Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor

Hung, Yin Pun; Albeck, John G.; Tantama, Mathew; Yellen, Gary

doi:10.1016/j.cmet.2011.08.012

Cited by 513Advanced Fluorescence Microscopy TechniquesRedox biology and oxidative stressbioluminescence and chemiluminescence research

Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor

Open access

Hung, Yin Pun, Albeck, John G., Tantama, Mathew, Yellen, Gary·2011·Cell Metabolism

DOI 10.1016/j.cmet.2011.08.012PMC PMC3190165

Open this paper in CoChat — free account

Abstract

NADH is a key metabolic cofactor whose sensitive and specific detection in the cytosol of live cells has been difficult. We constructed a fluorescent biosensor of the cytosolic NADH-NAD(+) redox state by combining a circularly permuted GFP T-Sapphire with a bacterial NADH-binding protein, Rex. Although the initial construct reported [NADH] × [H(+)] / [NAD(+)], its pH sensitivity was eliminated by mutagenesis. The engineered biosensor Peredox reports cytosolic NADH:NAD(+) ratios and can be calibrated with exogenous lactate and pyruvate. We demonstrated its utility in several cultured and primary cell types. We found that glycolysis opposed the lactate dehydrogenase equilibrium to produce a reduced cytosolic NADH-NAD(+) redox state. We also observed different redox states in primary mouse astrocytes and neurons, consistent with hypothesized metabolic differences. Furthermore, using high-content image analysis, we monitored NADH responses to PI3K pathway inhibition in hundreds of live cells. As an NADH reporter, Peredox should enable better understanding of bioenergetics.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.cmet.2011.08.012

Cites

58 of 58 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Use of pure lactate as an alternative fuel, rather than a redox-balanced mixture of lactate and pyruvate, abnormally elevates the low cytosolic NADH redox ratio in neurons.
“However, the use of pure lactate as an alternative fuel, rather than a redox-balanced mixture of lactate and pyruvate, abnormally elevates the low cytosolic NADH redox ratio in neurons (seen in vitro by Hung et al. [2011] and Mongeon et al. [2016] as well as in vivo by Díaz-García et al. [2017]); this decreases the rate of neuronal glycolysis in a way that would not represent the normal effect in”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Hung et al., 2011

