Mitochondrial uncoupling proteins in the central nervous system

Antioxidants and Redox Signaling

Volumn 7, Issue 9-10, 2005, Pages 1173-1181

  Kim Han, Jeong Sook ^a   Dugan, Laura L ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KAINIC ACID; MESSENGER RNA; MITOCHONDRIAL PROTEIN; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 4; UNCOUPLING PROTIEN 5;

BROWN ADIPOSE TISSUE; ELECTRON TRANSPORT; GENE EXPRESSION; GENE OVEREXPRESSION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NEUROPROTECTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SEQUENCE HOMOLOGY; THERMOGENESIS; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; CARRIER PROTEINS; CENTRAL NERVOUS SYSTEM; HUMANS; ION CHANNELS; ISCHEMIA; KAINIC ACID; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; OPEN READING FRAMES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; UNCOUPLING AGENTS; UP-REGULATION;

EID: 24144475250     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.1173     Document Type: Review

References (87)

1. Agardh CD, Chapman AG, Pelligrino D, and Siesjo BK. Influence of severe hypoglycemia on mitochondrial and plasma membrane function in rat brain. J Neurochem 38: 662-668, 1982.
2. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R, Bouillaud F, Richard D, Collins S, and Ricquier D. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26: 435-439, 2000.
3. Bathgate B, Freebairn EM, Greenland AJ, and Reid GA. Functional expression of the rat brown adipose tissue uncoupling protein in Saccharomyces cerevisiae. Mol Microbiol 6: 363-370, 1992.
4. Bazan NG Jr. Effects of ischemia and electroconvulsive shock on free fatty acid pool in the brain. Biochim Biophys Acta 218: 1-10, 1970.
5. Bechmann I, Diano S, Warden CH, Bartfai T, Nitsch R, and Horvath TL. Brain mitochondrial uncoupling protein 2 (UCP2): a protective stress signal in neuronal injury. Biochem Pharmacol 64: 363-367, 2002.
6. Ben-Ari Y and Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23: 580-587, 2000.
7. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, and Harper ME. Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Endocrinol Metab 286: E852-E861, 2004.
8. Bouillaud F, Couplan E, Pecqueur C, and Ricquier D. Homologues of the uncoupling protein from brown adipose tissue (UCP1): UCP2, UCP3, BMCP1 and UCP4. Biochim Biophys Acta 1504: 107-119, 2001.
9. Boyer BB, Barnes BM, Lowell BB, and Grujic D. Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels. Am J Physiol 175: R1232-R1238, 1998.
10. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, and Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 37: 755-767, 2004.
11. Brookes PS, Levonen AL, Shiva S, Sarti P, and Darley-Usmar VM. Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Mead 33: 755-764, 2002.
12. Busquets S, Alvarez B, Van Royen M, Figueras MT, Lopez-Soriano FJ, and Argiles JM. Increased uncoupling protein-2 gene expression in brain of lipopolysaccharide-injected mice: role of tumour necrosis factor-alpha? Biochim Biophys Acta 1499: 249-256, 2001.
13. Cadenas E, Boveris A, Ragan CI, and Stoppani AO. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180: 248-257, 1977.
14. Cannon B and Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359, 2004.
15. Casteilla L, Rigoulet M, and Penicaud L. Mitochondrial ROS metabolism: modulation by uncoupling proteins. IUBMB Life 52: 181-188, 2001.
16. Chen Z and Lash LH. Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J Pharmacol Exp Ther 285: 608-618, 1998.
17. Clavel S, Paradis E, Ricquier D, and Richard D. Kainic acid upregulates uncoupling protein-2 mRNA expression in the mouse brain. Neuroreport 14: 2015-2017, 2003.
18. Couplan E, del Mar Gonzalez-Barroso M, Alves-Guerra MC, Ricquier D, Goubern M, and Bouillaud F. No evidence for a basal, retinoic, or superoxide-induced uncoupling activity of the uncoupling protein 2 present in spleen or lung mitochondria. J Biol Chem 277: 26268-26275, 2002.
19. de Bilbao F, Arsenijevic D, Vallet P, Hjelle OP, Ottersen OP, Bouras C, Raffin Y, Abou K, Langhans W, Collins S, Plamondon J, Alves-Guerra MC, Haguenauer A, Garcia I, Richard D, Ricquier D, and Giannakopoulos P. Resistance to cerebral ischemic injury in UCP2 knockout mice: evidence for a role of UCP2 as a regulator of mitochondrial glutathione levels. J Neurochem 89: 1283-1292, 2004.
