Organic Osmotic Effectors in Cartilaginous Fishes

  • P. H. Yancey
Part of the Proceedings in Life Sciences book series (LIFE SCIENCES)

Abstract

The osmoregulatory system of the elasmobranchs (cartilaginous fishes) has often been regarded as a physiological oddity. As far back as 1858, the muscles of sharks were found to contain the waste product urea at concentrations a 100-fold those of other animals; and in 1909 unusually high levels of the methylamine compounds betaine and trimethylamine oxide (TMAO) were discovered in muscle also. In the early 1900’s, Frédericq, Hoppe-Seyler, H. Smith, and others demonstrated that these compounds form the basis of an osmoregulatory system that appears to differ greatly from those of the rest of the animal kingdom (reviewed by Smith 1936). Figure 1 shows some relatively recent analyses of extracellular (E) and intracellular muscle (I) fluids of two cartilaginous fishes, a shark and a chimaera (holocephalan). As can be seen, these fishes are isosmotic or slightly hyperosmotic to seawater (SW) (Fig. 1), quite unlike the majority of marine vertebrates, which are markedly hypo osmotic (represented by the teleost flatfish, Fig. 1). In this respect elasmobranchs are more like marine invertebrates; however, about one-half the osmotic pressure in the former is due to urea and TMAO in both blood and cell, distinct from the universal use of inorganic ions (extracellular) and free amino acids (intracellular) among the latter organisms (see Clark, this volume).

