• Journal of Innovative Optical Health Sciences
  • Vol. 17, Issue 1, 2350030 (2024)
Kathryn M. Priest, Jacob V. Schluns, Nathania Nischal, Colton L. Gattis, Jeffrey C. Wolchok, and Timothy J. Muldoon*
Author Affiliations
  • Department of Biomedical Engineering, University of Arkansas, Fayetteville, AR, USA
  • show less
    DOI: 10.1142/S179354582350030X Cite this Article
    Kathryn M. Priest, Jacob V. Schluns, Nathania Nischal, Colton L. Gattis, Jeffrey C. Wolchok, Timothy J. Muldoon. In vivo measurement of NADH fluorescence lifetime in skeletal muscle via fiber-coupled time-correlated single photon counting[J]. Journal of Innovative Optical Health Sciences, 2024, 17(1): 2350030 Copy Citation Text show less
    References

    [1] M. Morán, D. Moreno-Lastres, L. Marín-Buera, J. Arenas, M. A. Martín, C. Ugalde. Mitochondrial respiratory chain dysfunction: Implications in neurodegeneration. Free Radic. Biol. Med., 53, 595-609(2012).

    [2] I. Georgakoudi, K. P. Quinn. Optical imaging using endogenous contrast to assess metabolic state. Annu. Rev. Biomed. Eng., 14, 351-367(2012).

    [3] K. Alhallak, L. G. Rebello, T. J. Muldoon, K. P. Quinn, N. Rajaram. Optical redox ratio identifies metastatic potential-dependent changes in breast cancer cell metabolism. Biomed. Opt. Exp., 7, 4364-4374(2016).

    [4] J. S. Baker, M. C. McCormick, R. A. Robergs. Interaction among skeletal muscle metabolic energy systems during intense exercise. J. Nutr. Metab., 2010, 905612(2010).

    [5] J. Zheng. Energy metabolism of cancer: Glycolysis versus oxidative phosphorylation (Review). Oncol. Lett., 4, 1151-1157(2012).

    [6] B. Egan, J. R. Zierath. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab., 17, 162-184(2013).

    [7] R. J. DeBerardinis, C. B. Thompson. Cellular metabolism and disease: What do metabolic outliers teach us?. CellPress, 148, 1132-1144(2012).

    [8] M. T. Lewis, J. D. Kasper, J. N. Bazil, J. C. Frisbee, R. W. Wiseman. Quantification of mitochondrial oxidative phosphorylation in metabolic disease: Application to type 2 diabetes. Int. J. Mol. Sci., 20, 5271(2019).

    [9] E. P. Widmaier, S. Vander Luciano. Human Physiology: The Mechanisms of Body Function(2004).

    [10] L. D. Osellame, T. S. Blacker, M. R. Duchen. Cellular and molecular mechanisms of mitochondrial function. Best. Pract. Res. Clin. Endocrinol., 26, 711-723(2012).

    [11] E. A. Shoubridge. Supersizing the mitochondrial respiratory chain. Cell Metab., 15, 271-272(2012).

    [12] E. Lapuente-Brun, R. Moreno-Loshuertos, R. Acín-Pérez, A. Latorre-Pellicer, C. Colás, E. Balsa, E. Perales-Clemente, P. M. Quirós, E. Calvo, M. A. Rodríguez-Hernández, P. Navas, R. Cruz, A.́ Carracedo, C. López-Otín, A. Pérez-Martos, P. Fernández-Silva, E. Fernández-Vizarra, J. A. Enríquez. “Supercomplex assembly determines electron flux in the mitochondrial electron transport chain,”. Science, 340, 1567-1570(2013).

    [13] R. M. Stroud. Balancing ATP in the cell. Nat. Struct. Biol., 3, 567-569(1996).

    [14] J. Berg, Y. P. Hung, G. Yellen. A genetically encoded fluorescent reporter of ATP:ADP ratio. Nat. Methods, 6, 161-166(2009).

    [15] B. S. Khakh, G. Burnstock. The double life of ATP. Sci. Am., 301, 84-90(2009).

    [16] H. Imamura, K. P. Huynh Nhat, H. Togawa, K. Saito, R. Iino, Y. Kato-Yamada, T. Nagai, H. Noji. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc. Natl. Acad. USA, 106, 15651-15656(2009).

