Studies of the role of tubulin beta II isotype in regulation of mitochondrial respiration in intracellular energetic units in cardiac cells

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 2, 2012, Pages 437-447

  Gonzalez Granillo, Marcela ^a   Grichine, Alexei ^b   Guzun, Rita ^a   Usson, Yves ^b   Tepp, Kersti ^c   Chekulayev, Vladimir ^c   Shevchuk, Igor ^c   Karu Varikmaa, Minna ^c   Kuznetsov, Andrey V ^d   Grimm, Michael ^d   Saks, Valdur ^a,c   Kaambre, Tuuli ^c  

^a Domaine Universitaire   (France)

^b UNIV GRENOBLE ALPES   (France)

^c NATIONAL INSTITUTE OF CHEMICAL PHYSICS AND BIOPHYSICS   (Estonia)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cardiomyocytes; Cytoskeleton; Energy fluxes; Mitochondria; Regulation of respiration; Tubulin

Indexed keywords

ADENOSINE DIPHOSPHATE; ALPHA ACTININ; BETA TUBULIN; CREATINE; CYTOCHROME C; MITOCHONDRIAL CREATINE KINASE; PHOSPHOENOLPYRUVATE; PYRUVATE KINASE; TRYPSIN; TUBULIN BETA II ISOTYPE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL ENERGY; CELL PERMEABILIZATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; HEART MUSCLE CELL; IMMUNOFLUORESCENCE CONFOCAL MICROSCOPY; IMMUNOFLUORESCENCE MICROSCOPY; MALE; MEMBRANE PERMEABILITY; MITOCHONDRIAL INNER MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL OUTER MEMBRANE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RAT; RESPIROMETRY;

ADENOSINE DIPHOSPHATE; ANIMALS; CELL RESPIRATION; CREATINE KINASE, MITOCHONDRIAL FORM; ENERGY METABOLISM; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANES; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; PROTEIN TRANSPORT; RATS; RATS, WISTAR; TUBULIN;

EID: 84855990736     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.07.027     Document Type: Article

References (58)

