Metabolic control analysis of respiration in human cancer tissue

Frontiers in Physiology

Volumn 4 JUN, Issue , 2013, Pages

  Kaambre, Tuuli ^a   Chekulayev, Vladimir ^a   Shevchuk, Igor ^a   Tepp, Kersti ^a   Timohhina, Natalja ^a   Varikmaa, Minna ^a   Bagur, Rafaela ^b   Klepinin, Aleksandr ^a   Anmann, Tiia ^a   Koit, Andre ^a   Kaldma, Andrus ^a   Guzun, Rita ^b   Valvere, Vahur ^c,d   Saks, Valdur ^a,b  

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

^b Domaine Universitaire   (France)

^c North Estonia Medical Centre   (Estonia)

^d Department of Immunotherapy   (Estonia)

Author keywords

Breast and colorectal cancer; Metabolic control analysis; OXPHOS; Respiratory chain; Warburg effect

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE;

ADULT; AGED; ANALYTIC METHOD; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER TISSUE; CELL ENERGY; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; METABOLIC CONTROL ANALYSIS; METABOLOMICS; MITOCHONDRIAL RESPIRATION; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN;

EID: 84884556164     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00151     Document Type: Article

References (52)

1. Acín-Pérez, R., Fernández-Silva, P., Peleato, M. L., Perez-Martos, A., and Enriquez, J. A. (2008). Respiratory active mitochondrial supercomplexes. Mol. Cell. 32, 529-539. doi: 10.1016/j.molcel.2008.10.021
2. 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. doi: 10.1016/j.bbabio.2006.09.008
3. 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. doi: 10.1113/eph8802511
4. Bellance, N., Pabst, L., Allen, G., Rossignol, R., and Nagrath, D. (2012). Oncosecretomics coupled to bioenergetics identifies alpha-amino adipic acid, isoleucine and GABA as potential biomarkers of cancer: differential expression of c-Myc, Oct1 and KLF4 coordinates metabolic changes. Biochim. Biophys. Acta 1817, 2060-2071. doi: 10.1016/j.bbabio.2012.07.004
5. Bera, S., Wallimann, T., Ray, S., and Ray, M. (2008). Enzymes of creatine biosynthesis, arginine and methionine metabolism in normal and malignant cells. FEBS J. 275, 5899-5909. doi: 10.1111/j.1742-4658.2008.06718.x
6. Dzeja, P. P., and Terzic, A. (2003). Phosphotransfer networks and cellular energetics. J. Exp. Biol. 206, 2039-2047. doi: 10.1242/jeb.00426
7. Dudkina, N. V., Kudryashev, M., Stahlberg, H., and Boekema, E. J. (2011). Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc. Natl. Acad. Sci. U.S.A. 108, 15196-15200. doi: 10.1073/pnas.1107819108
8. Eimre, M., Paju, K., Pelloux, S., Beraud, N., Roosimaa, M., Kadaja, L., et al. (2008). Distinct organization of energy metabolism in HL-1 cardiac cell line and cardiomyocytes. Biochim. Biophys. Acta 1777, 514-524. doi: 10.1016/j.bbabio.2008.03.019
9. Fell, D. (1997). Understanding the Control of Metabolism. London; Miami: Portland Press.
10. Fell, D. (2005). "Metabolic control analysis" in Systems Biology, eds L. Alberghina and H. V. Westerhoff (Berlin: Springer-Verlag), 69-80.
11. Gellerich, F. N., Kunz, W. S., and Bohnensack, R. (1990). Estimation of flux control coefficients from inhibitor titrations by non-linear regression. FEBS Lett. 274, 167-170. doi: 10.1016/0014-5793(90)81355-R
12. Gnaiger, E., and Kemp, R. B. (1990). Anaerobic metabolism in aerobic mammalian cells: information from the ratio of calorimetric heat flux and respirometric oxygen flux. Biochim. Biophys. Acta 1016, 328-332. doi: 10.1016/0005-2728(90)90164-Y
13. Groen, A. K., Wanders, R. J., Westerhoff, H. V., Van Der Meer, R., and Tager, J. M. (1982). Quantification of the contribution of various steps to the control of mitochondrial respiration. J. Biol. Chem. 257, 2754-2757.
14. Gstraunthaler, G., Seppi, T., and Pfaller, W. (1999). Impact of culture conditions, culture media volumes, and glucose content on metabolic properties of renal epithelial cell cultures. Are renal cells in tissue culture hypoxic? Cell. Physiol. Biochem. 9, 150-172. doi: 10.1159/000016312
15. Guzun, R., Gonzalez-Granillo, M., Karu-Varikmaa, M., Grichine, A., Usson, Y., Kaambre, T., et al. (2012). Regulation of respiration in muscle cells in vivo by VDAC through interaction with the cytoskeleton and MtCK within mitochondrial interactosome. Biochim. Biophys. Acta 1818, 1545-1554. doi: 10.1016/j.bbamem.2011.12.034
