UCP1, the mitochondrial uncoupling protein of brown adipocyte: A personal contribution and a historical perspective

Biochimie

Volumn 134, Issue , 2017, Pages 3-8

  Ricquier, Daniel ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Brown adipose tissue; Membrane; Mitochondria; Mitochondrial transporter; Thermogenesis; UCP; Uncoupling

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; COMPLEMENTARY DNA; FATTY ACID; NUCLEOTIDE; POLYPEPTIDE; PROTON; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2;

AMINO ACID SEQUENCE; BROWN ADIPOCYTE; GENETIC TRANSCRIPTION; HISTORY OF MEDICINE; HUMAN; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PHOTOAFFINITY LABELING; PROTEIN ISOLATION; REVIEW; SYNTHESIS; THERMOGENESIS; ANIMAL; BROWN ADIPOSE TISSUE; CHICKEN; CYTOLOGY; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; HISTORY; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MUTATION; OBESITY; PATHOLOGY; PLANT;

ADIPOCYTES, BROWN; ADIPOSE TISSUE, BROWN; ANIMALS; CHICKENS; CLONING, MOLECULAR; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MUTATION; OBESITY; PLANTS; THERMOGENESIS; TRANSCRIPTION, GENETIC; UNCOUPLING PROTEIN 1;

EID: 85009810563     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2016.10.018     Document Type: Review

References (54)

