Pyruvate uptake is inhibited by valproic acid and metabolites in mitochondrial membranes

FEBS Letters

Volumn 582, Issue 23-24, 2008, Pages 3359-3366

  Aires, Cátia C P ^a   Soveral, Graça ^b   Luís, Paula B M ^a   ten Brink, Herman J ^c   de Almeida, Isabel Tavares ^a   Duran, Marinus ^d   Wanders, Ronald J A ^d   Silva, Margarida F B ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

4 Valproic acid; Drug metabolism; Inverted submitochondrial membranes; Mitochondrial pyruvate uptake; Pyruvate transport; Valproic acid

Indexed keywords

2 CYANO 4 HYDROXYCINNAMATE; COENZYME A; ENZYME INHIBITOR; PYRUVIC ACID; UNCLASSIFIED DRUG; VALPROIC ACID;

ARTICLE; DRUG EFFECT; DRUG INHIBITION; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ANTICONVULSANTS; BIOLOGICAL TRANSPORT; COENZYME A; FATTY ACIDS, MONOUNSATURATED; FATTY ACIDS, UNSATURATED; LIVER; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANES; OXIDATIVE PHOSPHORYLATION; PYRUVIC ACID; RATS; RATS, WISTAR; VALPROIC ACID;

RATTUS;

EID: 53049098697     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2008.08.028     Document Type: Article

References (45)

