Ultracentrifugation studies of the location of the site involved in the interaction of pig heart lactate dehydrogenase with acidic phospholipids at low pH. A comparison with the muscle form of the enzyme

• Autorzy: Terlecki G , Czapinska E. , Hotowy K.
• Języki publikacji: EN

Abstrakty

EN

Lactate dehydrogenase (LDH) from the pig heart interacts with liposomes made of acidic phospholipids most effectively at low pH, close to the isoelectric point of the protein (pH = 5.5). This binding is not observed at neutral pH or high ionic strength. LDH-liposome complex formation requires an absence of nicotinamide adenine dinucleotides and adenine nucleotides in the interaction environment. Their presence limits the interaction of LDH with liposomes in a concentration-dependent manner. This phenomenon is not observed for pig skeletal muscle LDH. The heart LDH-liposome complexes formed in the absence of nicotinamide adenine dinucleotides and adenine nucleotides are stable after the addition of these substances even in millimolar concentrations. The LDH substrates and studied nucleotides that inhibit the interaction of pig heart LDH with acidic liposomes can be ordered according to their effectiveness as follows: NADH > NAD > ATP = ADP > AMP > pyruvate. The phosphorylated form of NAD (NADP), nonadenine nucleotides (GTP, CTP, UTP) and lactate are ineffective. Chemically cross-linked pig heart LDH, with a tetrameric structure stable at low pH, behaves analogously to the unmodified enzyme, which excludes the participation of the interfacing parts of subunits in the interaction with acidic phospholipids. The presented results indicate that in lowered pH conditions, the NADH-cofactor binding site of pig heart LDH is strongly involved in the interaction of the enzyme with acidic phospholipids. The contribution of the ATP/ADP binding site to this process can also be considered. In the case of pig skeletal muscle LDH, neither the cofactor binding site nor the subunit interfacing areas seem to be involved in the interaction.

Słowa kluczowe

EN

pig; lactate dehydrogenase; acidic phospholipid; cardiolipin; muscle form; enzyme; ultracentrifugation; isoenzyme; lipid-protein interaction; heart; pH; phosphatidylserine

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2007
• Tom: 12
• Numer: 3
• Opis fizyczny: p.378-395,fig.,ref.

Twórcy

autor

Terlecki G

• Wroclaw Medical University, Wroclaw, Poland

autor

Czapinska E.

autor

Hotowy K.