16. 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. doi: 10.1016/j.bbabio.2011.01.010
17. Habano, W., Sugai, T., Nakamura, S., Uesugi, N., Higuchi, T., Terashima, M., et al. (2003). Reduced expression and loss of heterozygosity of the SDHD gene in colorectal and gastric cancer. Oncol. Rep. 10, 1375-1380.
18. Izuishi, K., Yamamoto, Y., Sano, T., Takebayashi, R., Nishiyama, Y., Mori, H., et al. (2012). Molecular mechanism underlying the detection of colorectal cancer by 18F-2-fluoro-2-deoxy-D-glucose positron emission tomography. J. Gastrointest. Surg. 16, 394-400. doi: 10.1007/s11605-011-1727-z
19. Jang, J. Y., Choi, Y., Jeon, Y. K., and Kim, C. W. (2008). Suppression of adenine nucleotide translocase-2 by vector-based siRNA in human breast cancer cells induces apoptosis and inhibits tumor growth in vitro and in vivo. Breast Cancer Res. 10:R11. doi: 10.1186/bcr1857
20. Jose, C., and Rossignol, R. (2013). Rationale for mitochondria-targeting strategies in cancer bioenergetic therapies. Int. J. Biochem. Cell. Biol. 45, 123-129. doi: 10.1016/j.biocel.2012.07.005
21. Kaambre, T., Chekulayev, V., Shevchuk, I., Karu-Varikmaa, M., Timohhina, N., Tepp, K., et al. (2012). Metabolic control analysis of cellular respiration in situ in intraoperational samples of human breast cancer. J. Bioenerg. Biomembr. 44, 539-558. doi: 10.1007/s10863-012-9457-9
22. Kholodenko, B. N., Demin, O. V., and Westerhoff, H. V. (1993). 'Channelled' pathways can be more sensitive to specific regulatory signals. FEBS Lett. 320, 75-78. doi: 10.1016/0014-5793(93)81661-I
23. Kholodenko, B. N., and Westerhoff, H. V. (1993). Metabolic channelling and control of the flux. FEBS Lett. 320, 71-74. doi: 10.1016/0014-5793(93)81660-R
24. Kunz, W. S., Kuznetsov, A. V., Clark, J. F., Tracey, I., and Elger, C. E. (1999). Metabolic consequences of the cytochrome c oxidase deficiency in brain of copper-deficient Mo(vbr) mice. J. Neurochem. 72, 1580-1585. doi: 10.1046/j.1471-4159.1999.721580.x
25. 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. doi: 10.1111/j.1432-1033.1996.00909.x
26. 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. doi: 10.1038/nprot.2008.61
27. Kuznetsov, A. V., Winkler, K., Kirches, E., Lins, H., Feistner, H., and Kunz, W. S. (1997). Application of inhibitor titrations for the detection of oxidative phosphorylation defects in saponin-skinned muscle fibers of patients with mitochondrial diseases. Biochim. Biophys. Acta 1360, 142-150. doi: 10.1016/S0925-4439(96)00072-5
28. Lenaz, G., and Genova, M. L. (2009). Structural and functional organization of the mitochondrial respiratory chain: a dynamic super-assembly. Int. J. Biochem. Cell. Biol. 41, 1750-1772. doi: 10.1016/j.biocel.2009.04.003
29. Lenaz, G., and Genova, M. L. (2010). Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid. Redox. Signal. 12, 961-1008. doi: 10.1089/ars.2009.2704
30. Lenaz, G., Baracca, A., Barbero, G., Bergamini, C., Dalmonte, M. E., Del Sole, M., et al. (2010). Mitochondrial respiratory chain super-complex I-III in physiology and pathology. Biochim. Biophys. Acta 1797, 633-640. doi: 10.1016/j.bbabio.2010.01.025
31. Marin-Hernandez, A., Rodriguez-Enriquez, S., Vital-Gonzalez, P. A., Flores-Rodriguez, F. L., Macias-Silva, M., Sosa-Garrocho, M., et al. (2006). Determining and understanding the control of glycolysis in fast-growth tumor cells. Flux control by an over-expressed but strongly product-inhibited hexokinase. FEBS J. 273, 1975-1988. doi: 10.1111/j.1742-4658.2006.05214.x
32. Monge, C., Beraud, N., Tepp, K., Pelloux, S., Chahboun, S., Kaambre, T., et al. (2009). Comparative analysis of the bioenergetics of adult cardiomyocytes and nonbeating HL-1 cells: respiratory chain activities, glycolytic enzyme profiles, and metabolic fluxes. Can. J. Physiol. Pharmacol. 87, 318-326. doi: 10.1139/Y09-018
33. Moreno-Sanchez, R., Rodriguez-Enriquez, S., Marin-Hernandez, A., and Saavedra, E. (2007). Energy metabolism in tumor cells. FEBS J. 274, 1393-1418. doi: 10.1111/j.1742-4658.2007.05686.x
34. Moreno-Sanchez, R., Saavedra, E., Rodriguez-Enriquez, S., Gallardo-Perez, J. C., Quezada, H., and Westerhoff, H. V. (2010). Metabolic control analysis indicates a change of strategy in the treatment of cancer. Mitochondrion 10, 626-639. doi: 10.1016/j.mito.2010.06.002
