Cytoskeleton and regulation of mitochondrial function: The role of beta-tubulin II

Frontiers in Physiology

Volumn 4 APR, Issue , 2013, Pages

  Kuznetsov, Andrey V ^a   Javadov, Sabzali ^b   Guzun, Rita ^c,d   Grimm, Michael ^a   Saks, Valdur ^d  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

^d Domaine Universitaire   (France)

Author keywords

Beta tubulin isotypes; Cardiomyocytes; Confocal microscopy; Creatine kinase; HL 1 cells; Mitochondria Cytoskeleton interactions; Mitochondrial regulation; VDAC

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; BETA TUBULIN; BETA TUBULIN II; CREATINE PHOSPHATE; MITOCHONDRIAL CREATINE KINASE; PLECTIN; PLECTIN 1B; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

AGING; ARTICLE; CANCER CELL; CELL ENERGY; CELLULAR DISTRIBUTION; CYTOSKELETON; DUCHENNE MUSCULAR DYSTROPHY; ENERGY METABOLISM; GLYCOLYSIS; HEART MUSCLE CELL; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MUSCLE FIBRIL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM;

EID: 84883813989     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00082     Document Type: Article

References (55)

1. Andrienko, T., Kuznetsov, A. V., Kaambre, T., Usson, Y., Orosco, A., Appaix, F., et al. (2003). Metabolic consequences of functional complexes of mitochondria, myofibrils and sarcoplasmic reticulum in muscle cells. J. Exp. Biol. 206, 2059-2072.
2. Anesti, V., and Scorrano, L. (2006). The relationship between mitochondrial shape and function and the cytoskeleton. Biochim. Biophys. Acta 1757, 692-699.
3. Anmann, T., Guzun, R., Beraud, N., Pelloux, S., Kuznetsov, A. V., Kogerman, L., et al. (2006). Different kinetics of the regulation of respiration in permeabilized cardiomyocytes and in HL-1 cardiac cells. Importance of cell structure/organization for respiration regulation. Biochim. Biophys. Acta 1757, 1597-1606.
4. Appaix, F., Kuznetsov, A. V., Usson, Y., Kay, L., Andrienko, T., Olivares, J., et al. (2003). Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria. Exp. Physiol. 88, 175-190.
5. Balaban, R. S. (1990). Regulation of oxidative phosphorylation in the mammalian cell. Am. J. Physiol. 258, C377-C389.
6. Balaban, R. S. (2002). Cardiac energy metabolism homeostasis: role of cytosolic calcium. J. Mol. Cell Cardiol. 34, 1259-1271.
7. Balaban, R. S., Bose, S., French, S. A., and Territo, P. R. (2003). Role of calcium in metabolic signaling between cardiac sarcoplasmic reticulum and mitochondria in vitro. Am. J. Physiol. Cell Physiol. 284, C285-C293.
8. Belikova, Y. O., Kuznetsov, A. V., and Saks, V. A. (1990). Specific limitations for intracellular diffusion of ADP in cardiomyocytes. Biochemistry 55, 1450-1460.
9. Braun, U., Paju, K., Eimre, M., Seppet, E., Orlova, E., Kadaja, L., et al. (2001). Lack of dystrophin is associated with altered integration of the mitochondria and ATPases in slow-twitch muscle cells of MDX mice. Biochim. Biophys. Acta 1505, 258-270.
10. Burelle, Y., and Hochachka, P. W. (2002). Endurance training induces muscle-specific changes in mitochondrial function in skinned muscle fibers. J. Appl. Physiol. 92, 2429-2438.
11. Capetanaki, Y. (2002). Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc. Med. 12, 339-348.
12. Carre, M., Andre, N., Carles, G., Borghi, H., Brichese, L., Briand, C., et al. (2002). Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J. Biol. Chem. 277, 33664-33669.
13. Eimre, M., Puhke, R., Alev, K., Seppet, E., Sikkut, A., Peet, N., et al. (2006). Altered mitochondrial apparent affinity for ADP and impaired function of mitochondrial creatine kinase in gluteus medius of patients with hip osteoarthritis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1271-R1275.
14. Fontaine, E. M., Keriel, C., Lantuejoul, S., Rigoulet, M., Leverve, X. M., and Saks, V. A. (1995). Cytoplasmic cellular structures control permeability of outer mitochondrial membrane for ADP and oxidative phosphorylation in rat liver cells. Biochem. Biophys. Res. Commun. 213, 138-146.
15. Glancy, B., and Balaban, R. S. (2012). Role of mitochondrial Ca2+ in the regulation of cellular energetics. Biochemistry 51, 2959-2973.
