From identification of fluorescent flavoproteins to mitochondrial redox indicators in intact tissues

Ilmo E. Hassinen

doi:10.1142/s1793545813500582

[1] B. Chance, L. Ernster, P. B. Garland, C. P. Lee, P. A. Light, T. Ohnishi, C. I. Ragan, D. Wong, "Flavoproteins of the mitochondrial respiratory chain," Proc. Natl. Acad. Sci. USA 57, 1498–1505 (1967).

[2] P. B. Garland, B. Chance, L. Ernster, C. P. Lee, D. Wong, "Flavoproteins of mitochondrial fatty acid oxidation," Proc. Natl. Acad. Sci. USA 58, 1696– 1702 (1967).

[3] I. Hassinen, B. Chance, "Oxidation-reduction properties of the mitochondrial flavoprotein chain," Biochem. Biophys. Res. Commun. 31, 895–900 (1968).

[4] H. Voltti, I. E. Hassinen, "Oxidation-reduction midpoint potentials of mitochondrial flavoproteins and their intramitochondrial localization," J. Bioenerg. Biomembr. 10, 45–58 (1978).

[5] I. E. Hassinen, K. Hiltunen, "Respiratory control in isolated perfused rat heart. Role of the equilibrium relations between the mitochondrial electron carriers and the adenylate system," Biochim. Biophys. Acta 408, 319–330 (1975).

[6] C. I. Ragan, P. B. Garland, "The intra-mitochondrial localization of flavoproteins previously assigned to the respiratory chain," Eur. J. Biochem. 10, 399–410 (1969).

[7] R. Baradaran, J. M. Berrisford, G. S. Minhas, L. A. Sazanov, "Crystal structure of the entire respiratory complex I," Nature 494, 443–448 (2013).

[8] R. Scholz, R. G. Thurman, J. R. Williamson, B. Chance, T. Bücher, "Flavin and pyridine nucleotide oxidation-reduction changes in perfused rat liver. I. Anoxia and subcellular localization of fluorescent flavoproteins," J. Biol. Chem. 244, 2317–2324 (1969).

[9] H. Franke, C. H. Barlow, B. Chance, "Fluorescence of pyridine nucleotide and flavoproteins as an indicator of substrate oxidation and oxygen demand of the isolated perfused rat kidney," Int. J. Biochem. 12, 269–275 (1980).

[10] A. Mayevsky, H. Kaplan, J. Haveri, J. Haselgrove, B. Chance, "Three-dimensional metabolic mapping of the freeze-trapped brain: Effects of ischemia in the mongolian gerbil," Brain Res. 367, 63–72 (1986).

[11] H. N. Xu, S. Nioka, B. Chance, L. Z. Li, "Heterogeneity of mitochondrial redox state in premalignant pancreas in a PTEN null transgenic mouse model," Adv. Exp. Med. Biol. 701, 207–213 (2011).

[12] I. Hassinen, R. H. Ylikahri, "Absorption spectrophotometry of perfused rat liver applied to fructoseinduced inhibition of respiration," Biochem. Biophys. Res. Commun. 38, 1091–1097 (1970).

[13] K. Kiviluoma, I. Hassinen, "Role of acetaldehyde and acetate in the development of ethanol-induced cardiac lipidosis, studied in isolated perfused rat hearts," Alcohol Clin. Exp. Res. 7, 169–175 (1983).

[14] I. E. Hassinen, "Reflectance spectrophotometric and surface fluorometric methods for measuring the redox state of nicotinamide nucleotides and flavins in intact tissues," Methods Enzymol. 123, 311–320 (1986).

[15] E. M. Nuutinen, "Subcellular origin of the surface fluorescence of reduced nicotinamide nucleotides in the isolated perfused rat heart," Basic Res. Cardiol. 79, 49–58 (1984).

[16] I. Hassinen, K. Ito, S. Nioka, B. Chance, "Mechanism of fatty acid effect on myocardial oxygen consumption. A phosphorus NMR study," Biochim. Biophys. Acta 1019, 73–80 (1990).

[17] J. B. Chapman, "Fluorometric studies of oxidative metabolism in isolated papillary muscle of the rabbit," J. Gen. Physiol. 59, 135–154 (1972).

[18] W. S. Kunz, W. Kunz, "Contribution of different enzymes to flavoprotein fluorescence of isolated rat liver mitochondria," Biochim. Biophys. Acta 841, 237–246 (1985).

[19] W. S. Kunz, "Evaluation of electron-transfer flavoprotein and alpha-lipoamide dehydrogenase redox states by two-channel fluorimetry and its application to the investigation of beta-oxidation," Biochim. Biophys. Acta 932, 8–16 (1988).

[20] W. S. Kunz, "Spectral properties of fluorescent flavoproteins of isolated rat liver mitochondria," FEBS Lett. 195, 92–96 (1986).

[21] C. I. Ragan, P. B. Garland, "Spectroscopic studies of flavoproteins and non-haem iron proteins of submitochondrial particles of torulopsis utilis modified by iron- and sulphate-limited growth in continuous culture," Biochem. J. 124, 171–187 (1971).