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Principles of Fluorescence Spectroscopy
Lakowicz, J. R. (1999) · Springer eBooks · doi:10.1007/978-1-4757-3061-6 · Cited by 26,948 · see citing works
Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197 · see citing works
On the origin of cancer cells
Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425 · see citing works
Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein
Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N. G., Palmer, A. E., & Tsien, R. Y. (2004) · Nature Biotechnology · doi:10.1038/nbt1037 · Cited by 4,619 · see citing works
Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization.
Pellerin, L., & Magistretti, P. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10625 · Cited by 2,927 · cited 1× · see citing works
“Primary Cultured Cortical Astrocytes and Neurons Differ in Their Cytosolic NADH-NAD Redox States Glucose metabolism has been proposed to differ in astrocytes and neurons (Pellerin and Magistretti, 1994; Herrero-Mendez et al., 2009).”
Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures
Debnath, J., Muthuswamy, S. K., & Brugge, J. S. (2003) · Methods · doi:10.1016/s1046-2023(03)00032-x · Cited by 2,001 · see citing works
The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver
Williamson, D., Lund, P., & Krebs, H. (1967) · Biochemical Journal · doi:10.1042/bj1030514 · Cited by 1,871 · see citing works
Genetically encoded fluorescent indicator for intracellular hydrogen peroxide
Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K., Terskikh, A. V., & Lukyanov, S. (2006) · Nature Methods · doi:10.1038/nmeth866 · Cited by 1,260 · see citing works
Short-chain dehydrogenases/reductases (SDR)
Jörnvall, H., Persson, B., Krook, M., Atrian, S., Gonzàlez‐Duarte, R., Jeffery, J., & Ghosh, D. (1995) · Biochemistry · doi:10.1021/bi00018a001 · Cited by 1,241 · see citing works
Regulation of the mTOR Complex 1 Pathway by Nutrients, Growth Factors, and Stress
Sengupta, S., Peterson, T. R., & Sabatini, D. M. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.026 · Cited by 1,234 · see citing works
Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity
Maira, S.-M., Stauffer, F., Brueggen, J., Furet, P., Schnell, C., Fritsch, C., Brachmann, S., Chène, P., De Pover, A., Schoemaker, K., et al. (2008) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-08-0017 · Cited by 1,134 · see citing works
Reducing the Environmental Sensitivity of Yellow Fluorescent Protein
Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A., & Tsien, R. Y. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102815200 · Cited by 1,023 · see citing works
Inhibition of Silencing and Accelerated Aging by Nicotinamide, a Putative Negative Regulator of Yeast Sir2 and Human SIRT1
Bitterman, K. J., Anderson, R. M., Cohen, H. Y., Latorre-Esteves, M., & Sinclair, D. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205670200 · Cited by 1,002 · see citing works
Circularly permuted green fluorescent proteins engineered to sense Ca 2+
Nagai, T., Sakaue-Sawano, A., Park, E. S., & Miyawaki, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051636098 · Cited by 969 · see citing works
Circular permutation and receptor insertion within green fluorescent proteins
Baird, G. S., Zacharias, D. A., & Tsien, R. Y. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11241 · Cited by 963 · see citing works
Intracellular Oxidation-Reduction States in Vivo
Chance, B., Cohen, P., Jöbsis, F. F., & Schoener, B. (1962) · Science · doi:10.1126/science.137.3529.499 · Cited by 947 · see citing works
Cytosolic phosphorylation potential.
Veech, R. L., Lawson, J., Cornell, N. W., & Krebs, H. A. (1979) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)50401-4 · Cited by 922 · see citing works
Nampt/PBEF/Visfatin Regulates Insulin Secretion in β Cells as a Systemic NAD Biosynthetic Enzyme
Revollo, J. R., Körner, A., Mills, K. F., Satoh, A., Wang, T., Garten, A., Dasgupta, B., Sasaki, Y., Wolberger, C., Townsend, R. R., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.09.003 · Cited by 911 · see citing works
The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1
Herrero-Mendez, A., Almeida, A., Fernández, E., Maestre, C., Moncada, S., & Bolaños, J. P. (2009) · Nature Cell Biology · doi:10.1038/ncb1881 · Cited by 844 · see citing works
Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis
Kasischke, K. A., Vishwasrao, H. D., Fisher, P. J., Zipfel, W. R., & Webb, W. W. (2004) · Science · doi:10.1126/science.1096485 · Cited by 742 · see citing works
Brain metabolism dictates the polarity of astrocyte control over arterioles
Gordon, G. R., Choi, H. B., Rungta, R. L., Ellis‐Davies, G. C. R., & MacVicar, B. A. (2008) · Nature · doi:10.1038/nature07525 · Cited by 739 · see citing works
Determination of the absolute quantum yield of fluorescent solutions
Weber, G., & Teale, F. W. J. (1957) · Transactions of the Faraday Society · doi:10.1039/tf9575300646 · Cited by 665 · see citing works
Regulation of Corepressor Function by Nuclear NADH
Zhang, Q., Piston, D. W., & Goodman, R. H. (2002) · Science · doi:10.1126/science.1069300 · Cited by 620 · see citing works
CellProfiler Analyst: data exploration and analysis software for complex image-based screens
Jones, T. R., Kang, I. H., Wheeler, D. B., Lindquist, R. A., Papallo, A., Sabatini, D. M., Golland, P., & Carpenter, A. E. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-482 · Cited by 541 · see citing works
THE FLUOROMETRIC MEASUREMENT OF PYRIDINE NUCLEOTIDES
Lowry, O. H., Roberts, N. R., & Kapphahn, J. I. (1957) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)64996-8 · Cited by 532 · see citing works
Role of NADH Shuttle System in Glucose-Induced Activation of Mitochondrial Metabolism and Insulin Secretion
Eto, K., Tsubamoto, Y., Terauchi, Y., 杉山, 拓., Kishimoto, T. E., Takahashi, N. K., Yamauchi, N., Kubota, N., Murayama, S., Aizawa, T., et al. (1999) · Science · doi:10.1126/science.283.5404.981 · Cited by 491 · see citing works
A genetically encoded fluorescent reporter of ATP:ADP ratio
Berg, J., Hung, Y. P., & Yellen, G. (2009) · Nature Methods · doi:10.1038/nmeth.1288 · Cited by 481 · see citing works
2-Deoxy-D-glucose reduces epilepsy progression by NRSF-CtBP–dependent metabolic regulation of chromatin structure
Garriga-Canut, M., Schoenike, B. A., Qazi, R., Bergendahl, K., Daley, T. J., Pfender, R. M., Morrison, J. F., Ockuly, J. C., Stafstrom, C. E., Sutula, T. P., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1791 · Cited by 446 · see citing works
Imaging Intracellular pH in Live Cells with a Genetically Encoded Red Fluorescent Protein Sensor
Tantama, M., Hung, Y. P., & Yellen, G. (2011) · Journal of the American Chemical Society · doi:10.1021/ja202902d · Cited by 411 · see citing works
Synthetic spectroscopic models related to coenzymes and base pairs. V. Emission properties of NADH. Studies of fluorescence lifetimes and quantum efficiencies of NADH, AcPyADH, [reduced acetylpyridineadenine dinucleotide] and simplified synthetic models
Scott, T. G., Spencer, R. D., Leonard, N. J., & Weber, G. (1970) · Journal of the American Chemical Society · doi:10.1021/ja00706a043 · Cited by 389 · see citing works
Accumulation of Free ADP-ribose from Mitochondria Mediates Oxidative Stress-induced Gating of TRPM2 Cation Channels
Perraud, A.-L., Takanishi, C. L., Shen, B. W., Kang, S. J., Smith, M., Schmitz, C., Knowles, H. M., Ferraris, D. V., Li, W., Zhang, J., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m411446200 · Cited by 358 · see citing works
An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts
Bartlett, W., & Banker, G. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-08-01944.1984 · Cited by 348 · see citing works
Transcription Corepressor CtBP Is an NAD+-Regulated Dehydrogenase
Kumar, V., Carlson, J. E., Ohgi, K. A., Edwards, T. A., Rose, D. W., Escalante, C. R., Rosenfeld, M. G., & Aggarwal, A. K. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00650-0 · Cited by 299 · see citing works
Crystal Structures of the GCaMP Calcium Sensor Reveal the Mechanism of Fluorescence Signal Change and Aid Rational Design
Akerboom, J., Rivera, J. D. V., Rodríguez‐Guilbe, M. M., Malavé, E. C. A., Hernández, H. H., Tian, L., Hires, S. A., Marvin, J. S., Looger, L. L., & Schreiter, E. R. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807657200 · Cited by 286 · see citing works
Separation of the glucose-stimulated cytoplasmic and mitochondrial NAD(P)H responses in pancreatic islet β cells
Patterson, G. H., Knobel, S. M., Arkhammar, P. O. G., Thastrup, M., & Piston, D. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.090098797 · Cited by 284 · see citing works
Regulation of redox metabolism in the mouse oocyte and embryo
Dumollard, R., Ward, Z., Carroll, J., & Duchen, M. R. (2006) · Development · doi:10.1242/dev.02744 · Cited by 246 · see citing works
GFP-like Proteins Stably Accumulate in Lysosomes
Katayama, H., Yamamoto, A., Mizushima, N., Yoshimori, T., & Miyawaki, A. (2008) · Cell Structure and Function · doi:10.1247/csf.07011 · Cited by 225 · see citing works
A novel sensor of NADH/NAD+ redox poise in Streptomyces coelicolor A3(2)
Brekasis, D., & Paget, M. S. B. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg453 · Cited by 224 · see citing works
Redox sensor CtBP mediates hypoxia-induced tumor cell migration
Zhang, Q., Wang, S.-Y., Nottke, A. C., Rocheleau, J. V., Piston, D. W., & Goodman, R. H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603269103 · Cited by 200 · see citing works
Biological Oxidation Systems
(1990) · Elsevier eBooks · doi:10.1016/b978-0-12-584552-6.x5001-0 · Cited by 195 · see citing works
Quantitative NAD(P)H/Flavoprotein Autofluorescence Imaging Reveals Metabolic Mechanisms of Pancreatic Islet Pyruvate Response
Rocheleau, J. V., Head, W. S., & Piston, D. W. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314005200 · Cited by 195 · see citing works
Efficiently folding and circularly permuted variants of the Sapphire mutant of GFP
Zapata-Hommer, O., & Griesbeck, O. (2003) · BMC Biotechnology · doi:10.1186/1472-6750-3-5 · Cited by 170 · see citing works
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
Bücher, T., Brauser, B., CONZE, A., KLEIN, F., Langguth, O., & Sies, H. (1972) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1972.tb01840.x · Cited by 165 · see citing works
Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors
Nausch, L., Ledoux, J., Bonev, A. D., Nelson, M. T., & Dostmann, W. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710387105 · Cited by 164 · see citing works
NAD(P)H fluorescence imaging of postsynaptic neuronal activation in murine hippocampal slices
Shuttleworth, C. W., Brennan, A. M., & Connor, J. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03196.2003 · Cited by 151 · see citing works
The redox switch/redox coupling hypothesis
Cerdán, S., Rodrigues, T. B., Sierra, A., Benito, M., Fonseca, L. L., Fonseca, C. P., & García-Martín, M. L. (2006) · Neurochemistry International · doi:10.1016/j.neuint.2005.12.036 · Cited by 146 · see citing works
Structure and functional properties of the Bacillus subtilis transcriptional repressor Rex
Wang, E., Bauer, M. C., Rogstam, A., Linse, S. S., Logan, D. T., & von Wachenfeldt, C. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06295.x · Cited by 143 · see citing works
BIOLOGICAL OXIDATIONS
Klingenberg, M., & Bücher, T. (1960) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.29.070160.003321 · Cited by 137 · see citing works
Fluorescence of Pyridine Nucleotides in Mitochondria
Avi‐Dor, Y., Olson, J. M., Doherty, M. D., & Kaplan, N. O. (1962) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)63448-4 · Cited by 127 · see citing works
Glucose-induced changes in cytosolic ATP content in pancreatic islets
Malaisse, W. J., & Sener, A. (1987) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(87)90134-0 · Cited by 116 · cited 1× · see citing works
“Although metabolic challenges often lead to energy deprivation and decrease in cytosolic ATP:ADP ratio, changes in cytosolic adenine nucleotide pool size are minimal (Schwenke et al., 1981; Malaisse and Sener, 1987) and would not be expected to interfere with Peredox response.”
Mitochondrial and cytosolic ATP/ADP ratios in rat liver in vivo
Schwenke, W. D., Soboll, S., Seitz, H. J., & Sies, H. (1981) · Biochemical Journal · doi:10.1042/bj2000405 · Cited by 114 · see citing works
Intracellular pH Sensing Using Autofluorescence Lifetime Microscopy
Ogikubo, S., Nakabayashi, T., Adachi, T., Islam, M. S., Yoshizawa, T., Kinjo, M., & Ohta, N. (2011) · The Journal of Physical Chemistry B · doi:10.1021/jp2058904 · Cited by 99 · see citing works
Structural Basis for NADH/NAD+ Redox Sensing by a Rex Family Repressor
McLaughlin, K. J., Strain-Damerell, C. M., Xie, K., Brekasis, D., Soares, A. S., Paget, M. S. B., & Kielkopf, C. L. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.006 · Cited by 93 · see citing works
X-Ray Structure of a Rex-Family Repressor/NADH Complex Insights into the Mechanism of Redox Sensing
Sickmier, E. A., Brekasis, D., Paranawithana, S. R., Bonanno, J. B., Paget, M. S. B., Burley, S. K., & Kielkopf, C. L. (2005) · Structure · doi:10.1016/j.str.2004.10.012 · Cited by 87 · see citing works
PROPERTIES OF THE COELENTERATE GREEN-FLUORESCENT PROTEINS
Ward, W. W. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-208820-9.50035-5 · Cited by 71 · see citing works
The conserved NAD(H)-dependent corepressor CTBP-1 regulates Caenorhabditis elegans life span
Chen, S., Whetstine, J. R., Ghosh, S. K., Hanover, J. A., Gali, R. R., Grosu, P., & Shi, Y. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802674106 · Cited by 65 · see citing works
Oxygen partial pressure and free intracellular adenosine of isolated cardiomyocytes
Smolenski, R. T., Schrader, J., de Groot, H., & Deussen, A. (1991) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1991.260.4.c708 · Cited by 50 · see citing works
Adenine nucleotides and the adenylate kinase equilibrium in livers of foetal and newborn rats
Ballard, F. J. (1970) · Biochemical Journal · doi:10.1042/bj1170231 · Cited by 39 · see citing works

