Mitochondrial pyruvate import and its effects on homeostasis

Current Opinion in Cell Biology

Volumn 33, Issue , 2015, Pages 35-41

  Vanderperre, Benoît ^a   Bender, Tom ^a   Kunji, Edmund RS ^b   Martinou, Jean Claude ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PYRUVATE CARRIER; MONOCARBOXYLATE TRANSPORTER; UNCLASSIFIED DRUG; CARRIER PROTEIN; GLUCOSE; PYRUVATE TRANSPORT PROTEIN; PYRUVIC ACID;

CANCER CELL; CELL PROLIFERATION; CITRIC ACID CYCLE; CYTOSOL; ENERGY YIELD; GENETIC CODE; GLUCOSE BLOOD LEVEL; GLYCOLYSIS; HOMEOSTASIS; HUMAN; INNER MEMBRANE; INSULIN RELEASE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; ANIMAL; GENETICS; METABOLISM; MUTATION; NEOPLASM; PATHOLOGY;

ANIMALS; GLUCOSE; HOMEOSTASIS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MUTATION; NEOPLASMS; PYRUVIC ACID;

EID: 84918584476     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.10.008     Document Type: Review

References (43)

1. Gray L.R., Tompkins S.C., Taylor E.B. Regulation of pyruvate metabolism and human disease. Cell Mol Life Sci 2014, 71:2577-2604.
2. Palmieri F., Pierri C.L., De Grassi A., Nunes-Nesi A., Fernie A.R. Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J 2011, 66:161-181.
3. Bricker D.K., Taylor E.B., Schell J.C., Orsak T., Boutron A., Chen Y.C., Cox J.E., Cardon C.M., Van Vranken J.G., Dephoure N., et al. A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 2012, 337:96-100.
4. Herzig S., Raemy E., Montessuit S., Veuthey J.L., Zamboni N., Westermann B., Kunji E.R., Martinou J.C. Identification and functional expression of the mitochondrial pyruvate carrier. Science 2012, 337:93-96.
5. Schell J.C., Rutter J. The long and winding road to the mitochondrial pyruvate carrier. Cancer Metab 2013, 1. 6-3002-1-6.
6. Papa S., Francavilla A., Paradies G., Meduri B. The transport of pyruvate in rat liver mitochondria. FEBS Lett 1971, 12:285-288.
7. Halestrap A.P., Denton R.M. Specific inhibition of pyruvate transport in rat liver mitochondria and human erythrocytes by alpha-cyano-4-hydroxycinnamate. Biochem J 1974, 138:313-316.
8. Halestrap A.P. The mitochondrial pyruvate carrier. Kinetics and specificity for substrates and inhibitors. Biochem J 1975, 148:85-96.
9. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
10. Da Cruz S., Xenarios I., Langridge J., Vilbois F., Parone P.A., Martinou J.C. Proteomic analysis of the mouse liver mitochondrial inner membrane. J Biol Chem 2003, 278:41566-41571.
11. Sickmann A., Reinders J., Wagner Y., Joppich C., Zahedi R., Meyer H.E., Schonfisch B., Perschil I., Chacinska A., Guiard B., et al. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci U S A 2003, 100:13207-13212.
12. Schonauer M.S., Kastaniotis A.J., Kursu V.A., Hiltunen J.K., Dieckmann C.L. Lipoic acid synthesis and attachment in yeast mitochondria. J Biol Chem 2009, 284:23234-23242.
13. Crichton P.G., Harding M., Ruprecht J.J., Lee Y., Kunji E.R. Lipid, detergent, and Coomassie Blue G-250 affect the migration of small membrane proteins in blue native gels: mitochondrial carriers migrate as monomers not dimers. J Biol Chem 2013, 288:22163-22173.
14. Li C.L., Wang M., Ma X.Y., Zhang W. NRGA1, a putative mitochondrial pyruvate carrier, mediates ABA regulation of guard cell ion channels and drought stress responses in arabidopsis. Mol Plant 2014.
15. Timon-Gomez A., Proft M., Pascual-Ahuir A. Differential regulation of mitochondrial pyruvate carrier genes modulates respiratory capacity and stress tolerance in yeast. PLoS One 2013, 8:e79405.
16. Divakaruni A.S., Wiley S.E., Rogers G.W., Andreyev A.Y., Petrosyan S., Loviscach M., Wall E.A., Yadava N., Heuck A.P., Ferrick D.A., et al. Thiazolidinediones are acute, specific inhibitors of the mitochondrial pyruvate carrier. Proc Natl Acad Sci U S A 2013, 110:5422-5427.
17. Colca J.R., McDonald W.G., Cavey G.S., Cole S.L., Holewa D.D., Brightwell-Conrad A.S., Wolfe C.L., Wheeler J.S., Coulter K.R., Kilkuskie P.M., et al. Identification of a mitochondrial target of thiazolidinedione insulin sensitizers (mTOT)-relationship to newly identified mitochondrial pyruvate carrier proteins. PLoS One 2013, 8:e61551.
18. Du J., Cleghorn W.M., Contreras L., Lindsay K., Rountree A.M., Chertov A.O., Turner S.J., Sahaboglu A., Linton J., Sadilek M., et al. Inhibition of mitochondrial pyruvate transport by zaprinast causes massive accumulation of aspartate at the expense of glutamate in the retina. J Biol Chem 2013, 288:36129-36140.
