Role of the transmembrane potential in the membrane proton leak

Biophysical Journal

Volumn 98, Issue 8, 2010, Pages 1503-1511

  Rupprecht, Anne ^a   Sokolenko, Elena A ^a   Beck, Valeri ^b,e   Ninnemann, Olaf ^b   Jaburek, Martin ^c   Trimbuch, Thorsten ^b   Klishin, Sergey S ^d   Jezek, Petr ^c   Skulachev, Vladimir P ^d   Pohl, Elena E ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e Bi MS Beck   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77951649660     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.12.4301     Document Type: Article

References (84)

1. Nicholls, D. G. 2001. A history of UCP1, Biochem. Soc. Trans. 29: 751-755.
2. Nedergaard, J., V. Golozoubova, ...,B. Cannon. 2001. UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim. Biophys. Acta. 1504:82-106. (Pubitemid 32179660)
3. Skulachev, V. P. 1998. Uncoupling: new approaches to an old problem of bioenergetics. Biochim. Biophys. Acta. 1363:100-124. (Pubitemid 28129344)
4. Dlasková, A., L. Hlavatá, and P. Jezek. 2008. Oxidative stress caused by blocking of mitochondrial complex I. H(+) pumping as a link in aging/ disease vicious cycle. Int. J. Biochem. Cell Biol. 40:1792-1805.
5. Brand, M. D., C. Affourtit, N. Parker. 2004. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic. Biol. Med. 37:755-767. (Pubitemid 39078548)
6. Rousset, S., M. C. Alves-Guerra, ..., D. Ricquier. 2004. The biology of mitochondrial uncoupling proteins. Diabetes. 53:130-135.
7. Horvath, T. L., S. Diano, and C. Barnstable. 2003. Mitochondrial uncoupling protein 2 in the central, nervous system: neuromodulator and neuroprotector. Biochem. Pharmacol. 65:1917-1921. (Pubitemid 36629575)
8. Nedergaard, J., and B. Cannon. 2003. The 'novel' 'uncoupling' proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp. Physiol. 88:65-84. (Pubitemid 36150060)
9. Krauss, S., C. Y. Zhang, and B. B. Lowell. 2005. The mitochondrial uncoupling-protein homologues. Nat. Rev. Mol. Cell Biol. 6:248-261.
10. Brown, G. C., and M. D. Brand. 1991. On the nature of the mitochondrial proton leak. Biochim. Biophys. Acta. 1059:55-62.
11. Porter, R. K., A. J. Hulbert, and M. D. Brand. 1996. Allometry of mitochondrial proton leak.: influence of membrane surface area and fatty acid composition. Am. J. Physiol. 271:R1550-R1560.
12. Brand, M. D., J. L. Pakay,..., E. J. Cornwall. 2005. The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem. J. 392:353-362.
13. Andreyev, A. Yu., T. O. Bondareva, ..., N. I. polkov. 1988. Carboxya- tractylate inhibits the uncoupling effect of free fatty acids. FEBS Lett. 226:265-269.
14. Andreyev, A. Yu., T. O. Bondareva, ..., T. V. Vygodina. 1989. The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur. J. Biochem. 182:585-592.
15. Cadenas, S., J. A. Buckingham, ..., M. D. Brand. 2000. AMP decreases the efficiency of skeletal-muscle mitochondria. Biochem. J. 351: 307-311.
16. Echtay, K. S., T. C. Esteves, ..., M. D. Brand. 2003. A signaling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22:4103-4110. (Pubitemid 37021739)
17. Shabalina, I. G., E. C. Backlund, ..., J. Nedergaard. 2008. Within brown-fat cells, UCP1-mediated fatty acid-induced uncoupling is independent of fatty acid metabolism. Biochim. Biophys. Acta. 1777: 642-650.
18. Klingenberg, M., and K. S. Echtay. 2001. Uncoupling proteins: the issues from a biochemist point of view. Biochim. Biophys. Acta. 1504:128-143. (Pubitemid 32179663)
19. Jabůrek, M., M. Varecha, ..., K. D. Garlid. 1999. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J. Biol. Chem. 274:26003-26007. (Pubitemid 129520020)
20. Urbánková, E., A. Voltchenko, E. E. Pohl. 2003. Transport kinetics of uncoupling proteins. Analysis of UCP1 reconstituted in planar lipid bilayers. J. Biol. Chem. 278:32497-32500. (Pubitemid 37055686)
21. Beck, V., M. Jabůrek, ..., E. E. Pohl. 2006. A new automated technique for the reconstitution of hydrophobic proteins into planar bilayer membranes. Studies of human recombinant uncoupling protein 1. Biochim. Biophys. Acta. 1757:474-479.