Bibliografia

• 1. Aubert, A., Costalat, R., Magistretti, P.J. and Pellerin, L. Brain lactate kinetics: Modeling evidence for neuronal lactate uptake upon activation. Proc. Natl. Acad. Sci. USA 102 (2005) 16448-16453.
• 2. Crawford, R.M., Budas, G.R., Jovanovic, S., Ranki, H.J., Wilson, T.J., Davies, A.M. and Jovanovic, A. M-LDH serves as a sarcolemmal K(ATP) channel subunit essential for cell protection against ischemia. EMBO J. 21 (2002) 3936-3948.
• 3. Pioli, P.A., Hamilton, B.J., Connolly, J.E., Brewer, G. and Rigby, WF. Lactate dehydrogenase is an AU-rich element-binding protein that directly interacts with AUF1. J. Biol. Chem. 277 (2002) 35738-35745.
• 4. Li, S.S. Lactate dehydrogenase isoenzymes A (muscle), B (heart) and C (testis) of mammals and the genes coding for these enzymes. Biochem. Soc. Trans. 2 (1989) 304-307.
• 5. Li, S.S. Human and mouse lactate dehydrogenase genes A (muscle), B (heart), and C (testis): protein structure, genomic organization, regulation of expression, and molecular evolution. Prog. Clin. Biol. Res. 344 (1990) 75-99.
• 6. Read, J.A., Winter, V.J., Eszes, C.M., Sessions, R.B. and Brady, R.L. Structural basis for altered activity of M- and H-isozyme forms of human lactate dehydrogenase. Proteins 43 (2001) 175-185.
• 7. Wang, X.C., Jiang, L. and Zhou, H.M. Minimal functional unit of lactate dehydrogenase. J. Protein Chem. 3 (1997) 227-231.
• 8. King, L. and Weber, G. Conformational drift of dissociated lactate dehydrogenases. Biochemistry 25 (1986) 3632-3637.
• 9. Dabrowska, A. and Gutowicz, J. Interaction of bovine heart lactate dehydrogenase with erythrocyte lipids. Biochim. Biophys. Acta 855 (1986) 99-104.
• 10. Dabrowska, A., Terlecki, G. and Gutowicz, J. Interaction of bovine skeletal muscle lactate dehydrogenase with liposomes. Comparison with the data for the heart enzyme. Biochim. Biophys. Acta 980 (1989) 357-360.
• 11. Terlecki, G., Czapińska, E., Rogozik, K., Lisowski, M. and Gutowicz, J. Investigation of the interaction of pig muscle lactate dehydrogenase with acidic phospholipids at low pH. Biochim. Biophys. Acta 1758 (2006) 133-144.
• 12. Terlecki, G., Czapinska, E. and Gutowicz J. The role of lipid phase structure in the interaction of lactate dehydrogenase with phosphatidylserine. Activity studies. Cell. Mol. Biol. Lett. 7 (2002) 895-903.
• 13. Terlecki, G. and Gutowicz, J. Further evidence for the importance of lipid bilayers in the interaction between lactate dehydrogenase and phosphatidylserine. Cell. Mol. Biol. Lett. 7 (2002) 905-910.
• 14. Marsh, D. Handbook of Lipids Bilayers, CRC Press, Boca Raton, FL, 1990.
• 15. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254.
• 16. Gottschalk, N. and Jaenicke, R. Chemically crosslinked lactate dehydrogenase: stability and reconstitution after glutaraldehyde fixation. Biotechnology and Applied Biochemistry 9 (1987) 387-400.
• 17. 18. Rouser, G., Siakatos, A.N. and Fleischer, S. Quantitative analysis of phospholipids by thin-layer chromatography and phosphorus analysis of spots. Lipids 1 (1966) 85-86.
• 18. Cabiaux, V., Vandenbranden, M., Falmagne, P. and Ruysschaert, J.M. Aggregation and fusion of lipid vesicles induced by diphtheria toxin at low pH: possible involvement of the P site and the NAD+ binding site. Biosci. Rep. 3 (1985) 243-250.
• 19. Cabiaux, V., Vandenbranden, M., Falmagne, P. and Ruysschaert, J.M. Diphtheria toxin induces fusion of small unilamellar vesicles at low pH. Biochim. Biophys. Acta 775 (1984) 31-36.
• 20. Wittenberger, C.L. Kinetic studies on the inhibition of a (D(-)-specific lactate dehydrogenase by adenosine triphosphate. J. Biol. Chem. 243 (1968) 3067-3075.
• 21. Torres-da Matta, J., Batista e Silva, C. and Hasson-Voloch, A. Effect of ATP on purified L(+) lactate dehydrogenase from electric organ of Electrophorus electricus (L.). Int. J. Biochem. 18 (1986) 191-194.
• 22. Busto, F., de Arriaga, D. and Soler, J. ATP, ADP and AMP on the regulation of lactate dehydrogenase activity of Phycomyces blakesleeanus. Int. J. Biochem. 15 (1983) 73-78.