Flagged first, then by citations

Sorted by citations

Understanding the Intersections between Metabolism and Cancer Biology
Heiden, M. G. V., & DeBerardinis, R. J. (2017) · Cell · doi:10.1016/j.cell.2016.12.039 · Cited by 2,316 · see citing works
Fueling Immunity: Insights into Metabolism and Lymphocyte Function
Pearce, E. L., Poffenberger, M. C., Chang, C.-H., & Jones, R. G. (2013) · Science · doi:10.1126/science.1242454 · Cited by 1,363 · see citing works
Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells
Sullivan, L. B., Gui, D. Y., Hosios, A. M., Bush, L. N., Freinkman, E., & Vander Heiden, M. G. (2015) · Cell · doi:10.1016/j.cell.2015.07.017 · Cited by 1,173 · see citing works
NAD(H) and NADP(H) Redox Couples and Cellular Energy Metabolism
Xiao, W., Wang, R., Handy, D. E., & Loscalzo, J. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7216 · Cited by 1,074 · see citing works
Brain Glucose Metabolism: Integration of Energetics with Function.
Dienel, G. (2019) · Physiological Reviews · doi:10.1152/physrev.00062.2017 · Cited by 806 · see citing works
Metabolomics and Isotope Tracing
Jang, C., Chen, L., & Rabinowitz, J. D. (2018) · Cell · doi:10.1016/j.cell.2018.03.055 · Cited by 841 · see citing works
PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes
Gupte, R., Liu, Z., & Kraus, W. L. (2017) · Genes & Development · doi:10.1101/gad.291518.116 · Cited by 681 · see citing works
The Redox Code
Jones, D. P., & Sies, H. (2015) · Antioxidants & Redox Signaling · doi:10.1089/ars.2015.6247 · Cited by 647 · see citing works
Separating NADH and NADPH fluorescence in live cells and tissues using FLIM
Blacker, T. S., Mann, Z. F., Gale, J. E., Ziegler, M., Bain, A. J., Szabadkai, G., & Duchen, M. R. (2014) · Nature Communications · doi:10.1038/ncomms4936 · Cited by 577 · see citing works
In vivo evidence for a lactate gradient from astrocytes to neurons
Mächler, P., Wyss, M. T., Elsayed, M., Stobart, J., Gutierrez, R., von Faber-Castell, A., Kaelin, V., Zuend, M., San Martín, A., Romero-Gómez, I., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.10.010 · Cited by 571 · see citing works
Increased demand for NAD(+) relative to ATP drives aerobic glycolysis
Luengo, A., Li, Z., Gui, D. Y., Sullivan, L. B., Zagorulya, M., Do, B. T., Ferreira, R., Naamati, A., Ali, A., Lewis, C. A., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.12.012 · Cited by 547 · see citing works
Complementation of mitochondrial electron transport chain by manipulation of the NAD + /NADH ratio
Titov, D. V., Cracan, V., Goodman, R. P., Peng, J., Grabarek, Z., & Mootha, V. K. (2016) · Science · doi:10.1126/science.aad4017 · Cited by 518 · see citing works
Genetically Encoded Fluorescent Biosensors Illuminate the Spatiotemporal Regulation of Signaling Networks
Greenwald, E. C., Mehta, S., & Zhang, J. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00333 · Cited by 488 · see citing works
Imaging energy status in live cells with a fluorescent biosensor of the intracellular ATP-to-ADP ratio
Tantama, M., Martínez‐François, J. R., Mongeon, R., & Yellen, G. (2013) · Nature Communications · doi:10.1038/ncomms3550 · Cited by 486 · see citing works
Neuronal Stimulation Triggers Neuronal Glycolysis and Not Lactate Uptake
Díaz-García, C. M., Mongeon, R., Lahmann, C., Koveal, D., Zucker, H., & Yellen, G. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.06.021 · Cited by 466 · see citing works
“The Peredox sensor (Hung et al., 2011) was expressed in mouse hippocampus and studied by imaging in acute hippocampal slices using a two-photon microscope equipped”
Influential
Glutamine‐driven oxidative phosphorylation is a major ATP source in transformed mammalian cells in both normoxia and hypoxia
Fan, J., Kamphorst, J. J., Mathew, R., Chung, M. K., White, E., Shlomi, T., & Rabinowitz, J. D. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.65 · Cited by 428 · see citing works
SoNar, a Highly Responsive NAD+/NADH Sensor, Allows High-Throughput Metabolic Screening of Anti-tumor Agents
Zhao, Y., Hu, Q., Cheng, F., Su, N., Wang, A., Zou, Y., Hu, H., Chen, X., Hai‐Meng, Z. H. O. U., Huang, X., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.04.009 · Cited by 434 · see citing works
Turn-On Fluorescence Sensor for Intracellular Imaging of Glutathione Using g-C3N4 Nanosheet–MnO2 Sandwich Nanocomposite
Zhang, X., Cheng, Z., Guo, S., Li, J., Yang, H., & Chen, G. (2014) · Analytical Chemistry · doi:10.1021/ac500336f · Cited by 415 · see citing works
The importance of serine metabolism in cancer
Mattaini, K. R., Sullivan, M. R., & Heiden, M. G. V. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201604085 · Cited by 409 · see citing works
Phosphoinositide 3-Kinase Regulates Glycolysis through Mobilization of Aldolase from the Actin Cytoskeleton
Hu, H., Juvekar, A., Lyssiotis, C. A., Lien, E. C., Albeck, J. G., Oh, D., Varma, G., Hung, Y. P., Ullas, S., Lauring, J. D., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.042 · Cited by 374 · see citing works
Biochemical adaptations of the retina and retinal pigment epithelium support a metabolic ecosystem in the vertebrate eye
Kanow, M. A., Giarmarco, M. M., Jankowski, C. S., Tsantilas, K., Engel, A. L., Du, J., Linton, J. D., Farnsworth, C. C., Sloat, S. R., Rountree, A., et al. (2017) · eLife · doi:10.7554/elife.28899 · Cited by 377 · see citing works
Understanding metabolic regulation and its influence on cell physiology
Metallo, C. M., & Vander Heiden, M. G. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.018 · Cited by 367 · see citing works
Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism
Yellen, G. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201803152 · Cited by 371 · see citing works
A genetically encoded FRET lactate sensor and its use to detect the Warburg effect in single cancer cells
San Martín, A., Ceballo, S., Ruminot, I., Lerchundi, R., Frommer, W. B., & Barros, L. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057712 · Cited by 361 · see citing works
The NAD+ precursor nicotinamide riboside rescues mitochondrial defects and neuronal loss in iPSC and fly models of Parkinson's disease
Schöndorf, D. C., Ivanyuk, D., Baden, P., Sanchez-Martinez, A., De Cicco, S., Yu, C., Giunta, I., Schwarz, L. K., Di Napoli, G., Panagiotakopoulou, V., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.009 · Cited by 337 · see citing works
Mechanoresponsive metabolism in cancer cell migration and metastasis
Zanotelli, M. R., Zhang, J., & Reinhart‐King, C. A. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.04.002 · Cited by 342 · see citing works
Genetically encoded fluorescent sensors reveal dynamic regulation of NADPH metabolism