22. Beck, V., M. Jabůrek, ..., E. E. Pohl. 2007. Polyunsaturated fatty acids activate human uncoupling proteins 1 and 2 in planar lipid bilayers. FASEBJ. 21:1137-1144.
23. Nicholls, D. G., and R. M. Locke. 1984. Thermogenic mechanisms in brown fat. Physiol. Rev. 64:1-64.
24. Grav, H. J., J. I. Pedersen, and E. N. Christiansen. 1970. Conditions in vitro which affect respiratory control and capacity for respirationlinked phosphorylation in brown, adipose tissue mitochondria. Eur. J. Biochem, 12:11-23.
25. Echtay, K. S., E. Winkler, and M. Klingenberg. 2000. Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature. 408:609-613.
26. Echtay, K. S., D. Roussel,..., M. D. Brand. 2002. Superoxide activates mitochondrial uncoupling proteins. Nature. 415:96-99. (Pubitemid 34062457)
27. Shabalina, I. G., N. Petrovic, ..., J. Nedergaard. 2006. UCPl and defense against oxidative stress. 4-Hydroxy-2-nonenal effects on brown fat mitochondria are uncoupling protein 1-independent. J. Biol. Chem. 281:13882-13893.
28. Silva, J. P., I. G. Shabalina, ..., N. G. Larsson. 2005. SOD2 overexpres- sion: enhanced mitochondrial tolerance but absence of effect on UCP activity. EMBO J. 24:406.1-4070.
29. Lombardi, A., P. Grasso, ..., F. Goglia. 2008. Interrelated influence of superoxides and free fatty acids over mitochondrial uncoupling in skelet al muscle. Biochim. Biophys. Acta. 1777:826-833.
30. Brand, M. D., N. Turner, ..., A. J. Hulbert 2003. Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem. J. 376:741-748.
31. Brookes, P. S., J. A. Buckingham, ..., M. D. Brand. 1998. The proton permeability of the inner membrane of liver mitochondria from, ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 119:325-334.
32. Stuart, J. A., S. Cadenas, ..., M. D. Brand. 2001. Mitochondrial proton leak and the uncoupling protein 1 homologues. Biochim. Biophys. Acta. 1504:144-1.58.
33. Brand, M. D., P. Couture, ..., A. J. Hulbert. 1991. Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem. J. 275:81-86.
34. Garlid, K. D., A. D. Beavis, and S. K. Ratkje. 1989. On the nature of ion leaks in energy-transducing membranes. Biochim. Biophys. Acta. 976:109-120.
35. Brookes, P. S., A. J. Hulbert, and M. D. Brand. 1997. The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Biochim. Biophys. Acta. 1330:157-164.
36. Schönfeld, P., M. R. Wieckowski, and L. Wojtczak. 2000. Long-chain fatty acid-promoted swelling of mitochondria: further evidence for the protonophoric effect of fatty acids in the inner mitochondrial, membrane. FEBS Lett. 471:108-112. (Pubitemid 30173303)
37. Wojtczak, L., M. R. Wieckowski, and P. Schönfeld. 1998. Protonophoric activity of fatty acid analogs and derivatives in the inner mitochondrial membrane: a further argument for the fatty acid cycling model. Arch. Biochem. Biophys. 357:76-84. (Pubitemid 28402587)
38. Skulachev, V. P. 1999. Anion carriers in fatty acid-mediated physiological uncoupling. J. Bioenerg. Biomembr. 31:431-445.
39. Heimpel, S., G. Basset, ..., M. Klingenberg. 2001. Expression of the mitochondrial ADP/ATP carrier in Escherichia coli. Renaturation, reconstitution, and the effect of mutations on 10 positive residues. J. Biol. Chem. 276:11499-11506. (Pubitemid 37385297)
40. Krämer, R. 1998. Mitochondrial carrier proteins can reversibly change their transport mode: the cases of the aspartate/glutamate and the phosphate carrier. Exp. Physiol. 83:259-265. (Pubitemid 28135089)
41. + translocator. EMBO J. 4:3087-3092.