1. Silva M.F.B., Ruiter J.P.N., IJlst L., Jakobs C., Duran M., de Almeida I.T., and Wanders R.J.A. Valproate inhibits the mitochondrial pyruvate-driven oxidative phosphorylation in vitro. J. Inherit. Metab. Dis. 20 (1997) 397-400
2. Hildyard J.C.W., and Halestrap A.P. Identification of the mitochondrial pyruvate carrier in Saccharomyces cerevisiae. Biochem. J. 374 (2003) 607-611
3. Palmieri F., Agrimi G., Blanco E., Castegna A., Di Noia M.A., Iacobazzi V., Lasorsa F.M., Morobbio C.M.T., Palmieri L., Scarcia P., Todisco S., Vozza A., and Walker J. Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins. Biochim. Biophys. Acta 1757 (2006) 1249-1262
4. Palmieri F., Bisaccia F., Capobianco L., Dolce V., Fiermonte G., Iacobazzi V., Indiveri C., and Palmieri L. Mitochondrial metabolite transporters. Biochim. Biophys. Acta 1275 (1996) 127-132
5. Papa S., Francavilla A., Paradies G., and Meduri B. The transport of pyruvate in rat liver mitochondria. FEBS Lett. 12 5 (1971) 285-288
6. Halestrap A.P., and Denton R.M. Specific inhibition of pyruvate transport in rat liver mitochondria and human erythrocytes by α-cyano-4-hydroxycinnamate. Biochem. J. 138 (1974) 313-316
7. Halestrap A.P. The mitochondrial pyruvate carrier: kinetics and specificity for substrates and inhibitors. Biochem. J. 148 (1975) 85-96
8. Halestrap A.P., and Denton R.M. The specificity and metabolic implications of the inhibition of pyruvate transport in isolated mitochondria and intact tissue preparations by α-cyano-4-hydroxycinnamate and related compounds. Biochem. J. 148 (1975) 97-106
9. Halestrap A.P. The mechanism of the inhibition of the mitochondrial pyruvate transporter by α-cyanocinnamate derivates. Biochem. J. 156 (1976) 181-183
10. Halestrap A.P. Pyruvate and ketone-body transport across the mitochondrial membrane: exchange properties, pH dependence and mechanism of the carrier. Biochem. J. 172 (1978) 377-387
11. Nalecz K.A., Bolli R., Wojtczak L., and Azzi A. The monocarboxylate carrier from bovine heart mitochondria: partial purification and its substrate-transporting properties in a reconstituted system. Biochim. Biophys. Acta 851 (1986) 29-37
12. Bolli R., Nalecz K.A., and Azzi A. Monocarboxylate and α-ketoglutarate carriers from bovine heart mitochondria. J. Biol. Chem. 264 30 (1989) 18024-18030
13. Capuano F., Paola M.D., Azzi A., and Papa S. The monocarboxylate carrier from rat liver mitochondria: purification and kinetic characterization in a reconstituted system. FEBS Lett. 261 1 (1990) 39-42
14. Nalecz M.J., Nalecz K.A., and Azzi A. Purification and functional characterisation of the pyruvate (monocarboxylate) carrier from baker's yeast mitochondria (Saccharomyces cerevisiae). Biochim. Biophys. Acta 1079 (1991) 87-95
15. Sugden M.C., and Holness M.J. Trials, tribulations and finally, a transporter: the identification of the mitochondrial pyruvate transporter. Biochem. J. (2003) 374 10.1042/BJ20031105
16. + transporter in Saccharomyces cerevisiae. J. Biol. Chem. 281 3 (2006) 1524-1531
17. Laloi M. Plant mitochondrial carriers: an overview. Cell. Mol. Life Sci. 56 (1999) 918-944
18. Criscuolo F., Mozo J., Hurtaud C., Nubel T., and Bouillaud F. UCP2, UCP3, avUCP, what do they do when proton transport is not stimulated? Possible relevance to pyruvate and glutamine metabolism. Biochim. Biophys. Acta 1757 (2006) 1284-1291
19. Sluse F.E., Jarmuszkiewicz W., Navet R., Douette P., Mathy G., and Sluse-Goffart C.M. Mitochondrial UCPs: new insights into regulation and impact. Biochim. Biophys. Acta 1757 (2006) 480-485
20. Jezek P., and Borecky J. Mitochondrial uncoupling protein may participate in futile cycling of pyruvate and other monocarboxylates. Am. J. Physiol. Cell Physiol. 275 (1998) 496-504
21. Villarroya F., Iglesias R., and Giralt M. PPARs in the control of uncoupling proteins gene expression. PPAR Res. 2007 (2007) 74364
22. Benavides J., Martin A., Ugarte M., and Valdivieso F. Inhibition by valproic acid of pyruvate uptake by brain mitochondria. Biochem. Pharmacol. 31 8 (1982) 1633-1636
23. Silva M.F.B., Ruiter J.P.N., Overmars H., Bootsma A.H., van Gennip A.H., Jakobs C., Duran M., de Almeida I.T., and Wanders R.J.A. Complete β-oxidation of valproate: cleavage of 3-oxovalproyl-CoA by a mitochondrial 3-oxoacyl-CoA thiolase. Biochem. J. 362 (2002) 755-760