Tao, R., Zhao, Y., Chu, H., Wang, A., Zhu, J., Chen, X., Zou, Y., Shi, M., Liu, R., Su, N., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4306 · Cited by 339 · see citing works
Plant mitochondria – past, present and future
Møller, I. M., Rasmusson, A. G., & Aken, O. V. (2021) · The Plant Journal · doi:10.1111/tpj.15495 · Cited by 332 · see citing works
Metabolic signaling by lactate in the brain
Barros, L. F. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.002 · Cited by 326 · see citing works
Quantitative determinants of aerobic glycolysis identify flux through the enzyme GAPDH as a limiting step
Shestov, A. A., Liu, X., Ser, Z., Cluntun, A. A., Hung, Y. P., Huang, L., Kim, D.-S., Le, A., Yellen, G., Albeck, J. G., et al. (2014) · eLife · doi:10.7554/elife.03342 · Cited by 315 · see citing works
Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms
Schmitt, F., Renger, G., Friedrich, T., Kreslavski, V. D., Zharmukhamedov, S. K., Los, D. A., Kuznetsov, V. V., & Allakhverdiev, S. I. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2014.02.005 · Cited by 314 · see citing works
HyPer-3: A Genetically Encoded H2O2 Probe with Improved Performance for Ratiometric and Fluorescence Lifetime Imaging
Bilan, D. S., Pase, L. B., Joosen, L., Gorokhovatsky, A. Y., Ermakova, Y. G., Gadella, T. W. J., Grabher, C., Schultz, C., Lukyanov, S., & Belousov, V. V. (2012) · ACS Chemical Biology · doi:10.1021/cb300625g · Cited by 280 · see citing works
Red fluorescent genetically encoded indicator for intracellular hydrogen peroxide
Ermakova, Y. G., Bilan, D. S., Matlashov, M. E., Mishina, N. M., Markvicheva, K. N., Subach, O. M., Subach, F. V., Bogeski, I., Hoth, M., Enikolopov, G., et al. (2014) · Nature Communications · doi:10.1038/ncomms6222 · Cited by 258 · see citing works
Cystathionine Beta-Synthase (CBS) Contributes to Advanced Ovarian Cancer Progression and Drug Resistance
Bhattacharyya, S., Saha, S., Giri, K., Lanza, I. R., Nair, K. S., Jennings, N. B., Rodriguez‐Aguayo, C., Lopez‐Berestein, G., Basal, E., Weaver, A. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079167 · Cited by 251 · see citing works
NADH Autofluorescence—A Marker on its Way to Boost Bioenergetic Research
Schaefer, P. M., Kalinina, S., Rueck, A. C., Arnim, C. A. F. V., & von Einem, B. (2018) · Cytometry Part A · doi:10.1002/cyto.a.23597 · Cited by 228 · see citing works
SIRT3‐dependent GOT2 acetylation status affects the malate–aspartate NADH shuttle activity and pancreatic tumor growth
Yang, H., Zhou, L., Shi, Q., Zhao, Y., Lin, H., Zhang, M., Zhao, S., Yang, Y. A., Ling, Z., Guan, K., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201591041 · Cited by 224 · see citing works
Modulating NAD+ metabolism, from bench to bedside
Katsyuba, E., & Auwerx, J. H. (2017) · The EMBO Journal · doi:10.15252/embj.201797135 · Cited by 224 · see citing works
Applications and advances of metabolite biosensors for metabolic engineering
Liu, D., Evans, T. D., & Zhang, F. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.06.008 · Cited by 214 · see citing works
Metabolic control by sirtuins and other enzymes that sense NAD+, NADH, or their ratio
Anderson, K. A., Madsen, A. S., Olsen, C. A., & Hirschey, M. D. (2017) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2017.09.005 · Cited by 210 · see citing works
SPG7 Is an Essential and Conserved Component of the Mitochondrial Permeability Transition Pore
Shanmughapriya, S., Rajan, S., Hoffman, N. E., Higgins, A. M., Tomar, D., Nemani, N., Hines, K. J., Smith, D. J., Eguchi, A., Vallem, S., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.08.009 · Cited by 209 · see citing works
Guidelines on experimental methods to assess mitochondrial dysfunction in cellular models of neurodegenerative diseases
Connolly, N. M. C., Theurey, P., Ádám‐Vizi, V., Bazan, N. G., Bernardi, P., Bolaños, J. P., Culmsee, C., Dawson, V. L., Deshmukh, M., Duchen, M. R., et al. (2017) · Cell Death and Differentiation · doi:10.1038/s41418-017-0020-4 · Cited by 208 · see citing works
Reactive oxygen species and redox compartmentalization
Kaludercic, N., Deshwal, S., & Lisa, F. D. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00285 · Cited by 213 · see citing works
Hepatic NADH reductive stress underlies common variation in metabolic traits
Goodman, R. P., Markhard, A. L., Shah, H., Sharma, R., Skinner, O. S., Clish, C. B., Deik, A., Patgiri, A., Hsu, Y.-H. H., Masia, R., et al. (2020) · Nature · doi:10.1038/s41586-020-2337-2 · Cited by 207 · see citing works
Imaging Mitochondrial Flux in Single Cells with a FRET Sensor for Pyruvate
San Martín, A., Ceballo, S., Baeza-Lehnert, F., Lerchundi, R., Valdebenito, R., Contreras-Baeza, Y., Alegría, K., & Barros, L. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085780 · Cited by 197 · see citing works
Genetically encoded fluorescent redox sensors
Lukyanov, K. A., & Belousov, V. V. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.05.030 · Cited by 199 · see citing works
Mitochondrial Energy and Redox Signaling in Plants
Schwarzländer, M., & Finkemeier, I. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.5104 · Cited by 192 · see citing works
Channel-Mediated Lactate Release by K + -Stimulated Astrocytes
Sotelo-Hitschfeld, T., Niemeyer, M. I., Mächler, P., Ruminot, I., Lerchundi, R., Wyss, M. T., Stobart, J. L., Fernández‐Moncada, I., Valdebenito, R., Garrido-Gerter, P., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5036-14.2015 · Cited by 188 · see citing works
A lysosomal switch triggers proteostasis renewal in the immortal C. elegans germ lineage
Bohnert, K. A., & Kenyon, C. J. (2017) · Nature · doi:10.1038/nature24620 · Cited by 177 · see citing works
Mapping metabolic changes by noninvasive, multiparametric, high-resolution imaging using endogenous contrast
Liu, Z., Pouli, D., Alonzo, C., Varone, A., Karaliota, S., Quinn, K. P., Münger, K., Karalis, K. P., & Georgakoudi, I. (2018) · Science Advances · doi:10.1126/sciadv.aap9302 · Cited by 175 · see citing works
In vivo monitoring of cellular energy metabolism using SoNar, a highly responsive sensor for NAD+/NADH redox state
Zhao, Y., Wang, A., Zou, Y., Su, N., Loscalzo, J., & Yang, Y. A. (2016) · Nature Protocols · doi:10.1038/nprot.2016.074 · Cited by 179 · see citing works
Adenosine signalling to astrocytes coordinates brain metabolism and function
Theparambil, S. M., Kopach, O., Braga, A., Nizari, S., Hosford, P. S., Sági‐Kiss, V., Hadjihambi, A., Konstantinou, C., Esteras, N., del Arroyo, A. G., et al. (2024) · Nature · doi:10.1038/s41586-024-07611-w · Cited by 176 · see citing works
Single-fluorophore biosensors for sensitive and multiplexed detection of signalling activities
