Control of mitochondrial pH by uncoupling protein 4 in astrocytes promotes neuronal survival

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31014-31028

  Lambert, Hélène Perreten ^a   Zenger, Manuel ^a   Azarias, Guillaume ^c   Chatton, Jean Yves ^c   Magistretti, Pierre J ^a,b,d   Lengacher, Sylvain ^a,d  

^a EPFL   (Switzerland)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d Center for Psychiatric Neuroscience Lausanne   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CARBON DIOXIDE; METABOLISM; MITOCHONDRIA; OXYGEN; PATHOLOGY; PROTEINS;

ELECTRICAL POTENTIAL; METABOLIC PARAMETERS; METABOLIC RESPONSE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION RATE; REACTIVE OXYGEN SPECIES; TRANSMEMBRANE TRANSFER; UNCOUPLING PROTEINS;

NEURONS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE; GLUTAMIC ACID; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 4; UNCOUPLING PROTEIN 5; CALCEIN; CARRIER PROTEIN; FLUORESCEIN DERIVATIVE; GLUCOSE; HYDROGEN PEROXIDE; LACTIC ACID DERIVATIVE; UCP4 PROTEIN, MOUSE;

ACIDIFICATION; AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN MITOCHONDRION; BRAIN OXYGEN CONSUMPTION; CELL PH; CELL SURVIVAL; CITRIC ACID CYCLE; CONTROLLED STUDY; EMBRYO; ENERGY YIELD; GLYCOLYSIS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NEWBORN; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; CHEMISTRY; COCULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HUMAN; METABOLISM; MITOCHONDRION; NERVE CELL; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PH; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; CARBON DIOXIDE; CELL SURVIVAL; COCULTURE TECHNIQUES; FLUORESCEINS; GENE EXPRESSION REGULATION; GLUCOSE; GLYCOLYSIS; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; LACTATES; MEMBRANE TRANSPORT PROTEINS; MICE; MITOCHONDRIA; NEURONS; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION;

EID: 84909953899     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570879     Document Type: Article

References (46)

