Abstract
This work is focused on the physicochemical nature and functional meaning of structural alterations in mitochondrial membranes. These alterations are observed at subnormal temperatures for homeothermic animals. Using pyrene as a fluorescent probe, some structural transitions in annular lipids were detected at 19 and 25°C, which are identified as the pre-transition and main phase transition temperatures. The observed changes are consistent with abrupt alterations in the efficiency of tryptophan fluorescence quenching by pyrene that occur at the same temperatures. The data imply considerable changes in the protein–lipid contact area. The effects are observed under low-amplitude mitochondrial swelling in media with lowered tonicity. Since the transition of the phosphorylating system into the supercomplex state has been previously shown under these conditions, it allows us to assume a relationship between the observed membrane structural alterations and the supercomplex formation. Measurements of the respiration rate in mitochondria in a hypoosmotic medium show that the activation energy of the rate-limiting step in the process of ATP synthesis changes abruptly at the temperature of the phase transition of annular lipids (25°C). Analysis of the literature data indicates that a similar abnormal low-temperature abrupt change in activation energy in the reaction of ATP synthesis around 25°C is observed for a variety of animal species. Hence, the low-temperature structural alterations in membranes of warm-blooded animals should have general biological importance. A comparison of the results obtained in our study and the literature data led, therefore, to a qualitative description of the physiochemical nature of the observed membrane alterations. Similar to the membrane-raft model, a model of supercomplex formation in mitochondria is proposed.
Similar content being viewed by others
References
I. P. Krasinskaya, I. S. Litvinov, S. D. Zakharov, et al., Biokhimiya (Moscow) 54 (9), 1550 (1989).
D. J. Pehowich et al., Biochemistry (Moscow) 27 (13), 4632 (1988).
T. N. Murugova, V. I. Gordeliy, A. I. Kuklin, et al., Biophysics 51 (6), 882 (2006).
I. P. Krasinskaya, V. N. Marshansky, S. F. Dragunova, and L. S. Yaguzhinsky, FEBS Lett. 167 (1), 176 (1984).
P. Mitchell, Nature 191, 144 (1961).
R. J. P. Williams, J. Theor. Biol. 1 (1), 1 (1961).
A. P. Halestrap, Biochim. Biophys. Acta 973 (3), 355 (1989).
J. K. Raison and E. J. McMurchie, Biochim. Biophys. Acta 363 (2), 135 (1974).
E. J. McMurchie and J. K. Raison, Biochim. Biophys. Acta 554 (2), 364 (1979).
F. Geiser and E. J. McMurchie, J. Comp. Physiol. B 155 (6), 711 (1985).
E. J. McMurchie, J. K. Raison, and K. D. Cairncross, Comp. Biochem. Physiol. B 44 (4), 1017 (1973).
H. J. Galla and W. Hartmann, Chem. Phys. Lipids 27 (3), 199 (1980).
M. Dembo, et al., Biochim. Biophys. Acta 552 (2), 201 (1979).
H. J. Galla and E. Sackmann, Biochim. Biophys. Acta 339 (1), 103 (1974).
N. L. Vekshin, in Photonics of Biopolymers (Springer, Berlin, 2002), pp. 165–171.
R. L. Melnick, H. C. Haspel, M. Goldenberg, et al., Biophys. J. 34 (3), 499 (1981).
J. Y. Lehtonen, J. M. Holopainen, and P. K. Kinnunen, Biophys. J. 70 (4), 1753 (1996).
A. D. Dergunov, A. S. Kaprel’iants, and D. N. Ostrovskii, Biokhimiya (Moscow) 46 (8), 1499 (1981).
I. S. Litvinov and V. V. Obraztsov, Biofizika 27 (1), 81 (1982).
J. K. Raison, J. M. Lyons, and W. W. Thomson, Arch. Biochem. Biophys. 142 (1), 83 (1971).
H. M. Levy, N. Sharon, E. M. Ryan, and D. E. Koshland, Jr., Biochim. Biophys. Acta 56, 118 (1962).
K. A. Riske, R. P. Barroso, C. C. Vequi-Suplicy, et al., Biochim. Biophys. Acta 1788 (5), 954 (2009).
T. Kaasgaard, C. Leidy, J. H. Crowe, et al., Biophys. J. 85 (1), 350 (2003).
L. Picas, M. T. Montero, A. Morros, et al., J. Fluoresc. 17 (6), 649 (2007).
H. Pfeiffer, H. Binder, G. Klose, and K. Heremans, Biochim. Biophys. Acta 1609 (2), 148 (2003).
K. Oglecka, P. Rangamani, B. Liederberg, et al., E-life 3, e03695 (2014). doi 10.7554/eLife.03695
W. R. Perkins, X. Li, J. L. Slater, et al., Biochim. Biophys. Acta 1327 (1), 41 (1997).
G. P. Gorbenko, V. M. Trusova, J. L. Molotkovsky, et al., Biochim. Biophys. Acta 1788 (6), 1358 (2009).
I. Levental and S. L. Veatch, J. Mol. Biol. 428, 4749 (2016). doi 10.1016/j.jmb.2016.08.022
M. Carquin, L. D’Auria, H. Pollet, et al., Prog. Lipid Res. 62, 1 (2016).
J. Y. Lehtonen and P. K. Kinnunen, Biophys. J. 72 (3), 1247 (1997).
C. Suárez-Germà, L. M. S. Loura, M. Prieto, et al., J. Phys. Chem. B (8), 2438 (2012).
B. Piknová, T. Hianik, V. N. Shestimirov, et al., Gen. Physiol. Biophys. 10 (4), 395 (1991).
S. V. Nesterov, Y. A. Skorobogatova, and L. S. Yaguzhinsky, Biophysics (Moscow) 59 (6), 904 (2014).
V. Luzzati and F. Husson, J. Cell Biol. 12, 207 (1962).
L. M. Gordon, R. D. Sauerheber, J. A, Esgate, et al., J. Biol. Chem. 255 (10), 4519 (1980).
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © L.S. Yaguzhinsky, Y.A. Skorobogatova, S.V. Nesterov, 2017, published in Biofizika, 2017, Vol. 62, No. 3, pp. 518–524.
Rights and permissions
About this article
Cite this article
Yaguzhinsky, L.S., Skorobogatova, Y.A. & Nesterov, S.V. Functionally significant low-temperature structural alterations in mitochondrial membranes of homoiothermic animals. BIOPHYSICS 62, 415–420 (2017). https://doi.org/10.1134/S0006350917030241
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006350917030241