Mehta, S., Zhang, Y., Roth, R. H., Zhang, J.-F., Mo, A., Tenner, B., Huganir, R. L., & Zhang, J. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0200-6 · Cited by 165 · see citing works
Pyoverdine, a siderophore from Pseudomonas aeruginosa , translocates into C. elegans , removes iron, and activates a distinct host response
Kang, D., Kirienko, D. R., Webster, P. J., Fisher, A. L., & Kirienko, N. V. (2018) · Virulence · doi:10.1080/21505594.2018.1449508 · Cited by 159 · see citing works
The Astrocyte: Powerhouse and Recycling Center
Weber, B., & Barros, L. F. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020396 · Cited by 195 · see citing works
Fluorescent proteins and genetically encoded biosensors
Wang, M., Da, Y., & Tian, Y. (2023) · Chemical Society Reviews · doi:10.1039/d2cs00419d · Cited by 156 · see citing works
An engineered enzyme that targets circulating lactate to alleviate intracellular NADH:NAD+ imbalance
Patgiri, A., Skinner, O. S., Miyazaki, Y., Schleifer, G., Marutani, E., Shah, H., Sharma, R., Goodman, R. P., To, T., Bao, X. R., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-019-0377-7 · Cited by 154 · see citing works
Spatiotemporal compartmentalization of hepatic NADH and NADPH metabolism
Goodman, R. P., Calvo, S. E., & Mootha, V. K. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.tm117.000258 · Cited by 148 · see citing works
Measuring Signaling and RNA-Seq in the Same Cell Links Gene Expression to Dynamic Patterns of NF-κB Activation
Lane, K. M., Valen, D. V., DeFelice, M. M., Macklin, D. N., Kudo, T., Jaimovich, A., Carr, A., Meyer, T., Pe’er, D., Boutet, S. C., et al. (2017) · Cell Systems · doi:10.1016/j.cels.2017.03.010 · Cited by 144 · see citing works
Ultrasensitive sensors reveal the spatiotemporal landscape of lactate metabolism in physiology and disease
Xie, L., Zhang, Y., Xu, L., Wang, A., Zou, Y., Li, T., Huang, L. Z., Chen, W., Liu, S., Jiang, K., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.10.002 · Cited by 148 · see citing works
Redox Paradox: A Novel Approach to Therapeutics-Resistant Cancer
Chaiswing, L., Clair, W. H. S., & Clair, D. K. S. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7485 · Cited by 147 · see citing works
Metabolic regulation of species-specific developmental rates
Díaz-Cuadros, M., Miettinen, T. P., Skinner, O. S., Sheedy, D., Díaz‐García, C. M., Gapon, S., Hubaud, A., Yellen, G., Manalis, S. R., Oldham, W. M., et al. (2023) · Nature · doi:10.1038/s41586-022-05574-4 · Cited by 145 · see citing works
Neuronal energy consumption: biophysics, efficiency and evolution
Niven, J. E. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.09.004 · Cited by 135 · see citing works
Circularly Permuted Fluorescent Protein-Based Indicators: History, Principles, and Classification
Kostyuk, A. I., Демидович, А. Д., Kotova, D. A., Belousov, V. V., & Bilan, D. S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174200 · Cited by 134 · see citing works
Location, Location, Location: Compartmentalization of NAD+ Synthesis and Functions in Mammalian Cells
Cambronne, X. A., & Kraus, W. L. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.05.010 · Cited by 137 · see citing works
Semisynthetic biosensors for mapping cellular concentrations of nicotinamide adenine dinucleotides
Sallin, O., Reymond, L., Gondrand, C., Raith, F., Koch, B., & Johnsson, K. (2018) · eLife · doi:10.7554/elife.32638 · Cited by 135 · see citing works
Recent advances in fluorescent probes for cellular antioxidants: Detection of NADH, hNQO1, H2S, and other redox biomolecules
Park, S. Y., Yoon, S. A., Cha, Y., & Lee, M. H. (2020) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2020.213613 · Cited by 134 · see citing works
A genetically encoded tool for manipulation of NADP+/NADPH in living cells
Cracan, V., Titov, D. V., Shen, H., Grabarek, Z., & Mootha, V. K. (2017) · Nature Chemical Biology · doi:10.1038/nchembio.2454 · Cited by 132 · see citing works
Aifm2, a NADH Oxidase, Supports Robust Glycolysis and Is Required for Cold- and Diet-Induced Thermogenesis
Nguyen, H. P., Yi, D., Lin, F., Viscarra, J. A., Nakamura-Tabuchi, C., Ngo, K., Shin, G., Lee, A. Y.-F., Wang, Y., & Sul, H. S. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.002 · Cited by 131 · see citing works
Redox Homeostasis in Photosynthetic Organisms: Novel and Established Thiol-Based Molecular Mechanisms
Zaffagnini, M., Fermani, S., Marchand, C. H., Costa, A., Sparla, F., Rouhier, N., Geigenberger, P., Lemaire, S. D., & Trost, P. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2018.7617 · Cited by 130 · see citing works
Arousal-induced cortical activity triggers lactate release from astrocytes
Zuend, M., Saab, A. S., Wyss, M. T., Ferrari, K. D., Hösli, L., Looser, Z. J., Stobart, J. L., Durán, J., Guinovart, J. J., Barros, L. F., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0170-4 · Cited by 129 · see citing works
Transcriptional Regulation of Central Carbon and Energy Metabolism in Bacteria by Redox-Responsive Repressor Rex
Ravcheev, D. A., Li, X., Latif, H., Zengler, K., Leyn, S. A., Korostelev, Y., Kazakov, A. E., Novichkov, P. S., Osterman, A. L., & Rodionov, D. A. (2011) · Journal of Bacteriology · doi:10.1128/jb.06412-11 · Cited by 128 · see citing works
Physical bioenergetics: Energy fluxes, budgets, and constraints in cells
Yang, X., Heinemann, M., Howard, J., Huber, G., Iyer‐Biswas, S., Treut, G. L., Lynch, M., Montooth, K. L., Needleman, D. J., Simone Pigolotti, A., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2026786118 · Cited by 128 · see citing works
Precision Redox: The Key for Antioxidant Pharmacology
Meng, J., Lv, Z., Zhang, Y., Wang, Y., Qiao, X., Sun, C., Chen, Y., Guo, M., Han, W., Ye, A., et al. (2021) · Antioxidants & Redox Signaling · doi:10.1089/ars.2020.8212 · Cited by 122 · see citing works
Genetically encoded fluorescent indicator for imaging NAD+/NADH ratio changes in different cellular compartments
Bilan, D. S., Matlashov, M. E., Gorokhovatsky, A. Y., Schultz, C., Enikolopov, G., & Belousov, V. V. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.11.018 · Cited by 121 · see citing works
Deciphering the molecular mechanism responsible for GCaMP6m's Ca2+-dependent change in fluorescence
Barnett, L. M., Hughes, T. E., & Drobizhev, M. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170934 · Cited by 119 · see citing works
Multiparametric real‐time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport
Wagner, S., Steinbeck, J., Fuchs, P., Lichtenauer, S., Elsässer, M., Schippers, J. H. M., Nietzel, T., Ruberti, C., Aken, O. V., Meyer, A. J., et al. (2019) · New Phytologist · doi:10.1111/nph.16093 · Cited by 119 · see citing works
HyPer Family Probes: State of the Art
Bilan, D. S., & Belousov, V. V. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6586 · Cited by 118 · see citing works
