Inhibition of mitochondrial pyruvate transport by Zaprinast causes massive accumulation of aspartate at the expense of glutamate in the retina

Journal of Biological Chemistry

Volumn 288, Issue 50, 2013, Pages 36129-36140

  Du, Jianhai ^a   Cleghorn, Whitney M ^a   Contreras, Laura ^b   Lindsay, Ken ^a   Rountree, Austin M ^c   Chertov, Andrei O ^a   Turner, Sally J ^a   Sahaboglu, Ayse ^d   Linton, Jonathan ^a   Sadilek, Martin ^c   Satruśtegui, Jorgina ^b   Sweet, Ian R ^c   Paquet Durand, François ^d   Hurley, James B ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF WASHINGTON   (United States)

^d Centre for Ophthalmology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID METABOLISM; BRAIN MITOCHONDRIA; COMPLETE OXIDATION; LIVER MITOCHONDRIA; METABOLIC EFFECTS; METABOLIC PROFILES; PHOSPHODIESTERASE ACTIVITY; PHOSPHODIESTERASE INHIBITORS;

AMINO ACIDS; BIOCHEMISTRY; ESTERS; GLUCOSE; METABOLISM; MODEL PREDICTIVE CONTROL;

MITOCHONDRIA;

ASPARTIC ACID; GLUTAMIC ACID; PYRUVIC ACID; ZAPRINAST;

AMINO ACID METABOLISM; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CELL TRANSPORT; CONTROLLED STUDY; LIVER MITOCHONDRION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RETINA;

ASPARTATE; GLUTAMATE; METABOLISM; PHOSPHODIESTERASES; PYRUVATE; RETINA;

ANIMALS; ASPARTIC ACID; BIOLOGICAL TRANSPORT; BRAIN; CITRIC ACID CYCLE; GLUTAMIC ACID; METABOLOMICS; MICE; MITOCHONDRIA; NEURONS; OXYGEN; PURINONES; PYRUVIC ACID; RETINA;

EID: 84890345210     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.507285     Document Type: Article

References (49)