    [17] O. I. Kolenc, K. P. Quinn. Evaluating cell metabolism through autofluorescence imaging of NAD(P)H and FAD. Antioxid. Redox Signal., 30, 875-889(2019).

    [18] 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).

    [19] C. H. Barlow, B. Chance. Ischemic areas in perfused rat hearts: measured by NADH fluorescence photography. Science, 193, 909-910(1976).

    [20] B. Chance, V. Legallais, J. Sorge, N. Graham. A versatile time-sharing multichannel spectrophotometer, reflectometer, and fluorometer. Anal. Biochem., 66, 498-514(1975).

    [21] B. Chance, S. Nioka, J. Kent, K. McCully, M. Fountain, R. Greenfeld, G. Holtom. Time-resolved spectroscopy of hemoglobin and myoglobin in resting and ischemic muscle. Anal. Biochem., 174, 698-707(1988).

    [22] A. Villringer, B. Chance. Non-invasive optical spectroscopy and imaging of human brain function. Trends Neurosci., 20, 435-442(1997).

    [23] K. P. Quinn, G. V. Sridharan, R. S. Hayden, D. L. Kaplan, K. Lee, I. Georgakoudi. Quantitative metabolic imaging using endogenous fluorescence to detect stem cell differentiation. Sci. Rep., 3, 3432(2013).

    [24] H. B. S. Griffiths, C. Williams, S. J. King, S. J. Allison. Nicotinamide adenine dinucleotide (NAD+): Essential redox metabolite, co-substrate and an anti-cancer and anti-ageing therapeutic target. Biochem. Soc. Trans., 48, 733-744(2020).

    [25] B. R. Masters, P. T. C. So, E. Gratton. Optical biopsy of in vivo human skin multiphoton excitation microscopy. Lasers Med. Sci., 13, 196-203(1998).

    [26] J. D. Jones, H. E. Ramser, A. E. Woessner, A. Veves, K. P. Quinn. Quantifying Age-related changes in skin wound metabolism using in vivo multiphoton microscopy. Adv. Wound Care, 9, 90-102(2020).

    [27] M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, V. Shcheslavskiy. Interrogation of metabolic and oxygen states of tumors with fiber-based luminescence lifetime spectroscopy. Opt. Lett., 42, 731-734(2017).

    [28] P. M. Schaefer, S. Kalinina, A. Rueck, C. A. F. von Arnim, B. von Einem. NADH autofluorescence: A marker on its way to boost bioenergetic research. Cytometry A, 95, 34-46(2019).

    [29] J. Deal, S. Mayes, C. Browning, S. Hill, P. Rider, C. Boudreaux, T. C. Rich, S. J. Leavesley. Identifying molecular contributors to autofluorescence of neoplastic and normal colon sections using excitation-scanning hyperspectral imaging. J. Biomed. Opt., 24, 1-11(2018).

    [30] H. Westerblad, J. D. Bruton, A. Katz. Skeletal muscle: Energy metabolism, fiber types, fatigue. Exp. Cell Res., 316, 3093-3099(2010).

    [31] M. Müller, M. Mentel, J. J. van Hellemond, K. Henze, C. Woehle, S. B. Gould, R.-Y. Yu, M. van der Giezen, A. G. M. Tielens, W. F. Martin. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev., 76, 444-495(2012).

    [32] M. Ahmad, A. Wolberg, C. I. Kahwaji. Biochemistry, Electron Transport Chain(2022).

    [33] J. T. Kim, B. M. Kasukonis, L. A. Brown, T. A. Washington, J. C. Wolchok. Recovery from volumetric muscle loss injury: A comparison Between young and aged rats. Exp. Gerontol., 83, 37-46(2016).

    [34] B. Kasukonis, J. Kim, L. Brown, J. Jones, S. Ahmadi, T. Washington, J. Wolchok. Codelivery of Infusion Decellularized skeletal muscle with minced muscle autographs improved recovery from volumetric muscle loss injury in a rat model. Tissue Eng. A, 22, 1151-1163(2016).

    [35] X. Wu, B. T. Corona, X. Chen, T. J. Walters. A standardized rat model of volumetric muscle loss injury for the development of tissue engineering therapies. Biores. Open Access, 1, 280-290(2012).