[22] K. H. Vuorinen, A. Ala-R mi, Y. Yan, P. Ingman, I. E. Hassinen, "Respiratory control in heart muscle during fatty acid oxidation. Energy state or substrate- level regulation by Ca2t " J. Mol. Cell. Cardiol. 27, 1581–1591 (1995).

[23] A. Ala-R mi, M. Ylihautala, P. Ingman, I. E. Hassinen, "Influence of calcium-induced workload transitions and fatty acid supply on myocardial substrate selection," Metabolism 54, 410–420 (2005).

[24] J. Koziol, "Fluorometric analyses of riboflavin and its coenzymes," Methods Enzymol. 18, 253–285 (1971).

[25] A. de Kok, A. J. Visser, "Flavin binding site differences between lipoamide dehydrogenase and glutathione reductase as revealed by static and timeresolved flavin fluorescence," FEBS Lett. 218, 135– 138 (1987).

[26] A. K. Lam, P. N. Silva, S. M. Altamentova, J. V. Rocheleau, "Quantitative imaging of electron transfer flavoprotein autofluorescence reveals the dynamics of lipid partitioning in living pancreatic islets," Integr. Biol. (Camb.) 4, 838–846 (2012).

[27] T. Bücher, B. Brauser, A. Conze, F. Klein, O. Langguth, H. Sies, "State of oxidation-reduction and state of binding in the cytosolic NADH-system as disclosed by equilibration with extracellular lactate- pyruvate in hemoglobin-free perfused rat liver," Eur. J. Biochem. 27, 301–317 (1972).

[28] J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, J. Zhou, "The bisretinoids of retinal pigment epithelium," Prog. Retin. Eye Res. 31, 121–135 (2012).

[29] K. Arai, T. Kanaseki, S. Ohkuma, "Isolation of highly purified lysosomes from rat liver: Identifi- cation of electron carrier components on lysosomal membranes," J. Biochem. 110, 541–547 (1991).

[30] H. J. Shin, J. L. Mego, "A rat liver lysosomal membrane flavin-adenine dinucleotide phosphohydrolase: Purification and characterization," Arch. Biochem. Biophys. 267, 95–103 (1988).

[31] B. Chance, B. Schoener, R. Oshino, F. Itshak, Y. Nakase, "Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals," J. Biol. Chem. 254, 4764–4771 (1979).

[32] B. Quistorff, B. Chance, "Simple techniques for freeze clamping and for cutting and milling of frozen tissue at low temperature for the purpose of two- or three-dimensional metabolic studies in vivo," Anal. Biochem. 108, 237–248 (1980).

[33] B. Quistorff, H. Poulsen, "Evaluation of a freezeclamping technique designed for two- and threedimensional metabolic studies of rat liver in vivo. quenching efficiency and effect of clamping on tissue morphology," Anal. Biochem. 108, 249–256 (1980).

[34] L. Z. Li, R. Zhou, T. Zhong, L. Moon, E. J. Kim, H. Qiao, S. Pickup, M. J. Hendrix, D. Leeper, B. Chance, J. D. Glickson, "Predicting melanoma metastatic potential by optical and magnetic resonance imaging," Adv. Exp. Med. Biol. 599, 67–78 (2007).

[35] H. N. Xu, G. Zheng, J. Tchou, S. Nioka, L. Z. Li, "Characterizing the metabolic heterogeneity in human breast cancer xenografts by 3D high resolution fluorescence imaging," Springerplus 2, 73 (2013).

[36] M. Mokry, P. Gal, B. Vidinsky, J. Kusnir, K. Dubayova, S. Mozes, J. Sabo, "In vivo monitoring the changes of interstitial pH and FAD/NADH ratio by fluorescence spectroscopy in healing skin wounds," Photochem. Photobiol. 82, 793–797 (2006).

[37] M. C. Skala, A. Fontanella, L. Lan, J. A. Izatt, M. W. Dewhirst, "Longitudinal optical imaging of tumor metabolism and hemodynamics," J. Biomed. Opt. 15, 011112 (2010).

[38] M. Minsky, "Memoir on inventing the confocal scanning microscope," Scanning 10, 128–138 (1988).

[39] K. M. Berland, P. T. So, E. Gratton, "Two-photon fluorescence correlation spectroscopy: Method and application to the intracellular environment," Biophys. J. 68, 694–701 (1995).

[40] A. V. Kuznetsov, J. Troppmair, R. Sucher, M. Hermann, V. Saks, R. Margreiter, "Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: Possible physiological role " Biochim. Biophys. Acta 1757, 686–691 (2006).

[41] F. Appaix, A. V. Kuznetsov, Y. Usson, L. Kay, T. Andrienko, J. Olivares, T. Kaambre, P. Sikk, R. Margreiter, V. Saks, "Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria," Exp. Physiol. 88, 175–190 (2003).

[42] A. V. Kuznetsov, O. Mayboroda, D. Kunz, K. Winkler, W. Schubert, W. S. Kunz, "Functional imaging of mitochondria in saponin-permeabilized mice muscle fibers," J. Cell. Biol. 140, 1091–1099 (1998).

[43] W. S. Kunz, K. Winkler, A. V. Kuznetsov, H. Lins, E. Kirches, C. W. Wallesch, "Detection of mitochondrial defects by laser fluorimetry," Mol. Cell. Biochem. 174, 97–100 (1997).