1. [1] Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Lévi-Meyrueis, C., Bouillaud, F., Seldin, M.F., Surwitt, R.S., Ricquier, D., Warden, C.H., Uncoupling Protein-2: a new thermogenic protein and a new gene linked to obesity and hyperinsulism. Nat. Genet. 15 (1997), 269–272.
2. [2] Ricquier, D., Bouillaud, F., The uncoupling proteins. Biochem. J. 345 (2000), 161–179.
3. [3] Nedergaard, J., Ricquier, D., Kozak, L.P., Uncoupling proteins: current status and therapeutic prospects. EMBO Rep. 6 (2005), 917–921.
4. [4] Himms-Hagen, J., Brown adipose tissue thermogenesis and obesity. Prog. Lipid Res. 28 (1989), 67–115.
5. [5] Ricquier, D., Kozak, L.P., Uncoupling proteins. Bray, G., Bouchard, C., James, W.P.T., (eds.) Handbook of Obesity, 2009, Marcel Dekker, New York, 539–558.
6. [6] Cannon, B., Nedergaard, J., Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 (2004), 277–359.
7. [7] Nicholls, D.G., Locke, R.M., Thermogenic mechanisms in brown fat. Physiol. Rev. 64 (1984), 1–64.
8. [8] Ricquier, D., Gaillard, J.C., Turc, J.M., Microcalorimetry of isolated mitochondria from brown adipose tissue. Effect of guanine-diphosphate. FEBS Lett. 99 (1979), 203–206.
9. [9] D. Ricquier J.C. Kader, Mitochondrial protein alteration in active brown fat. A sodium dodecyl sulfate-polyacrylamide gel electrophoretic study, Biochem. Biophys. Res. Commun. 73(976) 577–583.
10. [10] Ricquier, D., Mory, G., Hémon, P., Changes induced by cold adaptation in the brown adipose tissue of several rodent species, with special reference to mitochondrial components. Can. J. Biochem. 57 (1979), 1261–1266.
11. [11] Lin, C.S., Klingenberg, M., Isolation of the uncoupling protein from broawn fat mitochondria. FEBS Lett. 113 (1980), 299–303.
12. [12] Ricquier, D., Gervais, C., Kader, J.C., Hémon, P., Partial purification by guanosine-5'-diphosphate-agarose affinity chromatography of the 32,000 molecular weight polypeptide from mitochondria of brown adipose tissue. FEBS Lett. 101 (1979), 35–38.
13. [13] Heaton, G.M., Wagenwoord, R.J., Kemp, A., Nicholls, D.G., Brown adipose tissue mitochondria: photoaffinity labelling of the regulatory site for energy dissipation. Eur. J. Biochem. 82 (1978), 515–521.
14. [14] Ricquier, D., Lin, C.S., Klingenberg, M., Isolation of the GDP binding protein from brown adipose tissue mitochondria of several animals and amino acid composition study in rat. Biochem. Biophys. Res. Commun. 106 (1982), 582–589.
15. [15] Klingenberg, M., Winkler, E., The reconstituted isolated uncoupling protein is a membrane potential driven H+ translocator. EMBO J. 4 (1985), 3087–3092.
16. [16] Ricquier, D., Barlet, J.P., Garel, J.M., Combes-George, M., Dubois, M.P., An immunological study of the uncoupling protein of brown adipose tissue mitochondria. Biochem. J. 210 (1983), 859–866.
17. [17] Bouillaud, F., Ricquier, D., Thibault, J., Weissenbach, Molecular approach to thermogenesis in brown adipose tissue: cDNA cloning of the mitochondrial uncoupling protein. Proc. Natl. Acad. Sci. U. S. A. 82 (1985), 445–448.
18. [18] Ricquier, D., Mory, G., Bouillaud, F., Thibault, J., Weissenbach, J., Rapid increase of mitochondrial uncoupling protein and its mRNA in stimulated brown adipose tissue. Use of a cDNA probe. FEBS Lett. 178 (1984), 240–244.
19. [19] Aquila, H., Link, T.A., Klingenberg, M., The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. Analysis of sequence homologies and of folding of the protein in the membrane. EMBO J. 9 (1985), 2369–2376.
20. [20] Bouillaud, F., Weissenbach, J., Ricquier, D., Complete cDNA-derived aminoacid sequence of rat brown fat uncoupling protein. J. Biol. Chem. 261 (1986), 1487–1490.
21. [21] Casteilla, L., Blondel, O., Klaus, S., Raimbault, S., Diolez, P., Moreau, F., Bouillaud, F., Ricquier, Stable expression of functional mitochondrial uncoupling protein in Chinese hamster ovary cells. Proc. Natl. Acad. Sci. U. S. A. 87 (1990), 5124–5128.
22. [22] Klaus, S., Casteilla, L., Bouillaud, F., Raimbault, S., Ricquier, D., Expression of the brown fat mitochondria uncoupling protein in Xenopus oocytes and import into mitochondrial membrane. Biochem. Biophys. Res. Commun. 167 (1990), 784–789.