16. Gonzalez-Granillo, M., Grichine, A., Guzun, R., Usson, Y., Tepp, K., Chekulayev, V., et al. (2012). Studies of the role of tubulin beta II isotype in regulation of mitochondrial respiration in intracellular energetic units in cardiac cells. J. Mol. Cell Cardiol. 52, 437-447.
17. Guzun, R., Karu-Varikmaa, M., Gonzalez-Granillo, M., Kuznetsov, A. V., Michel, L., Cottet-Rousselle, C., et al. (2011). Mitochondria-cytoskeleton interaction: distribution of beta-tubulins in cardiomyocytes and HL-1 cells. Biochim. Biophys. Acta 1807, 458-469.
18. Hollenbeck, P. J., and Saxton, W. M. (2005). The axonal transport of mitochondria. J. Cell Sci. 118, 5411-5419.
19. Kaasik, A., Veksler, V., Boehm, E., Novotova, M., Minajeva, A., and Ventura-Clapier, R. (2001). Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ. Res. 89, 153-159.
20. Kay, L., Li, Z., Mericskay, M., Olivares, J., Tranqui, L., Fontaine, E., et al. (1997a). Study of regulation of mitochondrial respiration in vivo. An analysis of influence of ADP diffusion and possible role of cytoskeleton. Biochim. Biophys. Acta 1322, 41-59.
21. Kay, L., Rossi, A., and Saks, V. (1997b). Detection of early ischemic damage by analysis of mitochondrial function in skinned fibers. Mol. Cell Biochem. 174, 79-85.
22. Kay, L., Nicolay, K., Wieringa, B., Saks, V., and Wallimann, T. (2000). Direct evidence for the control of mitochondrial respiration by mitochondrial creatine kinase in oxidative muscle cells in situ. J. Biol. Chem. 275, 6937-6944.
23. Khuchua, Z. A., Ventura-Clapier, R., Kuznetsov, A. V., Grishin, M. N., and Saks, V. A. (1989). Alterations in the creatine kinase system in the myocardium of cardiomyopathic hamsters. Biochem. Biophys. Res. Commun. 165, 748-757.
24. Konieczny, P., Fuchs, P., Reipert, S., Kunz, W. S., Zeold, A., Fischer, I., et al. (2008). Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J. Cell Biol. 181, 667-681.
25. Kuznetsov, A. V., Mayboroda, O., Kunz, D., Winkler, K., Schubert, W., and Kunz, W. S. (1998a). Functional imaging of mitochondria in saponin-permeabilized mice muscle fibers. J. Cell Biol. 140, 1091-1099.
26. Kuznetsov, A. V., Winkler, K., Wiedemann, F. R., von Bossanyi, P., Dietzmann, K., and Kunz, W. S. (1998b). Impaired mitochondrial oxidative phosphorylation in skeletal muscle of the dystrophin-deficient mdx mouse. Mol. Cell. Biochem. 183, 87-96.
27. Kuznetsov, A. V., Tiivel, T., Sikk, P., Kaambre, T., Kay, L., Daneshrad, Z., et al. (1996). Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur. J. Biochem. 241, 909-915.
28. Kuznetsov, A. V., Veksler, V., Gellerich, F. N., Saks, V., Margreiter, R., and Kunz, W. S. (2008). Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat. Protoc. 3, 965-976.
29. Laclau, M. N., Boudina, S., Thambo, J. B., Tariosse, L., Gouverneur, G., Bonoron-Adele, S., et al. (2001). Cardioprotection by ischemic preconditioning preserves mitochondrial function and functional coupling between adenine nucleotide translocase and creatine kinase. J. Mol. Cell Cardiol. 33, 947-956.
30. Milner, D. J., Mavroidis, M., Weisleder, N., and Capetanaki, Y. (2000). Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J. Cell Biol. 150, 1283-1298.
31. Mose-Larsen, P., Bravo, R., Fey, S. J., Small, J. V., and Celis, J. E. (1982). Putative association of mitochondria with a subpopulation of intermediate-sized filaments in cultured human skin fibroblasts. Cell 31, 681-692.
32. Rappaport, L., Oliviero, P., and Samuel, J. L. (1998). Cytoskeleton and mitochondrial morphology and function. Mol. Cell Biochem. 184, 101-105.
33. Rostovtseva, T. K., and Bezrukov, S. M. (2008). VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J. Bioenerg. Biomembr. 40, 163-170.
34. Rostovtseva, T. K., Sheldon, K. L., Hassanzadeh, E., Monge, C., Saks, V., Bezrukov, S. M., et al. (2008). Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc. Natl. Acad. Sci. U.S.A. 105, 18746-18751.
35. Saetersdal, T., Greve, G., and Dalen, H. (1990). Associations between beta-tubulin and mitochondria in adult isolated heart myocytes as shown by immunofluorescence and immunoelectron microscopy. Histochemistry 95, 1-10.