    [36] T. A. Washington, R. A. Perry, J. T. Kim, W. S. Haynie, N. P. Greene, J. C. Wolchok. The effect of autologous repair and voluntary wheel running on torque recovery in a rat model of volumetric muscle loss. Exp. Physiol., 106, 994-1004(2021).

    [37] V. V. Ghukasyan, F.-J. Kao. Monitoring cellular metabolism with fluorescence lifetime of reduced nicotinamide adenine dinucleotide. J. Phys. Chem. C, 113, 11532-11540(2009).

    [38] T. S. Blacker, R. J. Marsh, M. R. Duchen, A. J. Bain. Activa-ted barrier crossing dynamics in the non-radiative decay of NADH and NADPH. Chem. Phys., 422, 184-194(2013).

    [39] G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, R. M. Costa. Deep brain optical measurements of cell type—specific neural activity in behaving mice. Nat. Protoc., 9, 1213-1228(2014).

    [40] G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, S. S. Vogel, D. M. Lovinger, R. M. Costa. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature, 494, 238-242(2013).

    [41] D. Duboc, M. Muffat-Joly, G. Renault, M. Degeorges, M. Toussaint, J. J. Pocidalo. In situ NADH laser fluorimetry of rat fast- and slow-twitch muscles during tetanus. J. Appl. Physiol., 64, 2692-2695(1988).

    [42] Y. Chen, Q. Yu, C.-B. Xu. A convenient method for quantifying collagen fibers in atherosclerotic lesions by ImageJ software. Int. J. Clin. Exp. Med., 10, 14904-14910(2017).

    [43] S. Wichaiyo, S. Lax, S. J. Montague, Z. Li, B. Grygielska, J. A. Pike, E. J. Haining, A. Brill, S. P. Watson, J. Rayes. Platelet glycoprotein VI and C-type lectin-like receptor 2 deficiency accelerates wound healing by impairing vascular integrity in mice. Platelet Biol. Disord., 104, 1648-1660(2019).

    [44] A. Rudkouskaya, J. T. Smith, X. Intes, M. Barroso. Quantification of Trastuzumab-HER2 engagement in vitro and in vivo. Molecules, 25, 5976(2020).

    [45] D. Llères, S. Swift, A. I. Lamond. Detecting protein-protein interactions in vivo with FRET using multiphoton fluorescence lifetime imaging microscopy (FLIM). Curr. Protocols Cytom., 42, 12.10.1-12.10.10(2007).

    [46] H. E. Schepers, J. H. G. M. van Beek, J. B. Bassingthwaighte. Four methods to estimate the fractal dimension from self-affine signals. IEEE Eng. Med. Biol. Mag., 11, 57-64(1992).

    [47] D. W. Repperger, K. A. Farris, C. C. Barton, S. F. Tebbens. Time series data analysis using fractional calculus concepts and fractal analysis. IEEE Int. Conf. Systems, Man and Cybernetics, 3311-3315(2009).

    [48] T. Higuchi. Approach to an irregular time series on the basis of the fractal theory. Physica D: Nonlinear Phenomena, 31, 277-283(1998).

    [49] T. S. Blacker, M. R. Duchen. Investigating mitochondrial redox state using NADH and NADPH autofluorescence. Free Radic. Biol. Med., 100, 53-65(2016).

    [50] M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, N. Ramanujam. In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proc. Natl. Acad. Sci., 104, 19494-19499(2007).

    [51] K. E. Conley, W. F. Kemper, G. J. Crowther. Limits to sustainable muscle performance: Interaction between glycolysis and oxidative phosphorylation. J. Exp. Biol., 204, 3189-3194(2001).

    [52] M. Sekine, T. Tamura, M. Akay, T. Fujimoto, T. Togawa, Y. Fukui. Discrimination of walking patterns using wavelet-based fractal analysis. IEEE Trans. Neural Syst. Rehabil. Eng., 10, 188-196(2002).

    [53] S. A. Eming, T. A. Wynn, P. Martin. Inflammation and metabolism in tissue repair and regeneration. Science, 356, 1026-1030(2017).