1. 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., Redin, C., Boudina, S., Gygi, S. P., Brivet, M., Thummel, C. S., and Rutter, J. (2012) A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 337, 96-100
2. Herzig, S., Raemy, E., Montessuit, S., Veuthey, J. L., Zamboni, N., Westermann, B., Kunji, E. R., and Martinou, J. C. (2012) Identification and functional expression of the mitochondrial pyruvate carrier. Science 337, 93-96
3. Brivet, M., Garcia-Cazorla, A., Lyonnet, S., Dumez, Y., Nassogne, M. C., Slama, A., Boutron, A., Touati, G., Legrand, A., and Saudubray, J. M. (2003) Impaired mitochondrial pyruvate importation in a patient and a fetus at risk. Mol. Genet. Metab. 78, 186-192
4. Halestrap, A. P. (1975) The mitochondrial pyruvate carrier. Kinetics and specificity for substrates and inhibitors. Biochem. J. 148, 85-96
5. 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., Gracheva, E., Korshunova, Y., Trusgnich, M., Karr, R., Wiley, S. E., Divakaruni, A. S., Murphy, A. N., Vigueira, P. A., Finck, B. N., and Kletzien, R. F. (2013) Identification of a mitochondrial target of thiazolidinedione insulin sensitizers (mTOT). Relationship to newly identified mitochondrial pyruvate carrier proteins. PloS ONE 8, e61551
6. 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., Henry, R. R., McDonald, W. G., Colca, J. R., Simon, M. I., Ciaraldi, T. P., and Murphy, A. N. (2013) Thiazolidinediones are acute, specific inhibitors of the mitochondrial pyruvate carrier. Proc. Natl. Acad. Sci. U.S.A. 110, 5422-5427
7. Hildyard, J. C., Ammälä, C., Dukes, I. D., Thomson, S. A., and Halestrap, A. P. (2005) Identification and characterisation of a new class of highly specific and potent inhibitors of the mitochondrial pyruvate carrier. Biochim. Biophys. Acta 1707, 221-230
8. Gillespie, P. G., and Beavo, J. A. (1989) Inhibition and stimulation of photoreceptor phosphodiesterases by dipyridamole and M&B 22,948. Mol. Pharmacol. 36, 773-781
9. Thompson, W. J. (1991) Cyclic nucleotide phosphodiesterases. Pharmacology, biochemistry, and function. Pharmacol. Ther. 51, 13-33
10. Gibson, A. (2001) Phosphodiesterase 5 inhibitors and nitrergic transmission-from zaprinast to sildenafil. Eur. J. Pharmacol. 411, 1-10
11. Turko, I. V., Francis, S. H., and Corbin, J. D. (1998) Potential roles of conserved amino acids in the catalytic domain of the cGMP-binding cGMP-specific phosphodiesterase. J. Biol. Chem. 273, 6460-6466
12. Francis, S. H., Blount, M. A., and Corbin, J. D. (2011) Mammalian cyclic nucleotide phosphodiesterases. Molecular mechanisms and physiological functions. Physiol. Rev. 91, 651-690
13. Zhang, X., Feng, Q., and Cote, R. H. (2005) Efficacy and selectivity of phosphodiesterase-targeted drugs in inhibiting photoreceptor phosphodiesterase (PDE6) in retinal photoreceptors. Invest. Ophthalmol. Vis. Sci. 46, 3060-3066
14. McLaughlin, M. E., Ehrhart, T. L., Berson, E. L., and Dryja, T. P. (1995) Mutation spectrum of the gene encoding the β subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 92, 3249-3253
15. Chang, B., Grau, T., Dangel, S., Hurd, R., Jurklies, B., Sener, E. C., Andreasson, S., Dollfus, H., Baumann, B., Bolz, S., Artemyev, N., Kohl, S., Heckenlively, J., and Wissinger, B. (2009) A homologous genetic basis of the murine cpfl1 mutant and human achromatopsia linked to mutations in the PDE6C gene. Proc. Natl. Acad. Sci. U.S.A. 106, 19581-19586
16. Huang, S. H., Pittler, S. J., Huang, X., Oliveira, L., Berson, E. L., and Dryja, T. P. (1995) Autosomal recessive retinitis pigmentosa caused by mutations in the α subunit of rod cGMP phosphodiesterase. Nat. Genet. 11, 468-471