1. Bessman S.P., Carpenter C.L. The creatine-creatine phosphate energy shuttle. Annu Rev Biochem 1985, 54:831-862.
2. Wallimann T., Wyss M., Brdiczka D., Nicolay K., Eppenberger H.M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem J 1992, 281:21-40.
3. Wallimann T., Tokarska-Schlattner M., Neumann D., Epand R.F., Andres R.H., Widmer H.R., et al. The phosphocreatine circuit: molecular and cellular physiology of creatine kinases, sensitivity to free radicals, and enhancement by creatine supplementation. Molecular system bioenergetics energy for life. GmbH, Germany 2007, 195-264. Wiley-VCH, Weinheim. V. Saks (Ed.).
4. Molecular system bioenergetics. Energy for life. Gmbh, Germany 2007, Wiley-VCH, Weinheim. V. Saks (Ed.).
5. Saks V., Anmann T., Guzun R., Kaambre T., Sikk P., Schlattner U., et al. The creatine kinase phosphotransfer network: thermodynamic and kinetic considerations, the impact of the mitochondrial outer membrane and modelling approaches. Creatine and creatine kinase in health and disease 2007, 27-66. Springer, Dordrecht. M. Wyss, G. Salomons (Eds.).
6. Saks V., Beraud N., Wallimann T. Metabolic compartmentation - a system level property of muscle cells: real problems of diffusion in living cells. Int J Mol Sci 2008, 9:751-767.
7. Saks V., Dzeja P., Schlattner U., Vendelin M., Terzic A., Wallimann T. Cardiac system bioenergetics: metabolic basis of the Frank-Starling law. J Physiol 2006, 571:253-273.
8. Saks V., Guzun R., Timohhina N., Tepp K., Varikmaa M., Monge C., et al. Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome. Biochim Biophys Acta 2010, 1797:678-697.
9. Saks V., Monge C., Anmann T., Dzeja P. Integrated and organized cellular energetic systems: theories of cell energetics, compartmentation and metabolic channeling. Molecular system bioenergetics energy for life. GmbH, Germany 2007, 59-110. Wiley-VCH, Weinheim. V. Saks (Ed.).
10. Saks V., Monge C., Guzun R. Philosophical basis and some historical aspects of systems biology: from Hegel to Noble - applications for bioenergetic research. Int J Mol Sci 2009, 10:1161-1192.
11. Guzun R., Saks V. Application of the principles of systems biology and Wiener's cybernetics for analysis of regulation of energy fluxes in muscle cells in vivo. Int J Mol Sci 2010, 11:982-1019.
12. Guzun R., Timohhina N., Tepp K., Monge C., Kaambre T., Sikk P., et al. Regulation of respiration controlled by mitochondrial creatine kinase in permeabilized cardiac cells in situ. Importance of system level properties. Biochim Biophys Acta 2009, 1787:1089-1105.
13. Guzun R., Timohhina N., Tepp K., Gonzalez-Granillo M., Shevchuk I., Chekulayev V., et al. Systems bioenergetics of creatine kinase networks: physiological roles of creatine and phosphocreatine in regulation of cardiac cell function. Amino Acids 2011, 40:1333-1348.
14. Guzun R., Karu-Varikmaa M., Gonzalez-Granillo M., Kuznetsov A.V., Michel L., Cottet-Rousselle C., et al. Mitochondria-cytoskeleton interaction: distribution of beta-tubulins in cardiomyocytes and HL-1 cells. Biochim Biophys Acta 2011, 1807:458-469.
15. Saks V.A., Kaambre T., Sikk P., Eimre M., Orlova E., Paju K., et al. Intracellular energetic units in red muscle cells. Biochem J 2001, 356:643-657.
16. Kummel L. Ca, Mg-ATPase activity of permeabilised rat heart cells and its functional coupling to oxidative phosphorylation of the cells. Cardiovasc Res 1988, 22:359-367.
17. Kuznetsov A.V., Veksler V., Gellerich F.N., Saks V., Margreiter R., Kunz W.S. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 2008, 3:965-976.
18. Saks V.A., Veksler V.I., Kuznetsov A.V., Kay L., Sikk P., Tiivel T., et al. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 1998, 184:81-100.
19. Saks V.A., Belikova Y.O., Kuznetsov A.V. In vivo regulation of mitochondrial respiration in cardiomyocytes: specific restrictions for intracellular diffusion of ADP. Biochim Biophys Acta 1991, 1074:302-311.
20. Saks V.A., Vasil'eva E., Belikova Yu O., Kuznetsov A.V., Lyapina S., Petrova L., et al. Retarded diffusion of ADP in cardiomyocytes: possible role of mitochondrial outer membrane and creatine kinase in cellular regulation of oxidative phosphorylation. Biochim Biophys Acta 1993, 1144:134-148.
21. Kuznetsov A.V., Tiivel T., Sikk P., Kaambre T., Kay L., Daneshrad Z., et al. Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur J Biochem 1996, 241:909-915.
22. Saks V.A., Khuchua Z.A., Vasilyeva E.V., Belikova O., Kuznetsov A.V. Metabolic compartmentation and substrate channelling in muscle cells. Role of coupled creatine kinases in in vivo regulation of cellular respiration - a synthesis. Mol Cell Biochem 1994, 133-134:155-192.
23. Saks V.A., Kuznetsov A.V., Khuchua Z.A., Vasilyeva E.V., Belikova J.O., Kesvatera T., et al. Control of cellular respiration in vivo by mitochondrial outer membrane and by creatine kinase. A new speculative hypothesis: possible involvement of mitochondrial-cytoskeleton interactions. J Mol Cell Cardiol 1995, 27:625-645.
24. Appaix F., Kuznetsov A.V., Usson Y., Kay L., Andrienko T., Olivares J., et al. Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria. Exp Physiol 2003, 88:175-190.
25. Rostovtseva T.K., Sheldon K.L., Hassanzadeh E., Monge C., Saks V., Bezrukov S.M., et al. Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci USA 2008, 105:18746-18751.