    [54] G. Soto-Heredero, M. M. Gómez de las Heras, E. Gabandé-Rodríguez, J. Oller, M. Mittelbrunn. Glycolysis — a key player in the inflammatory response. FEBS J., 287, 3350-3369(2020).

    [55] C. Smith, M. J. Kruger, R. M. Smith, K. H. Myburgh. The inflammatory response to skeletal muscle injury. Sports Med., 38, 947-969(2008).

    [56] K. Ohlendieck. Proteomics of skeletal muscle glycolysis. Biochim. Biophys. Acta (BBA) — Proteins Proteomics, 1804, 2089-2101(2010).

    [57] A. Torrelo, I. Colmenero, L. Requena, A. S. Paller, Y. Ramot, C.-C. R. Lee, A. Vera, A. Zlotogorski, R. Goldbach-Mansky, H. Kutzner. The histological and immunohistochemical features of the skin lesions in CANDLE syndrome. Am. J. Dermatopathol., 37, 517-522(2015).

    [58] A. Viola, F. Munari, R. Sanchez-Rodriguez, T. Scolaro, A. Castegna. Metabolic signature of macrophage responses. Front. Immunol., 10, 1462(2019).

    [59] Y.-F. Chen, C.-W. Lee, H.-H. Wu, W.-T. Lin, O. K. Lee. Immunometabolism of macrophages regulates skeletal muscle regeneration. Front. Cell Dev. Biol., 10, 948819(2022).

    [60] A. L. Goldberger, L. A. N. Amaral, J. M. Hausdorff, P. C. Ivanov, C.-K. Peng, H. E. Stanley. Fractal dynamics in physiology: Alterations with disease and aging. Proc. Natl. Acad. Sci., 99, 2466-2472(2002).

    [61] S. Spasic, A. Kalauzi, G. Grbic, L. Martac, M. Culic. Fractal analysis of rat brain activity after injury. Med. Biol. Eng. Comput., 43, 345-348(2005).

    [62] C. Lenz, A. Rebel, K. van Ackern, W. Kuschinsky, K. Waschke. Local cerebral blood flow, local cerebral glucose utilization, and flow-metabolism coupling during sevoflurane versus isoflurance anesthesia in rats. Anesthesiology, 89, 1480-1488(1998).

    [63] M. Maciejewski, H Qui, I. Rujan, M. Mobli, J. Hoch. Nonuniform sampling and spectral aliasing. J. Magn. Reson., 199, 1090-7807(2009).

    [64] S. Luo, P. Johnston. A review of electrocardiogram filtering. J. Electrocardiol., 43, 486-496(2010).

    [65] M. Seeck, L. Koessler, T. Bast, F. Leijten, C. Michel, C. Baumgartner, B. He, S. Beniczky. The standardized EEG electrode array of the IFCN. Clin. Neurophysiol., 128, 2070-2077(2017).

    [66] G. Yang, S. Yu, H. Dong, G. Slabaugh, P. Dragotti, X. Ye, F. Liu, S. Arridge, J. Keegan, Y. Guo, D. Firmin. DAGAN: Deep de-aliasing generative adversarial networks for fast compressed sensing MRI reconstruction. IEEE Trans. Med. Imaging, 37, 1310-1321(2018).

    [67] I. Gorbunova, M. Sasin, J. Rubayo-Soneira, A. Smolin, O. Vasyutinskii. Two-photon excited fluorescence dynamics in NADH in water-mathanol solutions: The role of conformation states. J. Phys. Chem., 124, 10682-10697(2020).

    [68] A. Belashov, A. Zhikhoreva, A. Salova, T. Belyaeva, I. Litvinov, E. Kornilova, I. Semenova, O. Vasyutinskii. Analysis of Radachlorin localization in living cells by fluorescence lifetime imaging microscopy. J. Photochem. Photobiol., B Biol., 243, 112699(2023).

    Kathryn M. Priest, Jacob V. Schluns, Nathania Nischal, Colton L. Gattis, Jeffrey C. Wolchok, Timothy J. Muldoon. In vivo measurement of NADH fluorescence lifetime in skeletal muscle via fiber-coupled time-correlated single photon counting[J]. Journal of Innovative Optical Health Sciences, 2024, 17(1): 2350030
    Download Citation