24. Silva M.F.B., Ruiter J.P.N., IJlst L., Allers P., ten Brink H.J., Jakobs C., Duran M., de Almeida I.T., and Wanders R.J.A. Synthesis and intramitochondrial levels of valproyl-Coenzyme A metabolites. Anal. Biochem. 290 (2001) 60-67
25. Abbott F.S., and Anari M.R. Chemistry and biotransformation. In: Löscher W. (Ed). Milestones in Drug Therapy-Valproate (1999), Birkhäuser Verlag, Basel 47-75
26. Aires C.C.P., Ruiter J.P.N., Luís P.B.M., ten Brink H.J., IJlst L., de Almeida I.T., Duran M., Wanders R.J.A., and Silva M.F.B. Studies on the extra-mitochondrial CoA-ester formation of valproic and 4-valproic acids. Biochim. Biophys. Acta 1771 (2007) 533-543
27. Rettenmeyer A.W., Prickett K.S., Gordon W.P., Bjorge S.M., Chang S.-L., Levy R.H., and Baillie T.A. Studies on the biotransformation in the perfused rat liver of 2-n-propyl-4-pentenoic acid, a metabolite of the antiepileptic drug valproic acid. Evidence for the formation of chemically reactive intermediates. Drug Metab. Dispos. 13 (1985) 81-96
28. Hautecler J.J., Sluse-Goffart C.M., Evens A., Duyckaerts C., and Sluse F.E. Effect of aspartate and glutamate on the oxoglutarate carrier investigated in rat heart mitochondria and inverted submitochondrial vesicles. Biochim. Biophys. Acta 1185 (1994) 153-159
29. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
30. Harmon H.J. Isolation of totally inverted submitochondrial particles by sonication of beef heart mitochondria. J. Bioenerg. Biomembr. 14 (1982) 377-386
31. King T.E. Preparation of succinate dehydrogenase and reconstitution of succinate oxidase. Method Enzymol. 10 (1967) 322-331
32. Perevucnik G., Schurtenberger P., Lasic D.D., and Hauser H. Size analysis of biological membrane vesicles by gel filtration, dynamic light scattering and electron microscopy. Biochim. Biophys. Acta 821 1 (1985) 169-173
33. Soveral G., Macey R.I., and Moura T.F. Water permeability of brush border membrane vesicles from kidney proximal tubule. J. Membr. Biol. 158 3 (1997) 219-228
34. Havelaar A.C., Mancini G.M.S., Beerens C.E.M.T., Souren R.M.A., and Verheijen F.W. Purification of the lysosomal sialic acid transporter. J. Biol. Chem. 273 51 (1998) 34568-34574
35. Hildyard J.C.W., Ammala C., Dukes I.D., Thomson S.A., and Halestrap A.P. Identification and characterization of a new class of highly specific and potent inhibitors of the mitochondrial pyruvate carrier. Biochim. Biophys. Acta 1707 (2005) 221-230
36. Halestrap A.P., and Price N.T. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 343 (1999) 281-299
37. Luís P.B.M., Ruiter J.P.N., Aires C.C.P., Soveral G., de Almeida I.T., Duran M., Wanders R.J.A., and Silva M.F.B. Valproic acid metabolites inhibit dihydrolipoyl dehydrogenase activity leading to impaired 2-oxoglutarate-driven oxidative phosphorylation. Biochim. Biophys. Acta 1767 (2007) 1126-1133
38. Valenti D., de Bari L., Atlante A., and Passarella S. l-Lactate transport into rat heart mitochondria and reconstruction of the l-lactate/pyruvate shuttle. Biochem. J. 364 Pt 1 (2002) 101-104
39. Passarella S., Atlante A., Valenti D., and de Bari L. The role of mitochondrial transport in energy metabolism. Mitochondrion 2 (2003) 319-343
40. De Bari L., Atlante A., Valenti D., and Passarella S. Partial reconstruction of in vitro gluconeogenesis arising from mitochondrial l-lactate uptake/metabolism and oxaloacetate export via novel l-lactate translocators. Biochem. J. 380 Pt. 1 (2004) 231-242
41. Becker C.M., and Harris R.A. Influence of valproic acid on hepatic carbohydrate and lipid metabolism. Arch. Biochem. Biophys. 223 (1983) 381-392
42. Rogiers V., Vandenberghe Y., and Vercruysse A. Inhibition of gluconeogenesis by sodium valproate and its metabolites in isolated rat hepatocytes. Xenobiotica 15 (1985) 759-765
43. Schmidt D. Adverse effects and interactions with other drugs. In: Löscher W. (Ed). Milestones in Drug Therapy-Valproate (1999), Birkhäuser Verlag, Basel 223-264
44. El-Khatib F., Rauchenzauner M., Lechleitner M., Hoppichler F., Naser A., Waldmann M., Trinka E., Unterberger I., Bauer G., and Luef G.J. Valproate, weight gain and carbohydrate craving: a gender study. Seizure 16 (2007) 226-232
45. Silva M.F.B., Aires C.C.P., Luis P.B.M., Ruiter J.P.N., IJlst L., Duran M., Wanders R.J.A., and de Almeida I.T. Valproic acid metabolism and its effects on mitochondrial fatty acid oxidation: a review. J. Inherit. Metab. Dis. 31 (2008) 205-216