36. Saks, V., Belikova, Y., Vasilyeva, E., Kuznetsov, A., Fontaine, E., Keriel, C., et al. (1995). Correlation between degree of rupture of outer mitochondrial membrane and changes of kinetics of regulation of respiration by ADP in permeabilized heart and liver cells. Biochem. Biophys. Res. Commun. 208, 919-926.
37. Saks, V., Dzeja, P., Schlattner, U., Vendelin, M., Terzic, A., and Wallimann, T. (2006a). Cardiac system bioenergetics: metabolic basis of the Frank-Starling law. J. Physiol. 571, 253-273.
38. Saks, V., Favier, R., Guzun, R., Schlattner, U., and Wallimann, T. (2006b). Molecular system bioenergetics: regulation of substrate supply in response to heart energy demands. J. Physiol. 577, 769-777.
39. Saks, V., Guzun, R., Timohhina, N., Tepp, K., Varikmaa, M., Monge, C., et al. (2010). Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome. Biochim. Biophys. Acta 1797, 678-697.
40. Saks, V., Kuznetsov, A., Andrienko, T., Usson, Y., Appaix, F., Guerrero, K., et al. (2003). Heterogeneity of ADP diffusion and regulation of respiration in cardiac cells. Biophys. J. 84, 3436-3456.
41. Saks, V., Kuznetsov, A. V., Gonzalez-Granillo, M., Tepp, K., Timohhina, N., Karu-Varikmaa, M., et al. (2012). Intracellular energetic units regulate metabolism in cardiac cells. J. Mol. Cell Cardiol. 52, 419-436.
42. Saks, V. A., Belikova, Y. O., and Kuznetsov, A. V. (1991a). In vivo regulation of mitochondrial respiration in cardiomyocytes: specific restrictions for intracellular diffusion of ADP. Biochim. Biophys. Acta 1074, 302-311.
43. Saks, V. A., Kaambre, T., Sikk, P., Eimre, M., Orlova, E., Paju, K., et al. (2001). Intracellular energetic units in red muscle cells. Biochem. J. 356, 643-657.
44. Saks, V. A., Kuznetsov, A. V., Kupriyanov, V. V., Miceli, M. V., and Jacobus, W. E. (1985). Creatine kinase of rat heart mitochondria. The demonstration of functional coupling to oxidative phosphorylation in an inner membrane-matrix preparation. J. Biol. Chem. 260, 7757-7764.
45. Saks, V. A., Vasil'eva, E., Belikova, Y., Kuznetsov, A. V., Lyapina, S., Petrova, L., et al. (1993). Retarded diffusion of ADP in cardiomyocytes: possible role of mitochondrial outer membrane and creatine kinase in cellular regulation of oxidative phosphorylation. Biochim. Biophys. Acta 1144, 134-148.
46. Tang, H. L., Lung, H. L., Wu, K. C., Le, A. H. P., Tang, H. M., and Fung, M. C. (2008). Vimentin supports mitochondrial morphology and organization. Biochem. J. 410, 141-146.
47. Tiivel, T., Kadaya, L., Kuznetsov, A., Kaambre, T., Peet, N., Sikk, P., et al. (2000). Developmental changes in regulation of mitochondrial respiration by ADP and creatine in rat heart in vivo. Mol. Cell Biochem. 208, 119-128.
48. Tonkonogi, M., and Sahlin, K. (2002). Physical exercise and mitochondrial function in human skeletal muscle. Exerc. Sport Sci. Rev. 30, 129-137.
49. Veksler, V. I., Kuznetsov, A. V., Anflous, K., Mateo, P., van Deursen, J., Wieringa, B., et al. (1995). Muscle creatine kinase-deficient mice. II. Cardiac and skeletal muscles exhibit tissue-specific adaptation of the mitochondrial function. J. Biol. Chem. 270, 19921-19929.
50. Vendelin, M., Beraud, N., Guerrero, K., Andrienko, T., Kuznetsov, A. V., Olivares, J., et al. (2005). Mitochondrial regular arrangement in muscle cells: a "crystal-like" pattern. Am. J. Physiol. Cell Physiol. 288, C757-C767.
51. Villani, G., Greco, M., Papa, S., and Attardi, G. (1998). Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem. 273, 31829-31836.
52. Williamson, J. R. (1979). Mitochondrial function in the heart. Annu. Rev. Physiol. 41, 485-506.
53. Winter, L., Abrahamsberg, C., and Wiche, G. (2008). Plectin isoform 1b mediates mitochondrion-intermediate lament network linkage and controls organelle shape. J. Cell Biol. 181, 903-911.
54. Zoll, J., Sanchez, H., N'Guessan, B., Ribera, F., Lampert, E., Bigard, X., et al. (2002). Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J. Physiol. 543, 191-200.
55. Zoll, J., Ventura-Clapier, R., Serrurier, B., and Bigard, A. X. (2001). Response of mitochondrial function to hypothyroidism in normal and regenerated rat skeletal muscle. J. Muscle Res. Cell Motil. 22, 141-147.