26. Rostovtseva T.K., Bezrukov S.M. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J Bioenerg Biomembr 2008, 40:163-170.
27. Monge C., Beraud N., Kuznetsov A.V., Rostovtseva T., Sackett D., Schlattner U., et al. Regulation of respiration in brain mitochondria and synaptosomes: restrictions of ADP diffusion in situ, roles of tubulin, and mitochondrial creatine kinase. Mol Cell Biochem 2008, 318:147-165.
28. Sokolova N., Vendelin M., Birkedal R. Intracellular diffusion restrictions in isolated cardiomyocytes from rainbow trout. BMC Cell Biol 2009, 10:90.
29. Sommer J., Jennings R. Ultrastructure of cardiac muscle. The heart and cardiovascular system 1986, 61-100. Raven, New York. H. Fozzard, E. Haber, R. Jennings, A. Katz, H. Morgan (Eds.).
30. Fawcett D.W., McNutt N.S. The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J Cell Biol 1969, 42:1-45.
31. Ultrastructure of mammalian cardiac muscle 1984, Nijhoff, Boston. M.S. Forbes, N.S. (Eds.).
32. Vendelin M., Beraud N., Guerrero K., Andrienko T., Kuznetsov A.V., Olivares J., et al. Mitochondrial regular arrangement in muscle cells: a "crystal-like" pattern. Am J Physiol Cell Physiol 2005, 288:C757-C767.
33. Beraud N., Pelloux S., Usson Y., Kuznetsov A.V., Ronot X., Tourneur Y., et al. Mitochondrial dynamics in heart cells: very low amplitude high frequency fluctuations in adult cardiomyocytes and flow motion in non beating Hl-1 cells. J Bioenerg Biomembr 2009, 41:195-214.
34. Appaix F., Guerrero K., Rampal D., Izziki M., Kaambre T., Sikk P., et al. Bax and heart mitochondria: uncoupling and inhibition of oxidative phosphorylation without permeability transition. Biochim Biophys Acta 2002, 1556:155-167.
35. Klingenberg M. The A.D.P. and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 2008, 1778:1978-2021.
36. Schlattner U., Wallimann T. Metabolite channeling: creatine kinase microcompartments. In Encyclopedia of Biological Chemistry 2004, 646-651. Academic Press, New York, USA. W.J. Lennarz, M.D. Lane (Eds.).
37. Schlattner U., Tokarska-Schlattner M., Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 2006 Feb, 1762(2):164-180.
38. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 2004, 256-257:107-115.
39. Colombini M. The published 3D structure of the VDAC channel: native or not?. Trends Biochem Sci 2009, 34:382-389.
40. Gellerich F., Saks V.A. Control of heart mitochondrial oxygen consumption by creatine kinase: the importance of enzyme localization. Biochem Biophys Res Commun 1982, 105:1473-1481.
41. Timohhina N., Guzun R., Tepp K., Monge C., Varikmaa M., Vija H., et al. Direct measurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for mitochondrial interactosome. J Bioenerg Biomembr 2009, 41:259-275.
42. Saetersdal T., Greve G., Dalen H. Associations between beta-tubulin and mitochondria in adult isolated heart myocytes as shown by immunofluorescence and immunoelectron microscopy. Histochemistry 1990, 95:1-10.
43. Redeker V. Mass spectrometry analysis of C-terminal posttranslational modifications of tubulins. Methods Cell Biol 2010, 95:77-103.
44. Luduena R.F. Multiple forms of tubulin: different gene products and covalent modifications. Int Rev Cytol 1998, 178:207-275.
45. Sackett D.L. Evolution and coevolution of tubulin's carboxy-terminal tails and mitochonsdria. Mitochondria: structure, functions and dysfunctions 2010, 441-470. Nova Science Publishers, USA. O.L. Svensson (Ed.).
46. Capetanaki Y., Bloch R.J., Kouloumenta A., Mavroidis M., Psarras S. Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res 2007, 313:2063-2076.
47. Ball E.H., Singer S.J. Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci USA 1982, 79:123-126.
48. Heggeness M.H., Simon M., Singer S.J. Association of mitochondria with microtubules in cultured cells. Proc Natl Acad Sci USA 1978, 75:3863-3866.
49. Rappaport L., Oliviero P., Samuel J.L. Cytoskeleton and mitochondrial morphology and function. Mol Cell Biochem 1998, 184:101-105.
50. Anesti V., Scorrano L. The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta 2006, 1757:692-699.
51. Aon M.A., Cortassa S. Coherent and robust modulation of a metabolic network by cytoskeletal organization and dynamics. Biophys Chem 2002, 97:213-231.
52. Aon M.A., O'Rourke B., Cortassa S. The fractal architecture of cytoplasmic organization: scaling, kinetics and emergence in metabolic networks. Mol Cell Biochem 2004, 256-257:169-184.
53. Guerrero K., Monge C., Bruckner A., Puurand U., Kadaja L., Kaambre T., et al. Study of possible interactions of tubulin, microtubular network, and STOP protein with mitochondria in muscle cells. Mol Cell Biochem 2010, 337:239-249.
54. Wolff J. Plasma membrane tubulin. Biochim Biophys Acta 2009, 1788:1415-1433.
55. Kostin S., Hein S., Arnon E., Scholz D., Schaper J. The cytoskeleton and related proteins in the human failing heart. Heart Fail Rev 2000, 5:271-280.
56. Schaper J., Kostin S., Hein S., Elsasser A., Arnon E., Zimmermann R. Structural remodelling in heart failure. Exp Clin Cardiol 2002, 7:64-68.
57. Tagawa H., Koide M., Sato H., Zile M.R., Carabello B.A., Cooper Gt Cytoskeletal role in the transition from compensated to decompensated hypertrophy during adult canine left ventricular pressure overloading. Circ Res 1998, 82:751-761.
58. Winter L., Abrahamsberg C., Wiche G. Plectin isoform 1b mediates mitochondrion-intermediate filament network linkage and controls organelle shape. J Cell Biol 2008, 181:903-911.