20. Dejean L, Camara Y, Sibille B, Solanes G, and Villarroya F. Uncoupling protein-3 sensitizes cells to mitochondrial-dependent stimulus of apoptosis. J Cell Physiol 201: 294-304, 2004.
21. Diano S, Matthews RT, Patrylo P, Yang L, Beal MF, Barnstable CJ, and Horvath TL. Uncoupling protein 2 prevents neuronal death including that occurring during seizures: a mechanism for preconditioning. Endocrinology 144: 5014-5021, 2003.
22. Duval C, Negre-Salvayre A, Dogilo A, Salvayre R, Penicaud L, and Casteilla L. Increased reactive oxygen species production with antisense oligonucleotides directed against uncoupling protein 2 in murine endothelial cells. Biochem Cell Biol 80: 757-764, 2002.
23. Ealey KN, El-Sohemy A, and Archer MC. Effects of dietary conjugated linoleic acid on the expression of uncoupling proteins in mice and rats. Lipids 37: 853-861, 2002.
24. Echtay KS, Winkler E, and Klingenberg M. Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature 408: 609-613, 2000.
25. + transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone). Proc Natl Acad Sci U S A 98: 1416-1421, 2001.
26. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, and Brand MD. Superoxide activates mitochondrial uncoupling proteins. Nature 415: 96-99, 2002.
27. Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, Portero-Otin M, Pamplona R, Vidal-Puig AJ, Wang S, Roebuck SJ, and Brand MD. A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J 22: 4103-4110, 2003.
28. Emerit J, Edeas M, and Bricaire F. Neurodegenerative diseases and oxidative stress. Biomed Pharmacother 58: 39-46, 2004.
29. Esteves TC, Echtay KS, Jonassen T, Clarke CF, and Brand MD. Ubiquinone is not required for proton conductance by uncoupling protein 1 in yeast mitochondria. Biochem J 379: 309-315, 2004.
30. Finkel T. Reactive oxygen species and signal transduction. IUBMB Life 52: 3-6, 2001.
31. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 15: 247-254, 2003.
32. Forman HJ, Fukuto JM, and Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol 287: C246-C256, 2004.
33. Fridell YW, Sanchez-Blanco A, Silvia BA, and Helfand SL. Functional characterization of a Drosophila mitochondrial uncoupling protein. J Bioenerg Biomembr 36: 219-228, 2004.
34. Garlid KD, Jaburek M, Jezek P, and Varecha M. How do uncoupling proteins uncouple? Biochim Biophys Acta 1459: 383-389, 2000.
35. Gonzalez-Barroso MM, Fleury C, Arechaga I, Zaragoza P, Levi-Meyrueis C, Raimbault S, Ricquier D, Bouillaud F, and Rial E. Activation of the uncoupling protein by fatty acids is modulated by mutations in the C-terminal region of the protein. Eur J Biochem 239: 445-450, 1996.
36. Hillered L and Chan PH. Role of arachidonic acid and other free fatty acids in mitochondrial dysfunction in brain ischemia. J Neurosci Res 20: 451-456, 1988.
37. Hioki C, Yoshida T, Kogure A, Takakura Y, Umekawa T, Yoshioka K, Shimatsu A, and Yoshikawa T. Effects of growth hormone (GH) on mRNA levels of uncoupling proteins 1, 2, and 3 in brown and white adipose tissues and skeletal muscle in obese mice. Horm Metab Res 36: 607-613, 2004.
38. Horvath B, Spies C, Horvath G, Kox WJ, Miyamoto S, Barry S, Warden CH, Bechmann I, Diano S, Heemskerk J, and Horvath TL. Uncoupling protein 2 (UCP2) lowers alcohol sensitivity and pain threshold. Biochem Pharmacol 64: 369-374, 2002.
39. Horvath TL, Warden CH, Hajos M, Lombardi A, Goglia F, and Diano S. Brain uncoupling protein 2: uncoupled neuronal mitochondria predict thermal synapses in homeostatic centers. J Neurosci 19: 10417-10427, 1999.
40. Horvath TL, Diano S, and Barnstable C. Mitochondrial uncoupling protein 2 in the central nervous system: neuromodulator and neuroprotector. Biochem Pharmacol 65: 1917-1921, 2003.
41. Horvath TL, Diano S, Leranth C, Garcia-Segura LM, Cowley MA, Shanabrough M, Elsworth JD, Sotonyi P, Roth RH, Dietrich EH, Matthews RT, Barnstable CJ, and Redmond DE Jr. Coenzyme Q induces nigral mitochondrial uncoupling and prevents dopamine cell loss in a primate model of Parkinson's disease. Endocrinology 144: 2757-2760, 2003.
