaller, J.F. and Murray, T.F. 1995. The effects of pressure on G protein-coupled signal transduction. In: Biochemistry and Molecular Biology of Fishes. Vol. 5, pp. 147-174. Edited by P.W. Hochachka and T.P. Mommsen, Elsevier, Amsterdam.

    Google Scholar 

  • Siebenaller, J.F. and Murray, T.F. 1999. Hydrostatic pressure alters the time course of GTP[S] binding to G proteins in brain membranes from two congeneric marine fishes. Biol. Bull. 197: 388-394.

    Google Scholar 

  • Siebenaller, J.F. and Somero, G.N. 1978. Pressure adaptive differences in lactate dehydrogenases of congeneric fishes living at different depths. Science 201: 255-257.

    Google Scholar 

  • Siebenaller, J.F. and Somero, G.N. 1989. Biochemical adaptation to the deep sea. CRC Rev. Aquatic Sci. 1: 1-25.

    Google Scholar 

  • Siebenaller, J.F. and Somero, G.N. and Haedrich, R.L. 1982. Biochemical characteristics of macrourid fishes differing in their depths of distribution. Biol. Bull. 163: 240-249.

    Google Scholar 

  • Siebenaller, J.F., Hagar, A.F. and Murray, T.F. 1991. The effects of hydrostatic pressure on A1 adenosine receptor signal transduction in brain membranes of two congeneric marine fishes. J. Exp. Biol. 159: 23-43.

    Google Scholar 

  • Sokal, R.R. and Rohlf, F.J. 1995. Biometry. Third edition. W.H. Freeman and Co., New York.

    Google Scholar 

  • Stevens, C.K. and Siebenaller, J.F. 2000. The effects of hydrostatic pressure on pertussis toxin-catalyzed ribosylation of G proteins from deep-living macrourid fishes. Comp. Biochem. Physiol. B125: 103-114.

    Google Scholar 

  • Wakefield, W.W. and Smith, K.L., Jr. 1990. Ontogenetic vertical migration in Sebastolobus altivelis as a mechanism for transport of particulate organic matter at continental slope depths. Limnol. Oceanog. 35: 1314-1328.

    Google Scholar 

  • Williams, M. Braunwalder, A. and Erickson, T.E. 1986. Evaluation of the binding of the A-1 selective adenosine radioligand, cyclopentyladenosine (CPA), to rate brain tissue. Naunyn-Schmiedeberg's Arch. Pharmacol. 332: 179-183.

    Google Scholar 

  • Wilson, R.R., Jr., Siebenaller, J.F. and Davis, B.J. 1991. Phylogenetic analysis of species of three subgenera of Coryphaenoides (Teleostei:Macrouridae) by peptide mapping of homologs of LDH-A4. Biochem. Syst. Ecol. 19: 277-287.

    Google Scholar 

  • Zobell, C.E. and Oppenheimer, C.H. 1950. Some effects of hydrostatic pressure on the multiplication and morphology of marine bacteria. J. Bacteriol. 60: 771-778.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Siebenaller, J. The effects of hydrostatic pressure on signal transduction in brain membranes of deep-sea fishes of the genus Coryphaenoides. Fish Physiology and Biochemistry 23, 99–106 (2000). https://doi.org/10.1023/A:1007830722804

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1007830722804

  • A1 adenosine receptor
  • adenosine
  • adenylyl cyclase
  • cAMP
  • Coryphaenoides armatus
  • Coryphaenoides cinereus
  • Coryphaenoides filifer
  • Coryphaenoides pectoralis
  • inhibitory G protein
  • Macrouridae