A Physicochemical Basis for the Selection of Osmolytes by Nature

  • S. N. Timasheff

Abstract

It is a striking fact of nature that compounds used as cellular osmolyte systems by a variety of plant and animal vertebrate and invertebrate systems are confined to a small number of chemical structures, all, or most of which are distributed over the entire gamut of organisms (Yancey et al. 1982; Somero 1986; Somero, this Vol.). These comprise sugars and other polyols, amino acids and amino acid derivatives, methylamines, and in some cases urea, frequently in combination with methylamines All are electrically neutral molecules. With the exception of urea all of these organic osmolytes are “compatible solutes” (Brown and Simpson 1972; Clark 1985), i.e., they do not disturb cellular structure and function. Among amino acids, arginine and lysine are not used as osmolytes (Yancey et al. 1982). They are known to be “incompatible” (Somero 1986), in that they interfere with some biochemical processes. Nor are amino acids that contain large hydrophobic side chains used. It is noteworthy that in a case where arginine is released it is immediately converted to the “compatible” solute octopine (Hochachka et al. 1977).

Keywords

Sugar Sucrose Glycerol Urea Glycine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arakawa T, Timasheff SN (1982) Stabilization of protein structure by sugars. Biochemistry 21: 6536–6544PubMedCrossRefGoogle Scholar
  2. Arakawa T, Timasheff SN (1983) Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Arch Biochem Biophys 224: 169–177PubMedCrossRefGoogle Scholar
  3. Arakawa T, Timasheff SN (1984a) The mechanism of action of Na glutamate, glysine HCI, and PIPES in the stabilization of tubulin and microtubule formation. J Biol Chem 259: 4979–4986PubMedGoogle Scholar
  4. Arakawa T, Timasheff SN (1984b) Protein stabilization and destabilization by guanidinium salts. Biochemistry 23: 5924–5929PubMedCrossRefGoogle Scholar
  5. Arakawa T, Timasheff SN (1985a) Mechanism of poly(ethylene glycol) interaction with proteins. Biochemistry 24: 6756–6762PubMedCrossRefGoogle Scholar
  6. Arakawa T, Timasheff SN (1985b) The stabilization of proteins by osmolytes. Biophys J 47: 411–414PubMedCrossRefGoogle Scholar
  7. Arakawa T, Bhat R, Timasheff SN (1990) Preferential interactions determine protein solubility in three-component solutions: The MgCl2 system. Biochemistry 29: 1914–1923PubMedCrossRefGoogle Scholar
  8. Berkeley the Earl of, Hartley EGJ (1906) On the osmotic pressure of some concentrated aqueous solutions. Trans R Soc Lond A 206: 481–507CrossRefGoogle Scholar
  9. Borowitzka LJ, Brown AD (1974) The salt relations of marine and halophilic species of the unicellular green alga, Duneliella. The role of glycerol as compatible solute. Arch Microbiol 96: 37–52CrossRefGoogle Scholar
  10. Bowlus RD, Somero GN (1979) Solute compatibility with enzyme function and structure: rationales for the selection of osmotic agents and end-products of anaerobic metabolism in marine invertebrates. J Exp Zool 208: 137–152PubMedCrossRefGoogle Scholar
  11. Brown AD, Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J Gen Microbiol 72: 589–591PubMedGoogle Scholar
  12. Bull HB, Breese K (1974) Surface tension of amino acid solutions: a hydrophobicity scale of the amino acid residues. Arch Biochem Biophys 161: 665–670PubMedCrossRefGoogle Scholar
  13. Clark ME (1985) The osmotic role of amino acids: Discovery and function. In: Gilles R, Gilles Baillien M (eds) Transport processes, iono-and osmoregulation. Springer, Berlin Heidelberg New York, pp 412–423CrossRefGoogle Scholar
  14. Clark ME, Zounes M (1977) The effects of selected cell osmolytes on the activity of lactate dehydrogenase from the euryhaline polychaete, Nereis succinea. Biol Bull, Woods Hole, Mass, 153: 468–484CrossRefGoogle Scholar
  15. Cohn EJ, Edsall JT (1943) Proteins, amino acids and peptides. Reinhold, New York, p 218Google Scholar
  16. Frazer JCW, Myrick RT (1916) Osmotic pressure of sucrose solutions at 30 °C. J Am Chem Soc 38: 1907–1922CrossRefGoogle Scholar
  17. Gekko K, Koga S (1984) The stability of protein structure in aqueous propylene glycol amino acid solubility and preferential solvation of protein. Biochim Biophys Acta 786: 151–160CrossRefGoogle Scholar