42. Jaburek M and Garlid KD. Reconstitution of recombinant uncoupling proteins: UCP1, -2, and -3 have similar affinities for ATP and are unaffected by coenzyme Q10. J Biol Chem 278: 25825-25831, 2003.
43. Jakus PB, Sipos K, Kispal G, and Sandor A. Opposite regulation of uncoupling protein 1 and uncoupling protein 3 in vivo in brown adipose tissue of cold-exposed rats. FEBS Lett 519: 210-214, 2002.
44. Jezek P, Zackova M, Ruzicka M, Skobisova E, and Jaburek M. Mitochondrial uncoupling proteins-facts and fantasies. Physiol Res 53 Suppl 1: S199-S211, 2004.
45. Kim-Han JS, Reichert SA, Quick KL, and Dugan LL. BMCP1: a mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production. J Neurochem 79: 658-668, 2001.
46. Klein NA, Houmard BS, Hansen KR, Woodruff TK, Sluss PM, Bremner WJ, and Soules MR. Age-related analysis of inhibin A, inhibin B, and activin a relative to the intercycle monotropic follicle-stimulating hormone rise in normal ovulatory women. J Clin Endocrinol Metab 89: 2977-2981, 2004.
47. Klingenberg M. Uncoupling protein-a useful energy dissipator. J Bioenerg Biomembr 31: 419-430, 1999.
48. Kondou S, Hidaka S, Yoshimatsu H, Tsuruta Y, Itateyama E, and Sakata T. Molecular cloning of rat brain mitochondrial carrier protein-1 cDNA and its up-regulation during postnatal development. Biochim Biophys Acta 1457: 182-189, 2000.
49. Korshunov SS, Skulachev VP, and Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15-18, 1997.
50. Krauss S, Zhang CY, Scorrano L, Dalgaard LT, St-Pierre J, Grey ST, and Lowell BB. Superoxide-mediated activation of uncoupling protein 2 causes pancreatic beta cell dysfunction. J Clin Invest 112: 1831-1842, 2003.
51. Kunz WS, Goussakov IV, Beck H, and Elger CE. Altered mitochondrial oxidative phosphorylation in hippocampal slices of kainate-treated rats. Brain Res 826: 236-242, 1999.
52. Kuwashima J, Nakamura K, Fujitani B, Kadokawa T, Yoshida K, and Shimizu M. Relationship between cerebral energy failure and free fatty acid accumulation following prolonged brain ischemia. Jpn J Pharmacol 28: 277-287, 1978.
53. Lazarewicz JW, Strosznajder J, and Gromek A. Effects of ischemia and exogenous fatty acids on the energy metabolism in brain mitochondria. Bull Acad Pol Sci Biol 20: 599-606, 1972.
54. Ledesma A, de Lacoba MG, and Rial E. The mitochondrial uncoupling proteins. Genome Biol 3: 3015, 2002.
55. Lengacher S, Magistretti PJ, and Pellerin L. 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, 2004.
56. Li G, Klein RL, Matheny M, King MA, Meyer EM, and Scarpace PJ. Induction of uncoupling protein 1 by central interleukin-6 gene delivery is dependent on sympathetic innervation of brown adipose tissue and underlies one mechanism of body weight reduction in rats. Neuroscience 115: 879-889, 2002.
57. MacManus JP, Graber T, Luebbert C, Preston E, Rasquinha I, Smith B, and Webster J. Translation-state analysis of gene expression in mouse brain after focal ischemia. J Cereb Blood Flow Metab 24: 657-667, 2004.
58. Mao W, Yu XX, Zhong A, Li W, Brush J, Sherwood SW, Adams SH, and Pan G. UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett 443: 326-330, 1999.
59. Mattiasson G, Shamloo M, Gido G, Mathi K, Tomasevic G, Yi S, Warden CH, Castilho RF, Melcher T, Gonzalez-Zulueta M, Nikolich K, and Wieloch T. Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat Med 9: 1062-1068, 2003.
60. Mills EM, Xu D, Fergusson MM, Combs CA, Xu Y, and Finkel T. Regulation of cellular oncosis by uncoupling protein 2. J Biol Chem 277: 27385-27392, 2002.
61. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Natunvissenschaften 191: 144-148, 1961.
62. Miwa S and Brand MD. Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. Biochem Soc Trans 31: 1300-1301, 2003.
63. Negre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Penicaud L, and Casteilla L. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11: 809-815, 1997.
64. Nicholls DG, Snelling R, and Rial E. Proton and calcium circuits across the mitochondrial inner membrane. Biochem Soc Trans 12: 388-390, 1984.
