Trimethylamine oxide stabilizes teleost and mammalian lactate dehydrogenases against inactivation by hydrostatic pressure and trypsinolysis

Journal of Experimental Biology

Volumn 202, Issue 24, 1999, Pages 3597-3603

  Yancey, Paul H ^a,b   Siebenaller, Joseph F ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b WHITMAN COLLEGE   (United States)

Author keywords

Deep sea; Hydrostatic pressure; Lactate dehydrogenase; Osmolyte; Trimethylamine oxide; Trypsinolysis

Indexed keywords

LACTATE DEHYDROGENASE; METHYLAMINE; TRIMETHYLOXAMINE; TRYPSIN;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; CATTLE; COMPARATIVE STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME STABILITY; FISH; HYDROSTATIC PRESSURE; METABOLISM; SPECIES DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; CATTLE; ENZYME ACTIVATION; ENZYME STABILITY; FISHES; HYDROSTATIC PRESSURE; L-LACTATE DEHYDROGENASE; METHYLAMINES; SPECIES SPECIFICITY; TRYPSIN;

ANIMALIA; BOS TAURUS; ELASMOBRANCHII; INVERTEBRATA; MAMMALIA; PISCES; SCORPAENIDAE; SEBASTES MELANOPS; SEBASTOLOBUS ALASCANUS; SEBASTOLOBUS ALTIVELIS; TELEOSTEI;