23. [23] Arechaga, I., Raimbault, S., Prieto, S., Lévi-Meyrueis, C., Zaragoza, P., Miroux, B., Ricquier, D., Bouillaud, F., Rial, E., Cysteine residues are not essential for uncoupling protein function. Biochem. J. 296 (1993), 693–700.
24. [24] Bouillaud, F., Arechaga, I., Petit, P.X., Lévi-Meyrueis, C., Casteilla, L., Laurent, M., Rial, E., Ricquier, D., A sequence related to a DNA recognition element is essential for the inhibition by nucleotides of the proton transport through the mitochondrial uncoupling protein. EMBO J. 13 (1994), 1990–1997.
25. [25] Gonzalez-Barroso, M., Fleury, C., Ricquier, D., Bouillaud, F., Rial, E., Activation of the UCP by Fatty acids is modulated by mutation of the protein. Eur. J. Biochem. 239 (1996), 445–450.
26. [26] Enerbäck, S., Jacobsson, A., Simpson, E.M., Guerra, C., Yamashita, H., Harper, M.E., Kozak, L.P., Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387 (1995), 90–94.
27. [27] Miroux, B., Casteilla, L., Klaus, S., Raimbault, S., Grandin, S., Clément, J.M., Ricquier, D., Bouillaud, F., Antibodies selected from whole antiserum by fusion proteins as tools for the study of the topology of mitochondrial membrane proteins - evidence that the N-terminal extremity of the 6th alpha-helix of the uncoupling protein is facing the matrix. J. Biol. Chem. 267 (1992), 13603–13609.
28. [28] Miroux, B., Frossard, V., Raimbault, S., Ricquier, D., Bouillaud, F., The topology of the brown adipose tissue mitochondrial uncoupling protein determined with antibodies against its antigenic sites revealed by a library of fusion proteins. EMBO J. 12 (1993), 3739–3745.
29. [29] Bouillaud, F., Raimbault, S., Ricquier, D., The gene for rat uncoupling protein: complete sequence, structure of primary transcript and evolutionary relationship between exons. Biochem. Biophys. Res. Commun. 157 (1988), 783–792.
30. [30] Cassard, A.M., Bouillaud, F., Mattei, M.G., Hentz, E., Raimbault, S., Thomas, M., Ricquier, D., Human uncoupling protein gene: structure, comparison with rat gene and assignment to the long arm of the chromosome 4. J. Cell. Biochem. 43 (1990), 255–264.
31. [31] Ricquier, D., Bouillaud, F., Toumelin, P., Mory, G., Bazin, R., Arch, J., Pénicaud, L., Expression of uncoupling protein mRNA in thermogenic or weakly thermogenic brown adipose tissue. Evidence for a rapid ß-adrenoceptor-mediated and transcriptionally regulated step during activation of thermogenesis. J. Biol. Chem. 261 (1986), 13905–13910.
32. [32] Cassard-Doulcier, A.M., Gelly, C., Fox, N., Schrementi, J., Raimbault, S., Klaus, S., Forest, C., Bouillaud, F., Ricquier, D., Tissue-specific and ß-adrenergic regulation of the mitochondrial uncoupling protein gene - control by cis-acting elements in the 5'-flanking region. Mol. Endocrinol. 7 (1993), 497–506.
33. [33] Cassard-Doulcier, A.M., Gelly, C., Bouillaud, F., Ricquier, D., The 211-bp enhancer of the rat UCP-1 gene controls specific and regulated expression in the brown adipose tissue. Biochem. J. 333 (1998), 243–246.
34. [34] Cassard-Doulcier, A.M., Larose, M., Matamala, J.C., Champigny, O., Bouillaud, F., Ricquier, D., In vitro interactions between nuclear proteins and uncoupling protein gene promoter reveal several putative trans-activating factors including Ets1, Retinoid X Receptor, Thyroid hormone Receptor and a NCACCC box-binding protein. J. Biol. Chem. 269 (1994), 24335–24342.
35. [35] Larose, M., Cassard-Doulcier, A.M., Fleury, C., Serra, F., Champigny, O., Bouillaud, F., Ricquier, D., Essential cis-acting elements in rat uncoupling protein gene are in the enhancer. Delineation of a complex element mediating the transcriptional activation by retinoic acid. J. Biol. Chem. 271 (1996), 31533–31542.
36. [36] Oppert, J.M., Vohl, M.C., Chagnon, M., Dionne, F.T., Cassard-Doulcier, A.M., Ricquier, D., Pérusse, L., Bouchard, C., cDNA polymorphism in the uncoupling protein (ucp) gene and human body fat. Intern. J. Obes. 18 (1994), 526–531.
37. [37] Cassard-Doulcier, A.M., Bouillaud, F., Chagnon, M., Gelly, C., Dionne, F.T., Oppert, J.M., Bouchard, C., Chagnon, Y., Ricquier, D., The Bcl I polymorphism of the human uncoupling protein (ucp) gene is due to a point mutation in the 5’ -flanking region. Intern. J. Obes. 20 (1996), 278–279.
38. [38] 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., 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 (1998), 34611–34615.
39. [39] Haguenauer, A., Raimbault, S., Masscheleyn, S., Gonzalez-Barroso, M.M., Criscuolo, F., Plamondon, J., Miroux, B., Ricquier, D., Richard, D., Bouillaud, F., Pecqueur, C., A new renal mitochondrial carrier, KMCP1, is up-regulated during tubular cell regeneration and induction of antioxidant enzymes. J. Biol. Chem. 280 (2005), 22036–22043.
40. [40] Raimbault, S., Dridi, S., Denjean, F., Lachuer, J., Couplan, E., Bouillaud, F., Bordas, F., Duchamp, C., Taouis, M., Ricquier, D., An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem. J. 353 (2001), 441–444.
41. [41] Laloi, M., Klein, M., Riesmeier, J.W., Fleury, C., Bouillaud, F., Ricquier, D., A plant cold-induced uncoupling protein. Nature 389 (1997), 135–136.
42. [42] Ricquier, D., Néchad, M., Mory, G., Ultrastructural and biochemical characterization of human brown adipose tissue in pheochromocytoma. J. Clin. Endocrinol. Metab. 54 (1982), 805–807.
43. [43] Bouillaud, F., Combes-George, M., Ricquier, D., Mitochondria of adult human brown adipose t issue contain a 32000-Mr uncoupling protein. Biosci. Rep. 3 (1983), 775–780.
44. [44] Champigny, O., Ricquier, D., Evidence from in vitro differentiating cells that adrenoceptot agonists can increase uncoupling protein mRNA level in adipocytes of adult humans. J. Lip. Res. 37 (1996), 1907–1914.
45. [45] Garruti, G., Ricquier, D., Analysis of uncoupling protein and its mRNA in adipose tissue deposits of adult humans. Int. J. Obes. 16 (1992), 383–390.
46. [46] Kortelainen, M.L., Pelletier, G., Ricquier, D., Bukowiecki, L.J., Immunohistochemical detection of human brown adipose tissue uncoupling protein in an autopsy series. J. Histochem. Cytochem 41 (1993), 759–764.
47. [47] Bouillaud, F., Ricquier, D., Gulik-Krzywicki, J., Gary-Bobo, C.M., The possible proton translocating activity of the mitochondrial uncoupling protein. Reconstitution studies in liposomes. FEBS Lett. 164 (1983), 272–276.
48. [48] Cinti, S., Zancanaro, C., Sbarbati, A., Cigolini, M., Vogel, P., Fakan, S., Ricquier, D., Immuno- cytochemical ultrastructural identification of the uncoupling protein in brown adipose tissue mitochondria. Biol. Cell 67 (1989), 359–362.
49. [49] Ricquier, D., Thibault, J., Bouillaud, F., Kuster, Y., Molecular approach to thermogenesis in brown adipose tissue. Cell-free translation of mRNA and characterization of the mitochondrial uncoupling protein. J. Biol. Chem. 258 (1983), 6675–6677.
50. [50] Champigny, O., Ricquier, D., Blondel, O., Mayers, R.M., Briscoe, M.G., Holloway, B.R., ß3- adrenoceptor stimulation restores message and expression of brown-fat mitochondrial uncoupling protein in adult dogs. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 10774–10777.
51. [51] Champigny, O., Holloway, B.R., Ricquier, D., Regulation of UCP gene expression in brown adipocytes differentiated in primary culture - effects of a new ß-adrenoceptor agonist. Mol. Cell. Endocrinol. 86 (1992), 73–82.
52. [52] Klaus, S., Muzzin, P., Revelli, J.P., Cawthorne, M.A., Giacobino, J.P., Ricquier, D., Control of ß-3 adrenergic receptor expression in brown adipocytes in culture. Mol. Cell. Endocr. 109 (1995), 189–195.
53. [53] Gonzalez-Barroso, M.M., Pecqueur, C., Gelly, C., Sanchis, D., Alvez-Guerra, M.C., Bouillaud, F., Cassard-Doulcier, Ricquier A.M., Transcriptional activation of the human UCP1 gene: synergism of retinoids, isoproterenol and thiazolidinedione is mediated by a multipartite response element. J. Biol. Chem. 275 (2000), 31722–31732.
54. [54] Rial, E., Gonzalez-Barroso, M.M., Fleury, C., Iturrizaga, S., Sanchis, D., Jimenez-Jimenez, J., Ricquier, D., Bouillaud, F., Retinoids activate proton transport by the uncoupling proteins UCP1 and UCP2. EMBO J. 18 (1999), 5827–5833.