35. Moreno-Sanchez, R., Saavedra, E., Rodriguez-Enriquez, S., and Olin-Sandoval, V. (2008). Metabolic control analysis: a tool for designing strategies to manipulate metabolic pathways. J. Biomed. Biotechnol. 2008, 597913. doi: 10.1155/2008/597913
36. Patra, S., Bera, S., Sinharoy, S., Ghoshal, S., Ray, S., Basu, A., et al. (2008). Progressive decrease of phosphocreatine, creatine and creatine kinase in skeletal muscle upon transformation to sarcoma. FEBS J. 275, 3236-3247. doi: 10.1111/j.1742-4658.2008.06475.x
37. Pedersen, P. L. (2008). Voltage dependent anion channels (VDACs): a brief introduction with a focus on the outer mitochondrial compartment's roles together with hexokinase-2 in the "Warburg effect" in cancer. J. Bioenerg. Biomembr. 40, 123-126. doi: 10.1007/s10863-008-9165-7
38. Queiros, O., Preto, A., Pacheco, A., Pinheiro, C., Azevedo-Silva, J., Moreira, R., et al. (2012). Butyrate activates the monocarboxylate transporter MCT4 expression in breast cancer cells and enhances the antitumor activity of 3-bromopyruvate. J. Bioenerg. Biomembr. 44, 141-153. doi: 10.1007/s10863-012-9418-3
39. Rossignol, R., Letellier, T., Malgat, M., Rocher, C., and Mazat, J. P. (2000). Tissue variation in the control of oxidative phosphorylation: implication for mitochondrial diseases. Biochem. J. 347(Pt 1), 45-53. doi: 10.1042/0264-6021:3470045
40. 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. doi: 10.1073/pnas.0806303105
41. 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. doi: 10.1016/j.bbabio.2010.01.011
42. Salem, A. F., Whitaker-Menezes, D., Lin, Z., Martinez-Outschoorn, U. E., Tanowitz, H. B., Al-Zoubi, M. S., et al. (2012). Two-compartment tumor metabolism: autophagy in the tumor microenvironment and oxidative mitochondrial metabolism (OXPHOS) in cancer cells. Cell Cycle 11, 2545-2556. doi: 10.4161/cc.20920
43. Small, J. R. (1993). Flux control coefficients determined by inhibitor titration: the design and analysis of experiments to minimize errors. Biochem. J. 296(Pt 2), 423-433.
44. Small, J. R., and Fell, D. A. (1990). Covalent modification and metabolic control analysis. Modification to the theorems and their application to metabolic systems containing covalently modifiable enzymes. Eur. J. Biochem. 191, 405-411. doi: 10.1111/j.1432-1033.1990.tb19136.x
45. Sotgia, F., Whitaker-Menezes, D., Martinez-Outschoorn, U. E., Flomenberg, N., Birbe, R. C., Witkiewicz, A. K., et al. (2012). Mitochondrial metabolism in cancer metastasis: visualizing tumor cell mitochondria and the "reverse Warburg effect" in positive lymph node tissue. Cell Cycle 11, 1445-1454. doi: 10.4161/cc.19841
46. Tager, J. M., Wanders, R. J., Groen, A. K., Kunz, W., Bohnensack, R., Kuster, U., et al. (1983). Control of mitochondrial respiration. FEBS Lett. 151, 1-9. doi: 10.1016/0014-5793(83)80330-5
47. Tepp, K., Shevchuk, I., Chekulayev, V., Timohhina, N., Kuznetsov, A. V., Guzun, R., et al. (2011). High efficiency of energy flux controls within mitochondrial interactosome in cardiac intracellular energetic units. Biochim. Biophys. Acta 1807, 1549-1561. doi: 10.1016/j.bbabio.2011.08.005
48. Tepp, K., Timohhina, N., Chekulayev, V., Shevchuk, I., Kaambre, T., and Saks, V. (2010). Metabolic control analysis of integrated energy metabolism in permeabilized cardiomyocytes - experimental study. Acta Biochim. Pol. 57, 421-430.
49. Warburg, O. (1956). On the origin of cancer cells. Science 123, 309-314. doi: 10.1126/science.123.3191.309
50. Warburg, O. H., and Dickens, F. (1930). The Metabolism of Tumours. London: Constable.
51. Whitaker-Menezes, D., Martinez-Outschoorn, U. E., Lin, Z., Ertel, A., Flomenberg, N., Witkiewicz, A. K., et al. (2011). Evidence for a stromal-epithelial "lactate shuttle" in human tumors: MCT4 is a marker of oxidative stress in cancer-associated fibroblasts. Cell Cycle 10, 1772-1783. doi: 10.4161/cc.10.11.15659
52. Witkiewicz, A. K., Whitaker-Menezes, D., Dasgupta, A., Philp, N. J., Lin, Z., Gandara, R., et al. (2012). Using the "reverse Warburg effect" to identify high-risk breast cancer patients: stromal MCT4 predicts poor clinical outcome in triple-negative breast cancers. Cell Cycle 11, 1108-1117. doi: 10.4161/cc.11.6.19530.