17. Bowes, C., Li, T., Danciger, M., Baxter, L. C., Applebury, M. L., and Farber, D. B. (1990) Retinal degeneration in the rd mouse is caused by a defect in the β subunit of rod cGMP-phosphodiesterase. Nature 347, 677-680
18. Chang, B., Hawes, N. L., Hurd, R. E., Davisson, M. T., Nusinowitz, S., and Heckenlively, J. R. (2002) Retinal degeneration mutants in the mouse. Vis. Res. 42, 517-525
19. Paquet-Durand, F., Beck, S., Michalakis, S., Goldmann, T., Huber, G., Mühlfriedel, R., Trifunovi, D., Fischer, M. D., Fahl, E., Duetsch, G., Becirovic, E., Wolfrum, U., van Veen, T., Biel, M., Tanimoto, N., and Seeliger, M. W. (2011) A key role for cyclic nucleotide gated (CNG) channels in cGMP-related retinitis pigmentosa. Hum. Mol. Genet. 20, 941-947
20. Hüttl, S., Michalakis, S., Seeliger, M., Luo, D. G., Acar, N., Geiger, H., Hudl, K., Mader, R., Haverkamp, S., Moser, M., Pfeifer, A., Gerstner, A., Yau, K. W., and Biel, M. (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J. Neurosci. 25, 130-138
21. Jalil, M. A., Begum, L., Contreras, L., Pardo, B., Iijima, M., Li, M. X., Ramos, M., Marmol, P., Horiuchi, M., Shimotsu, K., Nakagawa, S., Okubo, A., Sameshima, M., Isashiki, Y., Del Arco, A., Kobayashi, K., Satrústegui, J., and Saheki, T. (2005) Reduced N-acetylaspartate levels in mice lacking aralar, a brain- and muscle-type mitochondrial aspartate-glutamate carrier. J. Biol. Chem. 280, 31333-31339
22. Chertov, A. O., Holzhausen, L., Kuok, I. T., Couron, D., Parker, E., Linton, J. D., Sadilek, M., Sweet, I. R., and Hurley, J. B. (2011) Roles of glucose in photoreceptor survival. J. Biol. Chem. 286, 34700-34711
23. Millard, P., Letisse, F., Sokol, S., and Portais, J. C. (2012) IsoCor. Correcting MS data in isotope labeling experiments. Bioinformatics 28, 1294-1296
24. van Winden, W. A., Wittmann, C., Heinzle, E., and Heijnen, J. J. (2002) Correcting mass isotopomer distributions for naturally occurring isotopes. Biotechnol. Bioeng. 80, 477-479
25. Frezza, C., Cipolat, S., and Scorrano, L. (2007) Organelle isolation. Functional mitochondria from mouse liver, muscle, and cultured fibroblasts. Nat. Protoc. 2, 287-295
26. Sweet, I. R., Cook, D. L., Lernmark, A., Greenbaum, C. J., Wallen, A. R., Marcum, E. S., Stekhova, S. A., and Krohn, K. A. (2004) Systematic screening of potential β-cell imaging agents. Biochem. Biophys. Res. Commun. 314, 976-983
27. Janke, R., Genzel, Y., Wahl, A., and Reichl, U. (2010) Measurement of key metabolic enzyme activities in mammalian cells using rapid and sensitive microplate-based assays. Biotechnol. Bioeng. 107, 566-581
28. Zeevalk, G. D., and Nicklas, W. J. (2000) Lactate prevents the alterations in tissue amino acids, decline in ATP, and cell damage due to aglycemia in retina. J. Neurochem. 75, 1027-1034
29. Biel, M., and Michalakis, S. (2009) Cyclic nucleotide-gated channels. Handb. Exp. Pharmacol. 191, 111-136
30. Taniguchi, Y., Tonai-Kachi, H., and Shinjo, K. (2006) Zaprinast, a well-known cyclic guanosine monophosphate-specific phosphodiesterase inhibitor, is an agonist for GPR35. FEBS Lett. 580, 5003-5008
31. Guo, J., Williams, D. J., Puhl, H. L., 3rd, and Ikeda, S. R. (2008) Inhibition of N-type calcium channels by activation of GPR35, an orphan receptor, heterologously expressed in rat sympathetic neurons. J. Pharmacol. Exp. Ther. 324, 342-351
32. Wang, J., Simonavicius, N., Wu, X., Swaminath, G., Reagan, J., Tian, H., and Ling, L. (2006) Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. J. Biol. Chem. 281, 22021-22028
33. Mackenzie, A. E., Lappin, J. E., Taylor, D. L., Nicklin, S. A., and Milligan, G. (2011) GPR35 as a novel therapeutic target. Front. Endocrinol. 2, 68