42. Krishnamoorthy, G., and P. C. Hinkle. 1984. Non-ohmic proton conductance of mitochondria and liposomes. Biochemistry. 23:1640-1645.
43. Benz, R., and S. McLaughlin. 1983. The molecular mechanism of action of the proton ionophore FCCP (carbonylcyanide p-trifluoromethoxyphenylhydrazone). Biophys. J. 41:381-398. (Pubitemid 13082077)
44. Huang, S. G., and M. Klingenberg. 1996. Chloride channel properties of the uncoupling protein from brown adipose tissue mitochondria: a patch-clamp study. Biochemistry. 35:16806-16814.
45. Jezek, P., and K. D. Garlid. 1990. New substrates and competitive inhibitors of the Cl- translocating pathway of the uncoupling protein of brown adipose tissue mitochondria. J. Biol. Chem. 265:19303-19311. (Pubitemid 20378605)
46. Lin, C. S., and M. Klingenberg. 1980. Isolation of the uncoupling protein from brown adipose tissue mitochondria. FEBS Lett. 1.13: 299-303.
47. Lin, C. S., and M. Klingenberg. 1982. Characteristics of the isolated purine nucleotide binding protein from brown fat mitochondria. Biochemistry. 21:2950-2956.
48. Rigaud, J. L., B. Pitard, and D. Levy. 1995. Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins. Biochim. Biophys. Acta. 1231:223-246.
49. Záckova, M., and P. Jezek. 2002. Reconstitution of novel mitochondrial uncoupling proteins UCP2 and UCP3. Biosci. Rep. 22:33-46.
50. Jabůrek, M., and K. D. Garlid. 2003. 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. (Pubitemid 36835341)
51. Jabůrek, M., M. Varecha, ..., K. D. Garlid. 2001. Alkylsulfonates as probes of uncoupling protein transport mechanism. Ion pair transport demonstrates that direct H(+) translocation by UCP1 is not necessary for uncoupling. J. Biol. Chem. 276:31897-31905. (Pubitemid 37384844)
52. Smorodchenko, A., A. Rupprecht, ..., E. E. Pohl. 2009. Comparative analysis of uncoupling protein 4 distribution in various tissues under physiological conditions and during development. Biochim. Biophys. Acta. 1788:2309-2319.
53. Golozoubova, V., E. Hohtola, ..., J. Nedergaard. 2001, Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J. 15:2048-2050.
54. Echtay, K. S., J. L. Pakay, ..., M. D. Brand. 2005. Hydroxynonenal and uncoupling proteins: a model for protection against oxidative damage. Biofactors. 24:119-130.
55. Arsenijevic, D., H. Onuma, ..., D. Ricquier. 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.
56. 2+ uniport. Nat. Cell Biol. 9-445-452.
57. Gutknecht, J. 1988. Proton conductance caused by long-chain fatty acids in phospholipid bilayer membranes. V. Membr. Biol. 106:83-93.
58. Brunaldi, K., M. A. Miranda, ..., J. Procopio. 2005. Fatty acid flip-flop and proton transport determined by short-circuit current in planar bilayers. J. Lipid Res. 46:245-251. (Pubitemid 40271088)
59. Rial, E., A. Poustie, and D. G. Nicholls. 1983. Brown-adipose-tissue mitochondria: the regulation of the 32000-Mr uncoupling protein by fatty acids and purine nucleotides. Eur. J. Biochem. 137:197-203. (Pubitemid 14178258)
60. Kamp, F., and J. A. Hamilton. 1992. pH gradients across phospholipid membranes caused by fast flip-flop of un-ionized fatty acids. Proc. Natl. Acad. Sci. USA. 89:11367-11370.
61. Pohl, E. E., U. Peterson, ..., P. Pohl. 2000. Changes of intrinsic membrane potentials induced by flip-flop of long-chain fatty acids. Biochemistry. 39:1834-1839.
62. Pohl, E. E., A. M. Voltchenko, and A. Rupprecht. 2008. Flip-flop of hydroxy fatty acids across the membrane as monitored by proton-sensitive microelectrodes. Biochim. Biophys. Acta. 1778:1292-1297.