Keywords

Urea Respiration Pyruvate NADH Cardiol 

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References

  1. Altringham JD, Yancey PH, Johnston IA (1982) The effect of osmoregulatory solutes on tension of skinned muscle fibres from dogfish skeletal muscle. J Exp Biol 96:443–445Google Scholar
  2. Anderson PM (1981) Purification and properties of the glutamine- and N-acetyl-L-glutamate-dependent carbamoyl phosphate synthetase from liver of Squalus acanthias. J Biol Chem 256: 12228–12238PubMedGoogle Scholar
  3. Balaban RS, Knepper MA (1983) Nitrogen-14 nuclear magnetic resonance spectroscopy of mammalian tissues. Am J Physiol 245:c439–C444PubMedGoogle Scholar
  4. Balinsky JB (1981) Adaptation of nitrogen metabolism to hyperosmotic environment in amphibia. J Exp Zool 215:335–350CrossRefGoogle Scholar
  5. Bonaventura J, Bonaventura C, Sullivan B (1974) Urea tolerance as a molecular adaptation of elasmobranch hemoglobins. Science 186:57–59PubMedCrossRefGoogle Scholar
  6. Boyd TA, Cha C-J, Forster RP, Goldstein L (1977) Free amino acids in tissues of the skate Raja erinacea and the stingray Dasyatis sabina: effects of environmental dilution. J Exp Zool 199: 435–442PubMedCrossRefGoogle Scholar
  7. Cleworth DR (1967) A comparative study on the effects of urea on contraction in skeletal muscle. Doctoral Dissertation, University of California, Los AngelesGoogle Scholar
  8. Cohen JJ, Krupp MA, Chidsey III CA (1958) Renal conservation of trimethylamine oxide by the spiny dogfish Squalus acanthias. Am J Physiol 194:229–235PubMedGoogle Scholar
  9. Fessier JH, Tandberg WD (1975) Interactions between collagen chains and fiber formation. J Supramol Struct 3:17–23Google Scholar
  10. Finley KD (1984) The role of methylamines and free amino acids in protection of mammalian kidney proteins. Masters Dissertation, San Diego State University, CaliforniaGoogle Scholar
  11. Forster RP, Goldstein L (1976) Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs. Am J Physiol 230:925–931PubMedGoogle Scholar
  12. Foulger JH, Mills CA (1930) The influence of urea on blood clotting. I. Thrombin clotting. Am J Physiol 94:51–59Google Scholar
  13. Goldstein L, Funkhouser D (1972) Biosynthesis of trimethylamine oxide in the nurse shark, Ginglyostoma cirratum. Comp Biochem Physiol 42A:51–57CrossRefGoogle Scholar
  14. Gordon MS, Tucker VA (1968) Further observations on the physiology of salinity adaptation in the crab-eating frog (Rana cancrivora). J Exp Biol 49:185–193Google Scholar
  15. Griffith RW, Umminger BL, Grant BF, Pang PKT, Pickford GE (1974) Serum composition of the coelacanth Latimeria chalumnae Smith. J Exp Zoll 187:87–102CrossRefGoogle Scholar
  16. Grollman EF, Grollman A (1985) Toxicity of urea and its role in the pathogenesis of uremia. J Clin Invest 38:749–755CrossRefGoogle Scholar
  17. Hand SC, Somero GN (1982) Urea and methylamine effects on rabbit muscle phosphofructokinase. J Biol Chem 257:734–741PubMedGoogle Scholar
  18. Hermans J (1966) The effect of protein denaturants on the stability of the helix. J Am Chem Soc 88:2418–2422CrossRefGoogle Scholar
  19. Horne FR (1971) Accumulation of urea by a pulmonate snail during estivation. Comp Biochem Physiol 38A:565–570CrossRefGoogle Scholar
  20. Lange R, Fugelli K (1965) The osmotic adjustment in the euryhaline teleosts, the flounder, Pleuronectes flesus L., and the three-spined stickleback, Gastrosteus aculaetus L. Comp Biochem Physiol 15:283–292PubMedCrossRefGoogle Scholar
  21. Lutz PL, Robertson JD (1971) Osmotic constituents of the coelacanth Latimeria chalumnae Smith. Biol Bull 141:553–560CrossRefGoogle Scholar
  22. McMillan DB, Battle HI (1954) Effects of ethyl carbamate and related compounds on early developmental processes in the leopard frog Rana pipiens. Cancer Res 14:319–323PubMedGoogle Scholar
  23. Pang PKT, Griffith RW, Atz JW (1977) Osmoregulation in elasmobranchs. Am Zool 17:365–377Google Scholar
  24. Pollard A, Wyn Jones RG (1979) Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta 144:291–298CrossRefGoogle Scholar
  25. Rajagopalan KV, Fridovich I, Handler P (1961) Competitive inhibition of enzyme activity by urea. J Biol Chem 236:1059–1065PubMedGoogle Scholar
  26. Robertson JD (1975) Osmotic constituents of the blood plasma and parietal muscle of Squalus acanthias L. Biol Bull 148:303–319PubMedCrossRefGoogle Scholar
  27. Robertson JD (1976) Chemical composition of the body fluids and muscle of the hagfish, Myxine glutinosa, and the rabbit-fish, Chimaera monstrosa. J Zool (Lond) 178:261–277CrossRefGoogle Scholar
  28. Schmidt E, Wilkes AB, Holland WC (1972) Effects of various glycerol or urea concentrations and incubation times on atrial contraction and ultrastructure. J Mol Cell Cardiol 4:113–120PubMedCrossRefGoogle Scholar
  29. Shigenaka JM, Roth LE, Pihlaja DJ (1971) Microtubules in the heliozoan axopodium. III. Degradation and reformation after dilute urea treatment. J Cell Sci 8:127–151PubMedGoogle Scholar
  30. Simpson WW, Ogden E (1932) The physiological significance of urea. I. The elasmobranch heart. J Exp Biol 9:1–5Google Scholar
  31. Smith HW (1936) The retention and physiological role of urea in the elasmobranchii. Biol Rev 11: 49–82CrossRefGoogle Scholar
  32. Smith HW (1953) From fish to philosopher. Little, Brown, BostonGoogle Scholar
  33. Thesleffs S, Schmidt-Nielsen K (1962) Osmotic tolerance of the muscles of the crab-eating frog Rana cancrivora. J Cell Comp Physiol 59:31–34CrossRefGoogle Scholar
  34. Wetlaufer DB, Malik SK, Stoller L, Coffin RL (1964) Nonpolar group participation in the denaturation of proteins by urea and guanidinium salts. Model compound studies. J Am Chem Soc 86: 508–514CrossRefGoogle Scholar
  35. Wyn Jones RG, Storey R, Leigh RA, Ahmad N, Pollard A (1977) A hypothesis on cytoplasmic osmoregulation. In: Marre E, Cifferi O (eds) Regulation of cell membrane activities in plants. North Holland, Amsterdam, p 121Google Scholar
  36. Yancey PH (1978) Urea, trimethylamine oxide, and pH: adaptive interactions among enzymes and intracellular solutes in elasmobranchs and other vertebrates. Doctoral Dissertation, University of California San DiegoGoogle Scholar
  37. Yancey PH, Somero GN (1978a) Temperature dependence of intracellular pH: its role in the conservation of pyruvate apparent Km values of vertebrate lactate dehydrogenases. J Comp Physiol 125:129–134Google Scholar
  38. Yancey PH, Somero GN (1978b) Urea-requiring lactate dehydrogenases of marine elasmobranch fishes. J Comp Physiol 125:135–141Google Scholar
  39. Yancey PH, Somero GN (1979) Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. Biochem J 183:317–323PubMedGoogle Scholar
  40. Yancey PH, Somero GN (1980) Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes. J Exp Zool 212:205–213CrossRefGoogle Scholar
  41. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: the evolution of osmolyte systems. Science 217:1214–1222PubMedCrossRefGoogle Scholar
  42. Zigman S, Munro J, Lerman S (1965) Effect of urea on the cold precipitation of proteins in the lens of dogfish. Nature 207:414–415PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1985

Authors and Affiliations

  • P. H. Yancey
    • 1
  1. 1.Biology DepartmentWhitman CollegeWalla WallaUSA

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