34. Metallo, C. M., Gameiro, P. A., Bell, E. L., Mattaini, K. R., Yang, J., Hiller, K., Jewell, C. M., Johnson, Z. R., Irvine, D. J., Guarente, L., Kelleher, J. K., Vander Heiden, M. G., Iliopoulos, O., and Stephanopoulos, G. (2012) Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 481, 380-384
35. Pardo, B., Rodrigues, T. B., Contreras, L., Garzón, M., Llorente-Folch, I., Kobayashi, K., Saheki, T., Cerdan, S., and Satrústegui, J. (2011) Brain glutamine synthesis requires neuronal-born aspartate as amino donor for glial glutamate formation. J. Cereb. Blood Flow Metab. 31, 90-101
36. Fiermonte, G., Palmieri, L., Todisco, S., Agrimi, G., Palmieri, F., and Walker, J. E. (2002) Identification of the mitochondrial glutamate transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms. J. Biol. Chem. 277, 19289-19294
37. Sahaboglu, A., Tanimoto, N., Kaur, J., Sancho-Pelluz, J., Huber, G., Fahl, E., Arango-Gonzalez, B., Zrenner, E., Ekström, P., Löwenheim, H., Seeliger, M., and Paquet-Durand, F. (2010) PARP1 gene knock-out increases resistance to retinal degeneration without affecting retinal function. PloS ONE 5, e15495
38. Vallazza-Deschamps, G., Cia, D., Gong, J., Jellali, A., Duboc, A., Forster, V., Sahel, J. A., Tessier, L. H., and Picaud, S. (2005) Excessive activation of cyclic nucleotide-gated channels contributes to neuronal degeneration of photoreceptors. Eur. J. Neurosci. 22, 1013-1022
39. Sahaboglu, A., Paquet-Durand, O., Dietter, J., Dengler, K., Bernhard-Kurz, S., Ekström, P. A., Hitzmann, B., Ueffing, M., and Paquet-Durand, F. (2013) Retinitis pigmentosa. Rapid neurodegeneration is governed by slow cell death mechanisms. Cell Death Dis. 4, e488
40. Martínez-Fernández de la Cámara, C., Sequedo, M. D., Gómez-Pinedo, U., Jaijo, T., Aller, E., García-Tárraga, P., García-Verdugo, J. M., Millán, J. M., and Rodrigo, R. (2013) Phosphodiesterase inhibition induces retinal degeneration, oxidative stress, and inflammation in cone-enriched cultures of porcine retina. Exp. Eye Res. 111, 122-133
41. Romijn, H. J. (1988) Development and advantages of serum-free, chemically defined nutrient media for culturing of nerve tissue. Biol. Cell 63, 263-268
42. Proudlove, M. O., Beechey, R. B., and Moore, A. L. (1987) Pyruvate transport by thermogenic-tissue mitochondria. Biochem. J. 247, 441-447
43. Halestrap, A. P., and Denton, R. M. (1975) The specificity and metabolic implications of the inhibition of pyruvate transport in isolated mitochondria and intact tissue preparations by α-cyano-4-hydroxycinnamate andrelated compounds. Biochem. J. 148, 97-106
44. Butterworth, R. F., Merkel, A. D., and Landreville, F. (1982) Regional amino acid distribution in relation to function in insulin hypoglycaemia. J. Neurochem. 38, 1483-1489
45. Sandberg, M., Nyström, B., and Hamberger, A. (1985) Metabolically derived aspartate. Elevated extracellular levels in vivo in iodoacetate poisoning. J. Neurosci. Res. 13, 489-495
46. 2+-dependentrelease of aspartate and glutamate from hippocampal slices with changing glucose concentrations. Synapse 1, 265-272
47. Yudkoff, M., Nelson, D., Daikhin, Y., and Erecińska, M. (1994) Tricarboxylic acid cycle in rat brain synaptosomes. Fluxes and interactions with aspartate aminotransferase and malate/aspartate shuttle. J. Biol. Chem. 269, 27414-27420
48. Peng, L., Gu, L., Zhang, H., Huang, X., Hertz, E., and Hertz, L. (2007) Glutamine as an energy substrate in cultured neurons during glucose deprivation. J. Neurosci. Res. 85, 3480-3486
49. LaNoue, K. F., Berkich, D. A., Conway, M., Barber, A. J., Hu, L. Y., Taylor, C., and Hutson, S. (2001) Role of specific aminotransferases in de novo glutamate synthesis and redox shuttling in the retina. J. Neurosci. Res. 66, 914-922