63. Coster, H. G. 1975. Electromechanical stresses and the effect of pH on membrane structure. Biochim. Biophys. Acta. 382:142-146.
64. Bamberg, E., and R. Benz. 1976. Voltage-induced thickness changes of lipid bilayer membranes and the effect of an electrin field on gramicidin A channel formation. Biochim. Biophys. Acta. 426:570-580.
65. Sugar, I. P. 1981. The effects of external fields on the structure of lipid bilayers. J. Physiol. (Paris). 77:1035-1042. (Pubitemid 12085493)
66. Pohl, P., T. I. Rokitskaya, ..., S. M. Saparov. 1997. Permeation of phlor- etin across bilayer lipid membranes monitored by dipole potential, and microelectrode measurements. Biochim. Biophys. Acta. 1323:163-172. (Pubitemid 27065365)
67. Stulen, G. 1981. Electric field effects on lipid membrane structure. Biochim. Biophys. Acta. 640:621-627. (Pubitemid 11134802)
68. Le Saux, A., J. M. Ruysschaert, and E. Goormaghtigh. 2001. Membrane molecule reorientation in an electric field recorded by attenuated total reflection Fourier-transform infrared spectroscopy. Biophys. J. 80: 324-330. (Pubitemid 32108185)
69. Glaser, R. W., S. L. Leikin, ..., A. I. Sokirko. 1988. Reversible electrical breakdown of lipid bilayers: formation, and evolution of pores. Biochim. Biophys. Acta. 940:275-287.
70. Hladky, S. B. 1974. The energy barriers to ion transport by nonactin across thin lipid membranes. Biochim. Biophys. Acta. 352:71-85.
71. Hall, J. E., C. A. Mead, and G. Szabo. 1973. A barrier model for current flow in lipid bilayer membranes. J. Membr. Biol. 11:75-97.
72. Skulachev, V. P. 1991. Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett. 294:158-162.
73. Garlid, K. D., D. E. Orosz, ..., P. Jezek. 1996. On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein. J. Biol. Chem. 271:2615-2620.
74. Pebay-Peyroula, E., C. Dahout-Gonzalez, G. Brandolin. 2003. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature. 426:39-44. (Pubitemid 37432535)
75. Nicholls, D. G. 1974. The influence of respiration and ATP hydrolysis on the proton-electrochemical gradient across the inner membrane of rat-liver mitochondria as determined by ion distribution. Eur. J. Biochem. 50:305-315.
76. Nicholls, D. G. 1977. The effective proton conductance of the inner membrane of mitochondria from brown adipose tissue. Dependency on proton electrochemical potential gradient. Eur. J. Biochem. 77: 349-356.
77. Brown, G. C., and M. D. Brand. 1986. Changes in permeability to protons and other cations at high proton motive force in rat liver mitochondria. Biochem. J. 234:75-81.
78. Sorgato, M. C., and S. J. Ferguson. 1979. Variable proton conductance of submitochondrial particles. Biochemistry. 18:5737-5742.
79. Hauser, H., K. Howell, D. E. Bowyer. 1980. Rabbit small intestinal brush border membrane preparation and lipid composition. Biochim. Biophys. Acta. 602:567-577. (Pubitemid 11218316)
80. Boime, I., E. E. Smith, and F. E. Hunter, Jr. 1970. The role of fatty acids in mitochondrial changes during liver ischemia. Arch. Biochem. Biophys. 139:425-443.
81. Conner, W. E., D. S. Lin, and C. Colvis. 1996. Differential mobilization of fatty acids from adipose tissue. J. Lipid Res. 37:290-298. (Pubitemid 26078947)
82. Chien, K. R., A. Han, ... , J. T. Willerson. 1984. Accumulation of unesterified arachidonic acid in ischemic canine myocardium. Relationship to a phosphatidylcholine deacylation-reacylation cycle and the depletion of membrane phospholipids. Circ. Res. 54:313-322.
83. Schönfeld, P., L. Schild, and W. Kunz. 1989. Long-chain fatty acids act as protonophoric uncouplers of oxidative phosphorylation in rat liver mitochondria. Biochim. Biophys. Acta. 977:266-272. (Pubitemid 20004617)
84. Skulachev, V. P. 1996. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q. Rev. Biophys. 29:169-202.