Mitochondria as the Target of Hepatotoxicity and Drug-Induced Liver Injury: Molecular Mechanisms and Detection Methods
Mihajlovic, M., & Vinken, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063315 · Cited by 128 · see citing works
Non-invasive In-cell Determination of Free Cytosolic [NAD+]/[NADH] Ratios Using Hyperpolarized Glucose Show Large Variations in Metabolic Phenotypes
Christensen, C. E., Karlsson, M. G., Winther, J. R., Jensen, P. R., & Lerche, M. H. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.498626 · Cited by 117 · see citing works
ROS in AgingCaenorhabditis elegans: Damage or Signaling?
Back, P., Braeckman, B. P., & Matthijssens, F. (2012) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2012/608478 · Cited by 118 · see citing works
Multiparameter imaging of calcium and abscisic acid and high‐resolution quantitative calcium measurements using R‐GECO1‐mTurquoise in Arabidopsis
Waadt, R., Krebs, M., Kudla, J., & Schumacher, K. (2017) · New Phytologist · doi:10.1111/nph.14706 · Cited by 116 · see citing works
Illuminating NAD+ Metabolism in Live Cells and In Vivo Using a Genetically Encoded Fluorescent Sensor
Zou, Y., Wang, A., Huang, L. Z., Zhu, X., Hu, Q., Zhang, Y., Chen, X., Li, F., Wang, Q., Wang, H., et al. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.02.017 · Cited by 116 · see citing works
Investigating the Sensitivity of NAD+-dependent Sirtuin Deacylation Activities to NADH
Madsen, A. S., Andersen, C. D., Daoud, M., Anderson, K. A., Laursen, J. S., Chakladar, S., Huynh, F. K., Colaço, A. R., Backos, D. S., Fristrup, P., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.668699 · Cited by 110 · see citing works
In Vivo Fluorescent Adenosine 5′-Triphosphate (ATP) Imaging of Drosophila melanogaster and Caenorhabditis elegans by Using a Genetically Encoded Fluorescent ATP Biosensor Optimized for Low Temperatures
Tsuyama, T., Kishikawa, J.-I., Han, Y.-W., Harada, Y., Tsubouchi, A., Noji, H., Kakizuka, A., Yokoyama, K., Uemura, T., & Imamura, H. (2013) · Analytical Chemistry · doi:10.1021/ac4015325 · Cited by 110 · see citing works
Neurons rely on glucose rather than astrocytic lactate during stimulation
Díaz‐García, C. M., & Yellen, G. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24374 · Cited by 107 · see citing works
A high-throughput multiparameter screen for accelerated development and optimization of soluble genetically encoded fluorescent biosensors
Koveal, D., Rosen, P. C., Meyer, D. J., Díaz‐García, C. M., Wang, Y., Cai, L., Chou, P. J., Weitz, D. A., & Yellen, G. (2022) · Nature Communications · doi:10.1038/s41467-022-30685-x · Cited by 105 · see citing works
Novel uses of fluorescent proteins
Mishin, A. S., Belousov, V. V., Solntsev, K. M., & Lukyanov, K. A. (2015) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2015.05.002 · Cited by 107 · see citing works
Boronic Acid: A Bio-Inspired Strategy To Increase the Sensitivity and Selectivity of Fluorescent NADH Probe
Wang, L., Zhang, J., Kim, B., Peng, J., Berry, S. N., Ni, Y. Z., Su, D., Lee, J. Y., Yuan, L., & Chang, Y. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.6b05810 · Cited by 104 · see citing works
Metabolic Regulation of Cell Fate and Function
Ghosh-Choudhary, S. K., Liu, J., & Finkel, T. (2020) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.12.005 · Cited by 106 · see citing works
Mitochondrial calcium uniporter regulator 1 (MCUR1) regulates the calcium threshold for the mitochondrial permeability transition
Chaudhuri, D., Artiga, D. J., Abiria, S. A., & Clapham, D. E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602264113 · Cited by 102 · see citing works
Quantitative in vivo imaging of neuronal glucose concentrations with a genetically encoded fluorescence lifetime sensor
Díaz‐García, C. M., Lahmann, C., Martínez‐François, J. R., Li, B., Koveal, D., Nathwani, N., Rahman, M., Keller, J. P., Marvin, J. S., Looger, L. L., et al. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24433 · Cited by 97 · see citing works
Label-Free Optical Metabolic Imaging in Cells and Tissues
Georgakoudi, I., & Quinn, K. P. (2023) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071516-044730 · Cited by 102 · see citing works
Exploiting ROS and metabolic differences to kill cisplatin resistant lung cancer
Wangpaichitr, M., Wu, C., Li, Y. Y., Nguyen, D. J. M., Kandemir, H., Shah, S. S., Chen, S., Feun, L. G., Prince, J. S., Kuo, M. T., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.17568 · Cited by 101 · see citing works
Nicotine rebalances NAD+ homeostasis and improves aging-related symptoms in male mice by enhancing NAMPT activity
Yang, L., Shen, J., Liu, C., Kuang, Z., Tang, Y., Qian, Z., Guan, M., Yang, Y., Zhan, Y., Li, N., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36543-8 · Cited by 102 · see citing works
Cytosolic NADH-NAD + Redox Visualized in Brain Slices by Two-Photon Fluorescence Lifetime Biosensor Imaging
Mongeon, R., Venkatachalam, V., & Yellen, G. (2016) · Antioxidants & Redox Signaling · doi:10.1089/ars.2015.6593 · Cited by 100 · see citing works
Self-citation
Analysis of redox landscapes and dynamics in living cells and in vivo using genetically encoded fluorescent sensors
Zou, Y., Wang, A., Shi, M., Chen, X., Liu, R., Li, T., Zhang, C., Zhang, Z., Zhu, L., Ju, Z., et al. (2018) · Nature Protocols · doi:10.1038/s41596-018-0042-5 · Cited by 100 · see citing works
Inhibition of mitochondrial function by metformin increases glucose uptake, glycolysis and GDF-15 release from intestinal cells
Yang, M. H., Darwish, T., Larraufie, P., Rimmington, D., Cimino, I., Goldspink, D. A., Jenkins, B., Koulman, A., Brighton, C. A., Ma, M. K. L., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-81349-7 · Cited by 101 · see citing works
The distinct roles of calcium in rapid control of neuronal glycolysis and the tricarboxylic acid cycle
Díaz‐García, C. M., Meyer, D. J., Nathwani, N., Rahman, M., Martínez‐François, J. R., & Yellen, G. (2021) · eLife · doi:10.7554/elife.64821 · Cited by 95 · see citing works
Simultaneous mapping of membrane voltage and calcium in zebrafish heart in vivo reveals chamber-specific developmental transitions in ionic currents
Hou, J. H., Kralj, J. M., Douglass, A. D., Engert, F., & Cohen, A. E. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00344 · Cited by 94 · see citing works
Matrix Redox Physiology Governs the Regulation of Plant Mitochondrial Metabolism through Posttranslational Protein Modifications
Møller, I. M., Igamberdiev, A. U., Bykova, N. V., Finkemeier, I., Rasmusson, A. G., & Schwarzländer, M. (2020) · The Plant Cell · doi:10.1105/tpc.19.00535 · Cited by 89 · see citing works