1. Nicholls, D. G., Bernson, V. S., and Heaton, G. M. (1978) The identification of the component in the inner membrane of brown adipose tissue mitochondria responsible for regulating energy dissipation. Experientia Suppl. 32, 89-93
2. Kozak, L. P., Britton, J. H., Kozak, U. C., and Wells, J. M. (1988) The mitochondrial uncoupling protein gene. Correlation of exon structure to transmembrane domains. J. Biol. Chem. 263, 12274-12277
3. Bouillaud, F., Raimbault, S., and Ricquier, D. (1988) The gene for rat uncoupling protein: complete sequence, structure of primary transcript and evolutionary relationship between exons. Biochem. Biophys. Res. Commun. 157, 783-792
4. Horvath, T. L., Warden, C. H., Hajos, M., Lombardi, A., Goglia, F., and Diano, S. (1999) Brain uncoupling protein 2: uncoupled neuronal mitochondria predict thermal synapses in homeostatic centers. J. Neurosci. 19, 10417-10427
5. Arsenijevic, D., Onuma, H., Pecqueur, C., Raimbault, S., Manning, B. S., Miroux, B., Couplan, E., Alves-Guerra, M. C., Goubern, M., Surwit, R., Bouillaud, F., Richard, D., Collins, S., and Ricquier, D. (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat. Genet. 26, 435-439
6. Boss, O., Bobbioni-Harsch, E., Assimacopoulos-Jeannet, F., Muzzin, P., Munger, R., Giacobino, J. P., and Golay, A. (1998) Uncoupling protein-3 expression in skeletal muscle and free fatty acids in obesity. Lancet 351, 1933
7. Boss, O., Samec, S., Kühne, F., Bijlenga, P., Assimacopoulos-Jeannet, F., Seydoux, J., Giacobino, J. P., and Muzzin, P. (1998) Uncoupling protein-3 expression in rodent skeletal muscle is modulated by food intake but not by changes in environmental temperature. J. Biol. Chem. 273, 5-8
8. Alán, L., Smolková, K., Kronusová, E., Santorová, J., and Jezek, P. (2009) Absolute levels of transcripts for mitochondrial uncoupling proteins UCP2, UCP3, UCP4, and UCP5 show different patterns in rat and mice tissues. J. Bioenerg. Biomembr. 41, 71-78
9. Yu, X. X., Mao, W., Zhong, A., Schow, P., Brush, J., Sherwood, S. W., Adams, S. H., and Pan, G. (2000) Characterization of novel UCP5/BMCP1 isoforms and differential regulation of UCP4 and UCP5 expression through dietary or temperature manipulation. FASEB J. 14, 1611-1618
10. Liu, D., Chan, S. L., de Souza-Pinto, N. C., Slevin, J. R., Wersto, R. P., Zhan, M., Mustafa, K., de Cabo, R., and Mattson, M. P. (2006) Mitochondrial UCP4 mediates an adaptive shift in energy metabolism and increases the resistance of neurons to metabolic and oxidative stress. Neuromolecular Med. 8, 389-414
11. Wu, Z., Zhang, J., and Zhao, B. (2009) Superoxide anion regulates the mitochondrial free Ca2+ through uncoupling proteins. Antioxid. Redox Signal. 11, 1805-1818
12. Bélanger, M., Allaman, I., and Magistretti, P. J. (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14, 724-738
13. Sanchis, D., Fleury, C., Chomiki, N., Goubern, M., Huang, Q., Neverova, M., Grégoire, F., Easlick, J., Raimbault, S., Lévi-Meyrueis, C., Miroux, B., Collins, S., Seldin, M., Richard, D., Warden, C., Bouillaud, F., and Ricquier, D. (1998) BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast. J. Biol. Chem. 273, 34611-34615
14. Mao, W., Yu, X. X., Zhong, A., Li, W., Brush, J., Sherwood, S. W., Adams, S. H., and Pan, G. (1999) UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett. 443, 326-330
15. Chan, S. L., Liu, D., Kyriazis, G. A., Bagsiyao, P., Ouyang, X., and Mattson, M. P. (2006) Mitochondrial uncoupling protein-4 regulates calcium homeostasis and sensitivity to store depletion-induced apoptosis in neural cells. J. Biol. Chem. 281, 37391-37403
16. Smorodchenko, A., Rupprecht, A., Sarilova, I., Ninnemann, O., Bräuer, A. U., Franke, K., Schumacher, S., Techritz, S., Nitsch, R., Schuelke, M., and Pohl, E. E. (2009) Comparative analysis of uncoupling protein 4 distribution in various tissues under physiological conditions and during development. Biochim. Biophys. Acta 1788, 2309-2319
17. Kim-Han, J. S., Reichert, S. A., Quick, K. L., and Dugan, L. L. (2001) BMCP1: a mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production. J. Neurochem. 79, 658-668
18. Pichiule, P., Chavez, J. C., and LaManna, J. C. (2003) Oxygen and oxidative stress modulate the expression of uncoupling protein-5 in vitro and in vivo. Adv. Exp. Med. Biol. 540, 103-107
19. Huang, P. S., Son, J. H., Abbott, L. C., and Winzer-Serhan, U. H. (2011) Regulated expression of neuronal SIRT1 and related genes by aging and neuronal β2-containing nicotinic cholinergic receptors. Neuroscience 196, 189-202
20. Azarias, G., Perreten, H., Lengacher, S., Poburko, D., Demaurex, N., Magistretti, P. J., and Chatton, J. Y. (2011) Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes. J. Neurosci. 31, 3550-3559