  18. Gekko K, Morikawa T (1981) Preferential hydration of bovine serum albumin in polyhydric alcohol-water mixtures. J Biochem Jpn 90: 39–50Google Scholar
  19. Gekko K, Timasheff SN (1981) Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry 20: 4667–4676PubMedCrossRefGoogle Scholar
  20. Gibbs JW (1878) On the equilibrium of heterogeneous substances. Trans Conn Acad 3: 343–524Google Scholar
  21. Hochachka PW, Hartline PH, Fields JHA (1977) Octopine as an end product of anaerobic glycolysis in the chambered nautilus. Science 195: 72–74PubMedCrossRefGoogle Scholar
  22. Landt E (1931) The surface tensions of solutions of various sugars. Z Ver Dtsch Zuckerind 81: 119–124Google Scholar
  23. Lee JC, Timasheff SN (1974) Partial specific volumes and interactions with solvent components of proteins in guanidine hydrochloride. Biochemistry 13: 257–265PubMedCrossRefGoogle Scholar
  24. Lee JC, Timasheff SN (1981) The stabilization of proteins by sucrose. J Biol Chem 256: 7193–7201PubMedGoogle Scholar
  25. Low PS (1985) Molecular basis of the biological compatibility of Nature’s osmolytes. In: Gilles R, Gilles-Baillien M (eds) Transport processes, iono-and osmoregulation. Springer, Berlin Hei-delberg New York, pp 469–477CrossRefGoogle Scholar
  26. Melander W, Horvath C (1977) Salt effects on hydrophobic interactions in precipitation and chromatography of proteins: An interpretation of the lyotropic series. Arch Biochem Biophys 183: 200–215PubMedCrossRefGoogle Scholar
  27. Morse HN, Holland WW, Myers CN, Cash G, Zinn JB (1912) The omostic pressure of cane sugar solutions at high temperature. In: Washburn EW (ed) International Critical Tables (1928) 4:429. Am Chem J 48: 29–94Google Scholar
  28. Na GC, Timasheff SN (1981) Interaction of calf brain tubulin with glycerol. J Mol Biol 151: 165–178PubMedCrossRefGoogle Scholar
  29. Pappenheimer JR, Lepie MP, Wyman J Jr (1936) The surface tension of aqueous solutions of dipolar ions. J Am Chem Soc 58: 1851–1855CrossRefGoogle Scholar
  30. Pollard A, Wyn-Jones RG (1979) Enzyme activities in concentrated solutions of glycine betaine and other solutes. Planta 144: 291–298CrossRefGoogle Scholar
  31. Scatchard G, Prentiss SS (1934) Freezing points of aqueous solutions. VIII. J Am Chem Soc 56: 2314–2319CrossRefGoogle Scholar
  32. Smith PK, Smith ERB (1937) The activity of aliphatic amino acids in aqueous solution at 25 °C. J Biol Chem 121: 607–613Google Scholar
  33. Smith PK, Smith ERB (1940) The activities of some hydroxy-and N-methylamino acids and proline in aqueous solution at 25 °C. J Biol Chem 132: 57–64Google Scholar
  34. Somero GN (1986) Protons, osmolytes, and fitness of internal milieu for protein function. Am J Physiol 251: R197 - R213PubMedGoogle Scholar
  35. Tanford C (1973) The hydrophobic effect: formation of micelles and biological membranes. Wiley, New York LondonGoogle Scholar
  36. Timasheff SN (1991) Stabilization of protein structure by solvent additives. In: Ahern TJ, Manning M (eds) Stability of protein pharmaceuticals: in vivo pathways of degradation and strategies for protein stabilization, Vol 3Google Scholar
  37. von Hippel PH, Wong K-Y (1965) On the conformational stability of globular proteins. J Biol Chem 240: 3909–3923Google Scholar
  38. von Hippel PH, Wong K-Y (1965) On the conformational stability of globular proteins. The effects of various electrolytes and nonelectrolytes on the thermal ribonuclease transition. J Biol Chem 240: 3909–3923Google Scholar
  39. Warner DT (1962) Some possible relationships of carbohydrates and other biological components with the water structure at 37 °. Nature (Lond) 196: 1055–1058CrossRefGoogle Scholar
  40. Wyman J Jr (1964) Linked functions and reciprocal effects in hemoglobin: a second look. Adv Protein Chem 19: 223–286PubMedCrossRefGoogle Scholar
  41. 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
  42. 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
  43. Yancey PH, Somero GN (1980) Methylamine osmoregulatory solutes of elasmobranch fishes coun-teract urea inhibition of enzymes. J Exp Zool 212: 205–213CrossRefGoogle Scholar
  44. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217: 1214–1222PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1992

Authors and Affiliations

  • S. N. Timasheff
    • 1
  1. 1.Graduate Department of BiochemistryBrandeis UniversityWalthamUSA

Personalised recommendations