19. Jezegou A., Llinares E., Anne C., Kieffer-Jaquinod S., O'Regan S., Aupetit J., Chabli A., Sagne C., Debacker C., Chadefaux-Vekemans B., et al. Heptahelical protein PQLC2 is a lysosomal cationic amino acid exporter underlying the action of cysteamine in cystinosis therapy. Proc Natl Acad Sci U S A 2012, 109:E3434-E3443.
20. Xu Y., Tao Y., Cheung L.S., Fan C., Chen L.Q., Xu S., Perry K., Frommer W.B., Feng L. Structures of bacterial homologues of SWEET transporters in two distinct conformations. Nature 2014, 10.1038/nature13670.
21. Jeoung N.H., Harris C.R., Harris R.A. Regulation of pyruvate metabolism in metabolic-related diseases. Rev Endocr Metab Disord 2014, 15:99-110.
22. Brivet M., Garcia-Cazorla A., Lyonnet S., Dumez Y., Nassogne M.C., Slama A., Boutron A., Touati G., Legrand A., Saudubray J.M. Impaired mitochondrial pyruvate importation in a patient and a fetus at risk. Mol Genet Metab 2003, 78:186-192.
23. Vigueira P.A., McCommis K.S., Schweitzer G.G., Remedi M.S., Chambers K.T., Fu X., McDonald W.G., Cole S.L., Colca J.R., Kletzien R.F., et al. Mitochondrial pyruvate carrier 2 hypomorphism in mice leads to defects in glucose-stimulated insulin secretion. Cell Rep 2014, 7:2042-2053.
24. Jensen M.V., Joseph J.W., Ronnebaum S.M., Burgess S.C., Sherry A.D., Newgard C.B. Metabolic cycling in control of glucose-stimulated insulin secretion. Am J Physiol Endocrinol Metab 2008, 295:E1287-E1297.
25. Prentki M., Matschinsky F.M., Madiraju S.R. Metabolic signaling in fuel-induced insulin secretion. Cell Metab 2013, 18:162-185.
26. Sugden M.C., Holness M.J. The pyruvate carboxylase-pyruvate dehydrogenase axis in islet pyruvate metabolism: going round in circles?. Islets 2011, 3:302-319.
27. Patterson J.N., Cousteils K., Lou J.W., Manning Fox J.E., MacDonald P.E., Joseph J.W. Mitochondrial metabolism of pyruvate is essential for regulating glucose-stimulated insulin secretion. J Biol Chem 2014, 289:13335-13346.
28. Colca J.R., VanderLugt J.T., Adams W.J., Shashlo A., McDonald W.G., Liang J., Zhou R., Orloff D.G. Clinical proof-of-concept study with MSDC-0160, a prototype mTOT-modulating insulin sensitizer. Clin Pharmacol Ther 2013, 93:352-359.
29. Wojtczak L. The Crabtree effect: a new look at the old problem. Acta Biochim Pol 1996, 43:361-368.
30. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
31. Crabtree H.G. Observations on the carbohydrate metabolism of tumours. Biochem J 1929, 23:536-545.
32. Hebert A.S., Dittenhafer-Reed K.E., Yu W., Bailey D.J., Selen E.S., Boersma M.D., Carson J.J., Tonelli M., Balloon A.J., Higbee A.J., et al. Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol Cell 2013, 49:186-199.
33. Deng W.J., Nie S., Dai J., Wu J.R., Zeng R. Proteome, phosphoproteome, and hydroxyproteome of liver mitochondria in diabetic rats at early pathogenic stages. Mol Cell Proteomics 2010, 9:100-116.
34. Warburg O. On respiratory impairment in cancer cells. Science 1956, 124:269-270.
35. Christofk H.R., Vander Heiden M.G., Harris M.H., Ramanathan A., Gerszten R.E., Wei R., Fleming M.D., Schreiber S.L., Cantley L.C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233.
36. Yang W., Lu Z. Regulation and function of pyruvate kinase M2 in cancer. Cancer Lett 2013, 339:153-158.
37. Filipp F.V. Cancer metabolism meets systems biology: pyruvate kinase isoform PKM2 is a metabolic master regulator. J Carcinog 2013, 12:14-3163. 115423. eCollection 2013.
38. Lewis B.C., Prescott J.E., Campbell S.E., Shim H., Orlowski R.Z., Dang C.V. Tumor induction by the c-Myc target genes rcl and lactate dehydrogenase A. Cancer Res 2000, 60:6178-6183.
39. Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006, 3:177-185.
40. Eboli M.L., Paradies G., Galeotti T., Papa S. Pyruvate transport in tumour-cell mitochondria. Biochim Biophys Acta 1977, 460:183-187.
41. Paradies G., Capuano F., Palombini G., Galeotti T., Papa S. Transport of pyruvate in mitochondria from different tumor cells. Cancer Res 1983, 43:5068-5071.
42. Atherton H.J., Dodd M.S., Heather L.C., Schroeder M.A., Griffin J.L., Radda G.K., Clarke K., Tyler D.J. Role of pyruvate dehydrogenase inhibition in the development of hypertrophy in the hyperthyroid rat heart: a combined magnetic resonance imaging and hyperpolarized magnetic resonance spectroscopy study. Circulation 2011, 123:2552-2561.
43. San Martin A., Ceballo S., Baeza-Lehnert F., Lerchundi R., Valdebenito R., Contreras-Baeza Y., Alegria K., Barros L.F. Imaging mitochondrial flux in single cells with a FRET sensor for pyruvate. PLoS One 2014, 9:e85780.