21. Pellerin, L., and Magistretti, P. J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. U.S.A. 91, 10625-10629
22. Sorg, O., and Magistretti, P. J. (1992) Vasoactive intestinal peptide and noradrenaline exert long-term control on glycogen levels in astrocytes: blockade by protein synthesis inhibition. J. Neurosci. 12, 4923-4931
23. Allaman, I., Pellerin, L., and Magistretti, P. J. (2004) Glucocorticoids modulate neurotransmitter-induced glycogen metabolism in cultured cortical astrocytes. J. Neurochem. 88, 900-908
24. Smiley, S. T., Reers, M., Mottola-Hartshorn, C., Lin, M., Chen, A., Smith, T. W., Steele, G. D., Jr., and Chen, L. B. (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. U.S.A. 88, 3671-3675
25. Reers, M., Smith, T. W., and Chen, L. B. (1991) J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480-4486
26. Zhou, M., Diwu, Z., Panchuk-Voloshina, N., and Haugland, R. P. (1997) A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem. 253, 162-168
27. Haskew-Layton, R. E., Payappilly, J. B., Smirnova, N. A., Ma, T. C., Chan, K. K., Murphy, T. H., Guo, H., Langley, B., Sultana, R., Butterfield, D. A., Santagata, S., Alldred, M. J., Gazaryan, I. G., Bell, G. W., Ginsberg, S. D., and Ratan, R. R. (2010) Controlled enzymatic production of astrocytic hydrogen peroxide protects neurons from oxidative stress via an Nrf2-independent pathway. Proc. Natl. Acad. Sci. U.S.A. 107, 17385-17390
28. Zerez, C. R., Lee, S. J., and Tanaka, K. R. (1987) Spectrophotometric determination of oxidized and reduced pyridine nucleotides in erythrocytes using a single extraction procedure. Anal. Biochem. 164, 367-373
29. Allaman, I., Gavillet, M., Belanger, M., Laroche, T., Viertl, D., Lashuel, H. A., and Magistretti, P. J. (2010) Amyloid-β aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability. J. Neurosci. 30, 3326-3338
30. Demaurex, N., and Poburko, D. (2009) Modulation of mitochondrial proton gradients by the plasma membrane calcium ATPase. J. Physiol. Sci. 59, (Suppl. 1) 348
31. + dynamics in mouse cortical astrocytes: implications for cellular bioenergetics. Eur. J. Neurosci. 12, 3843-3853
32. Rosenberg, J. C., and Rush, B. F. (1966) An enzymatic-spectrophotometric determination of pyruvic and lactic acid in blood. Methodologic aspects. Clin. Chem. 12, 299-307
33. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
34. Lengacher, S., Magistretti, P. J., and Pellerin, L. (2004) Quantitative rt-PCR analysis of uncoupling protein isoforms in mouse brain cortex: methodological optimization and comparison of expression with brown adipose tissue and skeletal muscle. J. Cereb. Blood Flow Metab. 24, 780-788
35. Bittar, P. G., Charnay, Y., Pellerin, L., Bouras, C., and Magistretti, P. J. (1996) Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J. Cereb. Blood Flow Metab. 16, 1079-1089
36. Pellerin, L., Pellegri, G., Bittar, P. G., Charnay, Y., Bouras, C., Martin, J. L., Stella, N., and Magistretti, P. J. (1998) Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev. Neurosci. 20, 291-299
37. Jezek, P., Zácková, M., Ru˚zicka, M., Skobisová, E., and Jabu˚rek, M. (2004) Mitochondrial uncoupling proteins: facts and fantasies. Physiol. Res. 53, S199-S211
38. Magistretti, P. J., Pellerin, L., Rothman, D. L., and Shulman, R. G. (1999) Energy on demand. Science 283, 496-497
39. Pellerin, L., and Magistretti, P. J. (2004) Neuroscience. Let there be (NADH) light. Science 305, 50-52
40. Lee, Y., Morrison, B. M., Li, Y., Lengacher, S., Farah, M. H., Hoffman, P. N., Liu, Y., Tsingalia, A., Jin, L., Zhang, P. W., Pellerin, L., Magistretti, P. J., and Rothstein, J. D. (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487, 443-448
41. Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., and Alberini, C. M. (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144, 810-823
42. Nicholls, D. G., and Locke, R. M. (1984) Thermogenic mechanisms in brown fat. Physiol. Rev. 64, 1-64
43. Ricquier, D. (2006) Fundamental mechanisms of thermogenesis. C. R. Biol. 329, 578-586; discussion 653-575
44. Andrews, Z. B., Diano, S., and Horvath, T. L. (2005) Mitochondrial uncoupling proteins in the CNS: in support of function and survival. Nat. Rev. Neurosci. 6, 829-840
45. de la Monte, S. M., and Wands, J. R. (2006) Molecular indices of oxidative stress and mitochondrial dysfunction occur early and often progress with severity of Alzheimer's disease. J. Alzheimers Dis. 9, 167-181
46. Szolnoki, Z., Kondacs, A., Mandi, Y., Bodor, A., and Somogyvari, F. (2009) A homozygous genetic variant of mitochondrial uncoupling protein 4 exerts protection against the occurrence of multiple sclerosis. Neuromolecular Med. 11, 101-105