Live-Cell Imaging of Cytosolic NADH–NAD+ Redox State Using a Genetically Encoded Fluorescent Biosensor
Hung, Y. P., & Yellen, G. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-622-1_7 · Cited by 66 · see citing works
Single Cell Imaging of Metabolism with Fluorescent Biosensors
Hung, Y. P. (2012) · Digital Access to Scholarship at Harvard (DASH) (Harvard University)
Cytosolic NADH-NAD + Redox Visualized in Brain Slices by Two-Photon Fluorescence Lifetime Biosensor Imaging
Mongeon, R., Venkatachalam, V., & Yellen, G. (2016) · Antioxidants & Redox Signaling · doi:10.1089/ars.2015.6593 · Cited by 100 · see citing works
Assessment of the Peroxisomal Redox State in Living Cells Using NADPH- and NAD+/NADH-Specific Fluorescent Protein Sensors
Costa, C. F., Li, H., Hussein, M. A. F., Yang, Y. A., Lismont, C., & Fransen, M. (2023) · Methods in molecular biology · doi:10.1007/978-1-0716-3048-8_13 · Cited by 4 · see citing works
Genetically encoded biosensors for evaluating NAD+/NADH ratio in cytosolic and mitochondrial compartments
Hu, Q., Wu, D., Walker, M. A., Wang, P., Tian, R., & Wang, W. (2021) · Cell Reports Methods · doi:10.1016/j.crmeth.2021.100116 · Cited by 69 · see citing works