65. Nicholls DG, Vesce S, Kirk L, and Chalmers S. Interactions between mitochondrial bioenergetics and cytoplasmic calcium in cultured cerebellar granule cells. Cell Calcium 34: 407-424, 2003.
66. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, and Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790, 2000.
67. Palmieri F. The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 447: 689-709, 2004.
68. Paradis E, Clavel S, Bouillaud F, Ricquier D, and Richard D. Uncoupling protein 2: a novel player in neuroprotection. Trends Mol Med 9: 522-525, 2003.
69. Pecqueur C, Alves-Guerra MC, Gelly C, Levi-Meyrueis C, Couplan E, Collins S, Ricquier D, Bouillaud F, and Miroux B. Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J Biol Chem 276: 8705-8712, 2001.
70. Phillis JW and O'Regan MH. A potentially critical role of phospholipases in central nervous system ischemic, traumatic, and neurodegenerative disorders. Brain Res Brain Res Rev 44: 13-47, 2004.
71. Pichiule P, Chavez JC, and LaManna JC. Oxygen and oxidative stress modulate the expression of uncoupling protein-5 in vitro and in vivo. Adv Exp Med Biol 540: 103-107, 2003.
72. Richard D, Rivest R, Huang Q, Bouillaud F, Sanchis D, Champigny O, and Ricquier D. Distribution of the uncoupling protein 2 mRNA in the mouse brain. J Comp Neurol 397: 549-560, 1998.
73. Richard D, Clavel S, Huang Q, Sanchis D, and Ricquier D. Uncoupling protein 2 in the brain: distribution and function. Biochem Soc Trans 29: 812-817, 2001.
74. Sanchis D, Fleury C, Chomiki N, Goubern M, Huang Q, Neverova M, Gregoire F, Easlick J, Raimbault S, Levi-Meyrueis C, Miroux B, Collins S, Seldin M, Richard D, Warden C, Bouillaud F, and Ricquier D. 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, 1998.
75. Sivitz WI, Fink BD, and Donohoue PA. Fasting and leptin modulate adipose and muscle uncoupling protein: divergent effects between messenger ribonucleic acid and protein expression. Endocrinology 140: 1511-1519, 1999.
76. Skulachev VP. Uncoupling: new approaches to an old problem of bioenergetics. Biochim Biophys Acta 1363: 100-124, 1998.
77. Smith AM, Ratcliffe RG, and Sweetlove LJ. Activation and function of mitochondrial uncoupling protein in plants. J Biol Chem 279: 51944-51952, 2004.
78. Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, and Brand MD. Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3: 87-95, 2004.
79. Stephenson D, Rash K, Smalstig B, Roberts E, Johnstone E, Sharp J, Panetta J, Little S, Kramer R, and Clemens J. Cytosolic phospholipase A2 is induced in reactive glia following different forms of neurodegeneration. Glia 27: 110-128, 1999.
80. Sullivan PG, Rippy NA, Dorenbos K, Concepcion RC, Agarwal AK, and Rho JM. The ketogenic diet increases mitochondrial uncoupling protein levels and activity. Ann Neurol 55: 576-580, 2004.
81. Takahashi Y, Kushiro M, Shinohara K, and Ide T. Dietary conjugated linoleic acid reduces body fat mass and affects gene expression of proteins regulating energy metabolism in mice. Comp Biochem Physiol B Biochem Mol Biol 133: 395-404, 2002.
82. Talbot DA, Lambert AJ, and Brand MD. Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. FEBS Lett 556: 111-115, 2004.
83. Vincent AM, Olzmann JA, Brownlee M, Sivitz WI, and Russell JW. Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 53: 726-734, 2004.
84. Watanabe A and Hirai A. Two uncoupling protein genes of rice (Oryza sativa L.): molecular study reveals the defects in the pre-mRNA processing for the heat-generating proteins of the subtropical cereal. Planta 215: 90-100, 2002.
85. Yamada S, Isojima Y, Yamatodani A, and Nagai K. Uncoupling protein 2 influences dopamine secretion in PC12h cells. J Neurochem 87: 461-469, 2003.
86. Zackova M, Skobisova E, Urbankova E, and Jezek P. Activating omega-6 polyunsaturated fatty acids and inhibitory purine nucleotides are high affinity ligands for novel mitochondrial uncoupling proteins UCP2 and UCP3. J Biol Chem 278: 20761-20769, 2003.
87. Zhang CY, Baffy G, Perret P, Krauss S, Peroni O, Grujic D, Hagen T, Vidal-Puig AJ, Boss O, Kim YB, Zheng XX, Wheeler MB, Shulman GI, Chan CB, and Lowell BB. Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105: 745-755, 2001.