EID: 0033428092     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Balny, C., Mozhaev, V. V. and Lange, R. (1997). Hydrostatic pressure and proteins: basic concepts and new data. Comp. Biochem. Physiol. 116A, 299-304.
2. Baskakov, I. and Bolen, D. W. (1998). Forcing thermodynamically unfolded proteins to fold. J. biol. Chem. 273, 4831-4834.
3. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. Brown, A. D. and Simpson, J. R. (1972). Water relations of sugar-tolerant yeasts: The role of intracellular polyols. J. gen. Microbiol. 72, 589-591.
5. 4-lactate dehydrogenase homologs from marine fishes living at different depths. Int. J. Biochem. 24, 1125-1139.
6. Fyfe-Johnson, A. L. and Yancey, P. H. (1998). Pressure inhibition of deep-sea grenadier lactate dehydrogenase and counteractions by trimethylamine oxide. Am. Zool. 38, 120A.
7. Gillett, M. B., Suko, J. R., Santoso, F. O. and Yancey, P. H. (1997) Elevated levels of trimethylamine oxide in muscles of deep-sea gadiform teleosts: a high-pressure adaptation? J. exp. Zool. 279, 386-391
8. Graßl, M. and Walter, H.-E. (1983). Biochemical reagents for general use. Trypsin. In Methods of Enzymatic Analysis, vol. II (ed. U. Bergmeyer). pp. 319-320. Weinheim: Verlag Chemie.
9. Groß, M. Auerbach, G. and Jaenicke, R. (1993). The catalytic activities of monomeric enzymes show complex pressure dependence. FEBS Lett. 321, 256-260.
10. Hebard, C. E., Flick, G. J. and Martin, R. E. (1982). Occurrence and significance of trimethylamine oxide and its derivatives in fish and shellfish. In Chemistry and Biochemistry of Marine Food Products (ed. R. E. Martin), pp. 149-175. Westport, CT: AVI Publishing.
11. Hennessey, J. P., Jr. and Siebenaller, J. F. (1985). Pressure inactivation of tetrameric lactate dehydrogenase homologues of confamilial deep-living fishes. J. comp. Physiol. B 155, 647-652.
12. 4-lactate dehydrogenase homologues from marine fishes. J. exp. Zool. 241, 9-15.
13. Hennessey, J. P., Jr. and Siebenaller, J. F. (1987b). Inactivation of NAD-dependent dehydrogenases from shallow- and deep-living fishes by hydrostatic pressure and proteolysis. Biochim. Biophys. Acta 913, 285-291.
14. Hubbs, C. L. (1926). The supposed intergradation of the two species of Sebastolobus (a genus of Scorpaenoid fishes) of Western America. Amer. Mus. Novit. 216, 1-9.
15. Kelly, R. H. and Yancey, P. H. (1999). High contents of trimethylamine oxide correlating with depth in deep-sea teleost fishes, skates, and decapod crustaceans. Biol. Bull. 196, 18-25.
16. King, L. and Weber, G. (1986). Conformational drift of dissociated lactate dehydrogenases. Biochemistry 25, 3632-3637.
17. Kunugi, S., Fukuda, M. and Ise, N. (1982). Pressure dependence of trypsin-catalyzed hydrolyses of specific substrates. Biochim. Biophys. Acta 704, 107-113.
18. Laemmli, U. K. (1970). Cleavage of structural proteins during assembly of the head of bacleriophage T4. Nature 227, 680-685.
19. Lange, R. and Fugelli, K. (1965). The osmotic adjustment in the euryhaline teleosts, the flounder, Pleuranectes flesus L., and the three-spined stickleback, Gastrosteus aculaetus L. Comp. Biochem. Physiol. 15, 283-292.
20. Lauth, R. R., Wilkins, M. E. and Ramore, P. A., Jr. (1997). Results of trawl surveys of groundfish resouces of the West Coast upper continental slope from 1989 to 1993. US Department of Commerce, NOAA Technical Memorandum NMFS-AFSC-79, 342p.
21. Mustafa, T., Moon, T. W. and Hochachka, P. W. (1971). Effects of pressure and temperature on the catalytic and regulatory properties of muscle pyruvate kinase from an off-shore benthic fish. Am. Zool. 11, 451-466.
22. Neuman, R. C., Kauzmann, W. and Zipp, A. (1973). Pressure dependence of weak acid ionizations in aqueous buffers. J. phys. Chem. 77, 2687-2691.
23. Noto, R., Martorana, V., Emanuele, A., and Fornili, S. L. (1995). Comparison of the water perturbations induced by two small organic solutes: ab initio calculations and molecular dynamics simulation. J. Chem. Soc. Farad. Trans. 91, 3803-3808.
24. 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. US Department of Commerce, NOAA Technical Memorandum NMFS-AFSC-95, 46p.
25. Raymond, J. R. (1994). Seasonal variations of trimethylamine oxide and urea in the blood of a cold-adapted marine teleost, the rainbow smelt. Fish Physiol. Biochem. 12, 13-22.
26. Raymond, J. R. and DeVries, A. L. (1998). Elevated concentrations and synthetic pathways of trimethylamine oxide and urea in some teleost fishes of McMurdo Sound, Antarctica. Fish Physiol. Biochem. 18, 387-398.
27. Saunders, P. M. and Fofonoff, N. P. (1976). Conversion of pressure to depth in the ocean. Deep-Sea Res. 23, 109-111.
28. Schmid, G., Lüdeman, H. D. and Jaenicke, R. (1978). Oxidation of sulfhydryl groups in lactate dehydrogenase under high hydrostatic pressure. Eur. J. Biochem. 86, 219-224.
29. Siebenaller, J. F. (1984). Structural comparison of lactate dehydrogenase homologs differing in senstivity to hydrostatic pressure. Biochim. Biophys. Acta 786, 161-169.
30. Siebenaller, J. F. (1987). Pressure adaptation in deep-sea animals. In Current Perspectives in High Pressure Biology (ed. H. W. Jannasch, R. E. Marquis and A. M. Zimmerman), pp. 33-48. London: Academic Press.
31. 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.
32. Siebenaller, J. F. and Somero, G. N. (1989). Biochemical adaptation to the deep sea. CRC Crit. Rev. Aquatic Sci. 1, 1-25.
33. Somero, G. N. and Siebenaller, J. F. (1979) Inefficient lactate dehydrogenases of deep-sea fishes. Nature 282, 100-102.
34. Sokal, R. R. and Rohlf, F. J. (1995). Biometry, third edition, 887 pp. New York: W. H. Freeman and Co.
35. Spielman, H., Erickson, R. P. and Epstein, C. J. (1973). The separation of lactate dehydrogenase X from other lactate dehydrogenase isozymes of mouse testes by affinity chromatography. FEBS Lett. 35, 19-23.
36. Swezey, R. R. and Somero, G. N. (1982). Polymerization thermodynamics and structural stabilities of skeletal muscle actins from vertebrates adapted to different temperatures and hydrostatic pressures. Biochemistry 21, 4496-4503.
37. Swezey, R. R. and Somero, G. N. (1985). Pressure effects on actin self-assembly: interspecific differences in equilibrium kinetics of the G to F transformation. Biochemistry 24, 852-860.
38. Timasheff, S. N. (1992). A physicochemical basis for the selection of osmolytes by nature. In Water and Life: A Comparative Analysis of Water Relationships at the Organismic, Cellular, and Molecular Levels (ed. G. N. Somero, C. B. Osmond and C. L. Bolis), pp. 70-84. Berlin, New York: Springer-Verlag.
39. 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 dpeths. Limnol. Oceanogr. 35, 1314-1328.
40. Wang, A. and Bolen, D. W. (1997). A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 36, 9101-9108.
41. Weber, G. (1986). Phenomenological description of the association of protein subunits subjected to conformational drift. Effects of dilution and of hydrostatic pressure. Biochemistry 25, 3626-3631.
42. Welch, W. J. and Brown, C. R. (1996). Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1, 109-115.
43. Yancey, P. H. (1985). Organic osmotic effectors in cartilaginous fishes. In Transport Processes, Iono- and Osmoregulation (ed. R. Gilles and M. Gilles-Ballien), pp. 424-436. Berlin, New York: Springer-Verlag.
44. Yancey, P. H. (1994). Compatible and counteracting solutes. In Cellular and Molecular Physiology of Cell Volume Regulation (ed. K. Strange), pp. 81-109. London: CRC Press.
45. Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D. and Somero, G. N. (1982). Living with water stress: Evolution of osmolyte systems. Science 217, 1214-1222.
46. m values of vertebrate lactate dehydrogenase. J. comp. Physiol. 125, 129-134.
47. Zobell, C. E. and Oppenheimer, C. H. (1950). Some effects of hydrostatic pressure on the multiplication and morphology of marine bacteria. J. Bacterial. 60, 771-778.