• 23. Nemat-Gorgani, M. and Wilson, J.E. Acidic phospholipids may inhibit rat brain hexokinase by interaction at the nucleotide binding site. Arch. Biochem. Biophys. 236 (1985) 220-227.
• 24. Craig, D.B. and Wallace, C.J. ATP binding to cytochrome c diminishes electron flow in the mitochondrial respiratory pathway. Protein Sci. 2 (1993) 966-976.
• 25. .Kimelberg, H.K and Lee, C.P. Binding and electron transfer to cytochrome c in artificial phospholipid membranes. Biochem. Biophys. Res. Commun. 34 (1969) 784-790.
• 26. Vanderkooi, J., Erecinska, M. and Chance, B. Cytochrome c interaction with membranes. II. Comparative study of the interaction of c cytochromes with the mitochondrial membrane. Arch. Biochem. Biophys. 152 (1973) 531-540.
• 27. Mustonen, P., Virtanen, J.A., Somerharju, P.J. and Kinnunen, P.K. Binding of cytochrome c to liposomes as revealed by the quenching of fluorescence from pyrene-labeled phospholipids. Biochemistry 26 (1987) 2991-2997.
• 28. Demel, R.A., Jordi, W., Lambrechts, H., van Damme, H., Hovius, R. and de Kruijff, B. Differential interactions of apo- and holocytochrome c with acidic membrane lipids in model systems and the implications for their import into mitochondria. J. Biol. Chem. 264 (1989) 3988-3997.
• 29. Nicholls, P. Cytochrome c binding to enzymes and membranes. Biochim. Biophys. Acta 346 (1974) 261-310.
• 30. Brown, L.R. and Wuthrich, K. NMR and ESR studies of the interactions of cytochrome c with mixed cardiolipin-phosphatidylcholine vesicles. Biochim. Biophys. Acta 468 (1977) 389-410.
• 31. Rytomaa, M., Mustonen, P. and Kinnunen, P.K. Reversible, nonionic, and pHdependent association of cytochrome c with cardiolipin-phosphatidylcholine liposomes. J. Biol. Chem. 267 (1992) 22243-22248.
• 32. Rytomaa, M. and Kinnunen, P.K. Evidence for two distinct acidic phospholipidbinding sites in cytochrome c. J. Biol. Chem. 269 (1994) 1770-1774.
• 33. Lovell, S.J. and Winzor, D.J. Effects of phosphate on the dissociation and enzymatic stability of rabbit muscle lactate dehydrogenase. Biochemistry 13 (1974) 3527-3531.
• 34. Okeley, N.M. and Gelb, M.H. A designed probe for acidic phospholipids reveals the unique enriched anionic character of the cytosolic face of the mammalian plasma membrane. J. Biol. Chem. 279 (2004) 21833-21840.
• 35. Korzeniewski, B. and Zoladz, J.A. Influence of rapid changes in cytosolic pH on oxidative phosphorylation in skeletal muscle: theoretical studies. Biochem. J. 365 (2002) 249-258.
• 36. Korzeniewski, B. AMP deamination delays muscle acidification during heavy exercise and hypoxia. J. Biol. Chem. 281 (2006) 3057-3066.
• 37. Kraayenhof, R., Sterk, G.J. and Sang, H.W. Probing biomembrane interfacial potential and pH profiles with a new type of float-like fluorophores positioned at varying distance from the membrane surface. Biochemistry 32 (1993) 10057- 10066.
• 38. Zhao, H., Tuominen, E.K. and Kinnunen, P.K. Formation of amyloid fibers triggered by phosphatidylserine-containing membranes. Biochemistry 43 (2004) 10302-10307.
• 39. Baba, N. and Sharma, H.M. Histochemistry of lactic dehydrogenase in heart and pectoralis muscles of rat. J. Cell. Biol. 51 (1971) 621-635.
• 40. Kline, E.S., Brandt, R.B., Laux, J.E., Spainhour, S.E., Higgins, E.S., Rogers, K.S., Tinsley, S.B. and Waters, M.G. Localization of L-lactate dehydrogenase in mitochondria. Arch. Biochem. Biophys. 246 (1986) 673-680.
• 41. Brandt, R.B., Laux, J.E., Spainhour, S.E. and Kline, E.S. Lactate dehydrogenase in rat mitochondria. Arch. Biochem. Biophys. 259 (1987) 412-422
• 42. Gladden, LB. Lactate metabolism: a new paradigm for the third millennium. J. Physiol. 558 (2004) 5-30.
• 43. Brooks, G.A., Dubouchaud, H., Brown, M., Sicurello, J.P. and Butz, C.E. Role of mitochondrial lactate dehydrogenase and lactate oxidation in the intracellular lactate shuttle. Proc. Natl. Acad. Sci. USA 96 (1999) 1129-1134.
• 44. Hashimoto, T., Hussien, R. and Brooks, G.A. Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: evidence of a mitochondrial lactate oxidation complex. Am. J. Physiol. Endocrinol. Metab. 290 (2006) 1237-1244.