Authors: Hung, Y. P., Albeck, J. G., Tantama, M., & Yellen, G.
Affiliations: Harvard University (US)
Corresponding author: Yellen, Gary
ORCID: Hung, Yin Pun
Albeck, John G.
Tantama, Mathew
Yellen, Gary
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2011-10
Volume: 14
Issue: 4
Pages: 545-554
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2011.08.012
PMC: PMC3190165
OpenAlex: W2155184340
Cited by: 509
References: 58
Citations by year: 2026: 31 · 2025: 29 · 2024: 32 · 2023: 34 · 2022: 34 · 2021: 43 · 2020: 59 · 2019: 29 · 2018: 46 · 2017: 39 · 2016: 30 · 2015: 29 · 2014: 34 · 2013: 26 · 2012: 12
FWCI: 13.40
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 655 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: U.S. Army (W81XWH-08-1-0609)
National Institutes of Health (R01 NS055031, F32 NS066613)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › bioluminescence and chemiluminescence research
Keywords: genetically encoded fluorescent sensors, circularly permuted GFP, glycolysis, lactate dehydrogenase, astrocytes, neurons, bioenergetics, live-cell imaging
MeSH terms: Phosphoinositide-3 Kinase Inhibitors, Animals, Bacterial Proteins, Cells, Cultured, Cytosol, Glycolysis, Hydrogen-Ion Concentration, L-Lactate Dehydrogenase, Luminescent Proteins, NAD, Oxidation-Reduction, Recombinant Fusion Proteins, Biosensing Techniques, Phosphatidylinositol 3-Kinases, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks