Mitochondrial uncoupling proteins and energy metabolism

Frontiers in Physiology

Volumn 6, Issue FEB, 2015, Pages 36-

  Busiello, Rosa A ^a   Savarese, Sabrina ^b   Lombardi, Assunta ^c  

^a UNIVERSITY OF SANNIO   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Energy metabolism; Mitochondria; Obesity; Proton leak; Uncoupling protein

Indexed keywords

FATTY ACID; GLUCOSE; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 3;

BROWN ADIPOSE TISSUE; ENERGY BALANCE; ENERGY EXPENDITURE; ENERGY METABOLISM; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HUMAN; INSULIN RESISTANCE; LIPID METABOLISM; MISSENSE MUTATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PROTEIN TARGETING; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; THERMOGENESIS;

EID: 84926463276     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00036     Document Type: Short Survey

References (64)

1. Adams, S. H., Hoppel, C. L., Lok, K. H., Zhao, L., Wong, S. W., Minkler, P. E., et al. (2009). Plasma acylcarnitine profiles suggestincomplete long-chain fatty acid beta-oxidation and altered tricarboxylic acid cycleactivity in type 2 diabetic African-American women. J. Nutr. 139, 1073-1081. doi: 10.3945/jn.108.103754
2. 1 augments energy expenditure and glutathione content while mitigating ROS production. Am. J. Physiol. Endocrinol. Metab. 305, E405-E415. doi: 10.1152/ajpendo.00057
3. Aguer, C., Fiehn, O., Seifert, E. L., Bézaire, V., Meissen, J. K., Daniels, A., et al. (2013). Muscle uncoupling protein 3 overexpression mimics endurance training and reduces circulating biomarkers of incomplete ß-oxidation. FASEB J. 27, 4213-4225. doi: 10.1096/fj.13-234302
4. Argyropoulos, G., Brown, A. M., Willi, S. M., Zhu, J., He, Y., Reitman, M., et al. (1998). Effects of mutations in the human uncoupling protein 3 gene on the respiratory quotient and fat oxidation in severe obesity and type 2 diabetes. J. Clin. Invest. 102, 1345-1351. doi: 10.1172/JCI4115
5. Bartelt, A., Merkel, M., and Heeren, J. (2012). A new powerful player in lipoprotein metabolism: brown adipose tissue. J Mol. Med. (Berl.) 90, 887-893. doi: 10.1007/s00109-012-0858-3
6. Bezaire, V., Seifert, E. L., and Harper, M. E. (2007). Uncoupling protein-3: clues in an ongoing mitochondrial mystery. FASEB J. 21, 312-324. doi: 10.1096/fj.06-6966rev
7. Boss, O., Samec, S., Dulloo, A., Seydoux, J., Muzzin, P., and Giacobino, J. P. (1997). Uncoupling protein-3, a new member of the mitochondrialcarrier family with tissue specific expression. FEBS Lett. 408, 39-42.
8. 3. Cell Metab. 2, 85-93. doi: 10.1016/j.cmet.2005.06.002
9. Bukowiecki, L., Collet, A. J., Follea, N., Guay, G., and Jahjah, L. (1982). Brown adipose tissue hyperplasia: a fundamental mechanism of adaptation to cold and hyperphagia. Am. J. Physiol. 242, E353-E359.
10. 3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett. 462, 257-260. doi: 10.1016/S0014-5793(99)01540-9
11. Cannon, B., and Nedergard, J. (2004). Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359. doi: 10.1152/physrev.00015.2003
12. Carrière, A., Jeanson, Y., Berger-Müller, S., André, M., Chenouard, V., Arnaud, E., et al. (2014). Browning of white adipose cells by intermediate metabolites: an adaptive mechanism to alleviate redox pressure. Diabetes 63, 3253-3265. doi: 10.2337/db13-1885
13. Choi, C. S., Fillmore, J. J., Kim, J. K., Liu, Z. X., Kim, S., Collier, E. F., et al. (2007). Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J. Clin. Invest. 117, 1995-2003. doi: 10.1172/JCI13579
14. Cioffi, F., Senese, R., de Lange, P., Goglia, F., Lanni, A., and Lombardi, A. (2009). Uncoupling proteins: a complex journey to function discovery. Biofactors 35, 417-428. doi: 10.1002/biof.54
15. 3. Am. J. Physiol. Endocrinol. Metab. 295, E1018-E1024. doi: 10.1152/ajpendo.00779.2007
16. Costford, S. R., Chaudhry, S. N., Salkhordeh, M., and Harper, M. E. (2006). Effects of the presence, absence, and overexpression of uncoupling protein-3 on adiposity and fuel metabolism in congenic mice. Am. J. Physiol. Endocrinol. Metab. 290, E1304-E1312. doi: 10.1152/ajpendo.00401.2005
17. de Almeida Brondani, L., de Souza, B. M., Assmann, T. S., Bouças, A. P., Bauer, A. C., Canani, L. H., et al. (2014). Association of the UCP polymorphisms with susceptibility to obesity: case-control study and meta-analysis. Mol. Biol. Rep. 41, 5053-5067. doi: 10.1007/s11033-014-3371-7
18. Divakaruni, A. S., and Brand, M. D. (2011). The regulation and physiology of mitochondrial proton-leak. Physiology 26, 192-205. doi: 10.1152/physiol.00046.2010
19. Enerback, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M. E., et al. (1997). Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90-94. doi: 10.1038/387090a0
20. 1 Ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 9, 203-209. doi: 10.1016/j.cmet.2008.12.014
21. Fink, B. D., Herlein, J. A., Almind, K., Cinti, S., Kahn, C. R., and Sivitz, W. I. (2007). Mitochondrial proton-leak in obesity resistant and obesity-prone mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1773-R1780. doi: 10.1152/ajpregu.00478.2007
22. Goglia, F., and Skulachev, V. P. (2003). A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from the inner to the outer membrane leaflet. FASEB J. 17, 1585-1591. doi: 10.1096/fj.03-0159hyp
23. 1 is essential for adaptive adrenergic nonshivering thermogenesis. Am. J. Physiol. 291, E350-E357. doi: 10.1152/ajpendo.00387.2005
24. Gong, D. W., Monemdjou, S., Gavrilova, O., Leon, L. R., Marcus-Samuels, B., Chou, C. J., et al. (2000). Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncouplingprotein-3. J. Biol. Chem. 275, 16251-16257. doi: 10.1074/jbc.M910177199
25. Goodpaster, B. H., He, J., Watkins, S., and Kelley, D. E. (2001). Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J. Clin. Endocrinol. Metab. 86, 5755-5761. doi: 10.1210/jcem.86.12.8075
26. Harms, M., and Seale, P. (2013). Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19, 1252-1263. doi: 10.1038/nm.3361
27. Harper, M. E., Green, K., and Brand, M. D. (2008). The efficiency of cellular energy transduction and its implications for obesity. Annu. Rev. Nutr. 28, 13-33. doi: 10.1146/annurev.nutr.28.061807.155357
28. Herrmann, S. M., Wang, J. G., Staessen, J. A., Kertmen, E., and Schmidt-Petersen, K., Zidek, W., et al. (2003). Uncoupling protein 1 and 3 polymorphisms are associated with waist-to-hip ratio. J. Mol. Med. 81, 327-332. doi: 10.1007/s00109-003-0431-1
29. 1 genes associated with fat metabolism, obesity and diabetes. Mol. Biol. Rep. 37, 1513-1522. doi: 10.1007/s11033-009-9550-2
30. Keipert, S., Ost, M., Chadt, A., Voigt, A., Ayala, V., Portero-Otin, M., et al. (2013). Skeletal muscle uncoupling-induced longevity in mice is linked to increased substrate metabolism and induction of the endogenous antioxidant defense system. Am. J. Physiol. Endocrinol. Metab. 304, E495-E506. doi: 10.1152/ajpendo.00518.2012
31. Klaus, S., Keipert, S., Rossmeisl, M., and Kopecky, J. (2012). Augmenting energy expenditure by mitochondrial uncoupling: a role of AMP-activated protein kinase. Genes Nutr. 7, 369-386. doi: 10.1007/s12263-011-0260-8
32. Klingenberg, M., and Echtay, K. S. (2001). Uncoupling proteins: the issues from a biochemist point of view. Biochim. Biophys. Acta. 1504, 128-143. doi: 10.1016/S0005-2728(00)00242-5
33. Korshunov, S. S., Skulachev, V. P., and Starkov, A. A. (1997). High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416, 15-18. doi: 10.1016/S0014-5793(97)01159-9
34. Krauss, S., Zhang, C. Y. and Lowell, B. B. (2005). The mitochondrial uncoupling-protein homologues. Nat. Rev. Mol. Cell Biol. 6, 248-261. doi: 10.1038/nrm1592
35. 3 with body weight in type 2 diabetic patients. Int. J. Obes. (Lond). 38, 873-877. doi: 10.1038/ijo.2013.174
36. 3 gene with obesity phenotypes in Caucasian families. Physiol. Genomics 22, 197-203. doi: 10.1152/physiolgenomics.00031.2005
37. 3 Translocates lipid hydroperoxide and mediates lipid hydroperoxide-dependent mitochondrial uncoupling. J. Biol. Chem. 285, 16599-16605. doi: 10.1074/jbc.M110.102699
38. Lombardi, A., Grasso, P., Moreno, M., de Lange, P., Silvestri, E., Lanni, A., et al. (2008). Interrelated influence of superoxides and free fatty acids over mitochondrial uncoupling in skeletal muscle. Biochim. Biophys. Acta 1777, 826-833. doi: 10.1016/j.bbabio.2008.04.019
39. 3. J. Biol. Chem. 286, 21865-21875. doi: 10.1074/jbc.M111.240242
40. Meirhaeghe, A., Amouyel, P., Helbecque, N., Cottel, D., Otabe, S., Froguel, P., et al. (2000). An uncoupling protein 3 gene polymorphism associated with a lower risk of developing Type II diabetes and with atherogenic lipid profile in a French cohort. Diabetologia 43, 1424-1428. doi: 10.1007/s001250051549
41. Mensink, M., Hesselink, M. K., Borghouts, L. B., Keizer, H., Moonen-Kornips, E., Schaart, G., et al. (2007). Skeletal muscle uncoupling protein-3 restores upon intervention in the prediabetic and diabetic state: implications for diabetes pathogenesis? Diabetes Obes. Metab. 9, 594-596. doi: 10.1111/j.1463-1326.2006.00628.x
42. 3 gene variants associated with childhood obesity: effect on fatty acid oxidation and on prevention of triglyceride storage. Int. J. Obes. 36, 207-217. doi: 10.1038/ijo.2011.81
43. 3 overexpression on mitochondrial ROS production in skeletal muscle of young versus aged mice. FEBS Lett. 582, 4147-4152. doi: 10.1016/j.febslet.2008.11.016
44. Nabben, M., Hoeks, J., Moonen-Kornips, E., van Beurden, D., Briedé, J. J., Hesselink, M. K., et al. (2011). Significance of uncoupling protein 3 in mitochondrial function upon mid- and long-term dietary high-fat exposure. FEBS Lett. 585, 4010-4017. doi: 10.1016/j.febslet.2011.11.012
45. Nedergaard, J., Bengtsson, T., and Cannon, B. (2007). Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 293, E444-E452. doi: 10.1152/ajpendo.00691.2006
46. Ost, M., Werner, F., Dokas, J., Klaus, S., and Voigt, A. (2014). Activation of AMPKa2 is not crucial for mitochondrial uncoupling-induced metabolic effects but required to maintain skeletal muscle integrity. PLoS ONE 9:e94689. doi: 10.1371/journal.pone.0094689
47. Patti, M. E., and Corvera, S. (2010). The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr. Rev. 31, 364-395. doi: 10.1210/er.2009-0027
48. Peirce, V., and Vidal-Puig, A. (2013). Regulation of glucose homoeostasis by brown adipose tissue. Lancet Diabetes Endocrinol. 1, 353-360. doi: 10.1016/S2213-8587(13)70055-X
49. 1-containing adipocytes molecularly distinct from classic brown adipocytes. J. Biol. Chem. 285, 7153-7164. doi: 10.1074/jbc.M109.053942
50. Porter, R. K. (2008). Uncoupling protein 1: a short-circuit in the chemiosmotic process. J. Bioenerg. Biomembr. 40, 457-461. doi: 10.1007/s10863-008-9172-8
51. Rolfe, D. F. and Brand, M. D. (1996). Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am. J. Physiol. 271, C1380-C1389.
52. Saito, M. (2013). Brown adipose tissue as a therapeutic target for human obesity. Obes. Res. Clin. Pract. 7, e432-e438. doi: 10.1016/j.orcp.2013.09.001
53. Schrauwen, P., and Hesselink, M. K. (2004b). The role of uncoupling protein3 in fatty acid metabolism: protection against lipotoxicity? Proc. Nutr. Soc. 63, 287-292. doi: 10.1079/PNS2004336
54. Schrauwen, P., and Hesselink, M. K. C. (2004a). Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53, 1412-1417. doi: 10.2337/diabetes.53.6.1412
55. Schrauwen, P., Hesselink, M. K. C., Blaak, E. E., Borghouts, L. B., Schaart, G., Saris, W. H., et al. (2001). Uncoupling protein 3 content is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 50, 2870-2873. doi: 10.2337/diabetes.50.12.2870
56. 3mRNA expression and obesity in male non-diabetic Pima Indians. Int. J. Obes. Relat. Metab. Disord. 23, 1242-1245.
57. Senese, R., Valli, V., Moreno, M., Lombardi, A., Busiello, R. A., and Cioffi, F. (2011). Uncoupling protein 3 expression levels influence insulin sensitivity, fatty acid oxidation, and related signaling pathways. Pflugers Arch. 461, 153-164. doi: 10.1007/s00424-010-0892-3
58. 1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 5, 1196-1203. doi: 10.1016/j.celrep.2013.10.044
59. Son, C., Hosoda, K., Ishihara, K., Bevilacqua, L., Masuzaki, H., Fushiki, T., et al. (2004). Reduction of diet-induced obesity in transgenic mice overexpressing uncoupling protein 3 in skeletal muscle. Diabetologia 47, 47-54. doi: 10.1007/s00125-003-1272-8
60. van Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M., Kemerink, G. J., Bouvy, N. D., et al. (2009). Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500-1508. doi: 10.1056/NEJMoa0808718
61. Vidal-Puig, A. J., Grujic, D., Zhang, C. Y., Hagen, T., Boss, O., Ido, Y., et al. (2000). Energy metabolism in uncoupling protein 3 gene knockout mice. J. Biol. Chem. 275, 16258-16266. doi: 10.1074/jbc.M910179199
62. Vitali, A., Murano, I., Zingaretti, M. C., Frontini, A., Ricquier, D., and Cinti, S. (2012). The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes. J. Lipid Res. 53, 619-629. doi: 10.1194/jlr.M018846
63. Wu, J., Boström, P., Sparks, L. M., Ye, L., Choi, J. H., Giang, A. H., et al. (2012). Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376. doi: 10.1016/j.cell.2012.05.016
64. Wu, J., Cohen, P., and Spiegelman, B. M. (2013). Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev. 27, 234-250. doi: 10.1101/gad.211649.112.