regulation and bioenergetics of glycolysis

When NADH and AMPK index were tracked in individual cells, we found a high degree of variance over time within each cell, with some cells showing pronounced peaks and troughs (Figure 2—figure supplement 2). Color scale bar on upper left indicates approximate AMPK index, with white representing low activity and orange/brown representing high activity. Glycolysis & the Oxidation of Pyruvate - Bioenergetics & the Metabolism of Carbohydrates & Lipids - Clear, concise, and in full color, this book is unrivaled in its ability to clarify the link between biochemistry and the molecular basis of disease. Consistent with previous data (Hung et al., 2011), steady-state NADH index increased with glucose concentrations (Figure 1—figure supplement 2C), and Peredox could detect glycolytic dynamics in individual live cells (Figure 1H). Regulation of glycogen synthesis and breakdown. Previous studies of glycolytic oscillations have measured periods ranging from several seconds to 20 min (Chou et al., 1992; O'Rourke et al., 1994; Tornheim and Lowenstein, 1973; Yang et al., 2008). (F, G) Simultaneous measurements of NADH and Akt indices (F) or AMPK and Akt indices (G) within the same cell. (D) Fluctuation scores for each of the conditions shown in (A-C), calculated as described in the Materials and methods section. Regulation of glycolysis and gluconeogenesis. Oligomycin and IA-treated cells showed significantly increased pulse scores relative to untreated cells (Figure 3D). We generated dual-reporter cell lines expressing both AKT-KTR and AMPKAR2, or AKT-KTR and Peredox, allowing Akt activity and metabolic status to be measured in the same cell. iGM contained all supplements used in MCF10A culture medium (above), but with horse serum replaced by 0.1% (w/v) bovine serum albumin. Gluconeogenesis can be regulated by fructose 1,6-bisphosphatase. (D, E) Single-cell measurements of NADH index (D) and Akt index (E) for the indicated concentrations of IA. The color of the dark meat comes from the iron present in the cytochromes involved in oxygen‐consuming respiration. Oscillations often arise in feedback systems in which there is a delay between induction of feedback and recovery of the feedback-controlled variables (Glass et al., 1988). oscillatory) responses result (Chandra et al., 2011). In terms of nonlinear dynamics, such responses occur in limited regions of parameter space near unstable fixed points. (C) Glucose uptake from culture medium by MCF10A cells. Finally, the kinetics of feedback responses were common to the point of inhibition, as other inhibitors of the electron transport chain including metformin and antimycin A induced pulses with durations similar to those of oligomycin (Figure 3—figure supplement 3B). glycolysis may offer a promising strategy to preferentially kill cancer cells. The balance of glycogen synthesis (storing glucose) and breakdown (releasing glucose) is regulated by activation and inhibition of kinase (phosphorylates) and phosphatase (dephosphorylates) enzyme activity. Thank you for submitting your article "Akt regulation of glycolysis mediates bioenergetic stability in epithelial cells" for consideration by eLife. For example, insulin enhances the occurrence of IA-induced oscillations (Figure 4I), but has a suppressive role for oligomycin-induced oscillations (Figure 5C). Annotation was performed as for Video 1. With a Hamamatsu Photonics (Hamamatsu, Japan) ORCA-ER or ORCA-AG cooled CCD camera or an Andor Zyla 5.5 scMOS camera, images were acquired every 3–8 min with 2 × 2 binning and an exposure time of 200–225 ms for T-Sapphire, 70–225 ms for YFP, 70–225 ms for RFP. In this study, we established a panel of proliferative epithelial cells expressing multiple fluorescent biosensors to enable detailed tracking of single-cell metabolic responses. This video cannot be played in place because your browser does support HTML5 video. 2007). The committed step is the one after which the substrate has only one way to go. Accordingly, treatment of insulin-cultured cells with an Akt or PI3K inhibitor decreased glucose uptake and NADH index (Figure 2—figure supplement 1B–C) while increasing AMPK index (Figure 2E). As with the initial pulse, each burst of AMPK activity lasted 2–4 hr, suggesting that continuing oligomycin treatment induced ongoing bioenergetic challenges, which were, nevertheless, overcome by cells maintained at 17 mM glucose. A phosphate group is added to glucose, and fructose-6-phosphate. The tools developed here will be of use in detecting and analyzing similar oscillations in other cell types and conditions. Secondary staining was performed with Alexa647-conjugated anti-rabbit (Life Technologies), followed by DNA staining with Hoechst-33342. When possible, data from independent replicates were merged into a single data set using a set of calibration conditions for normalization of reporter signals; these data are indicated as ‘combined’ in the figure legends. Should be able to break down all relevant reactions into their half-reactions; Helps determine the number of electrons that are being transferred Time-lapse wide-field microscopy was performed as previously described (Hung et al., 2011; Albeck et al., 2013). All three probes reported predictable responses to major metabolic stressors, and some perturbations were accompanied by oscillatory responses in the metabolic/signaling state, many of which persisted for hours. (E) Quantification of pulse score for each condition shown in (D). […] A consultation including the Reviewer, Reviewing Editor and Senior Editor concluded that the paper could be considered again after one additional round of revision that more thoroughly addresses the question of the influence of sensor expression on metabolism. All supplemental movies were created using Nikon Elements software; ratiometric images of mTurquoise2 signal divided by YPet signal were constructed following background subtraction, and intensity modulation display was used to suppress spurious background values. Regulation of the pyruvate dehydrogenase complex (PDC) Regulation of Key Enzymes in the Citric Acid Cycle; Entry of pyruvate into the the citric acid cycle leading to aerobic production of energy and intermediates for biosynthesis is a key metabolic step. View Notes - Bioenergetics and Glycolysis-1 from STEP 1 at Montgomery College. The net products of glycolysis are 2ATP and a reduced NAD (N icotinamide A denine D inucleotide) or NADH. Cells were then washed, blocked with Odyssey Blocking Buffer (Li-Cor, Lincoln, NE), and incubated with anti-pACC (Cell Signaling , Danvers, MA #11818) diluted 1:125 in blocking buffer, overnight at 4°C. (D) Mean and 25th-75th percentile AMPK index for cells treated as in (A), recorded between 16 and 21 hr following treatment. GFs were added at time 0. Although Rad51 is the key protein that drives HR, multiple auxiliary factors interact with Rad51 to potentiate its activity. High concentrations of citrate indicate a plentiful supply of intermediates for energy production; therefore, high activity of the glycolytic pathway is not required. In contrast, mitochondrial oxidation of glucose in slow‐red muscle makes more ATP but the process takes longer. The revision does compare metabolism between parental MCF10A cells and cell lines expressing the various sensors, but the reviewers found this experiment insufficient for two reasons. Presumably you would be able to extract these data from previous live-cell imaging experiments, therefore allowing you to revise the paper quickly. Oligomycin-induced fluctuations in AMPK differed from IA-induced oscillations in their longer time scale (2–6 hr), in their irregular nature, and in that they were not tightly associated with coordinated changes in NADH and Akt indices (Figure 5—figure supplement 1A–B). Glutamine was required for the suppression of oscillations by insulin (Figure 5—figure supplement 1D), but regardless of the presence of insulin, cells cultured in the presence of glutamine without glucose failed to recover their AMPK index and died within 12 hr (Figure 5—figure supplement 1E), suggesting that glutamine may play a role in supporting glucose metabolism, but cannot alone provide sufficient ATP in the absence of oxidative phosphorylation. However, we would be happy to include this panel if the reviewers feel that it would add significantly to the paper. Withdrawal of insulin and EGF from the growth medium, which both reduces Akt and mTOR activity and glucose uptake (Figure 2A and C and Worster et al., 2012), also resulted in attenuation of IA-induced oscillations (Figure 4—figure supplement 3A), while inhibition of fatty acid oxidation, which could link pulses of AMPK activity to NADH production, reduced the persistence of AMPK index oscillations, but did not eliminate them (Figure 4—figure supplement 3B). N = 3, representative. To elucidate the mechanisms by which curcumin affects systemic amyloidosis, we investigated amyloid deposition and molecular changes in a mouse model of amyloid apolipoprotein A-II (AApoAII) amyloidosis, in which mice were fed a curcumin-supplemented diet. Similarly, in the presence of insulin, moderate inhibition of glycolysis with a dose of IA too low to independently stimulate oscillations resulted in amplification of oligomycin-induced AMPK pulses (Figure 5—figure supplement 1C). Fatty acids also allosterically inhibit pyruvate kinase, serving as an indicator that alternative energy sources are available for the cell. Cells cultured in combinations of glucose, pyruvate, or glutamine displayed varying elevated levels of steady-state AMPK index (Figure 1—figure supplement 2A–B), demonstrating that AMPKAR2 could monitor AMPK status across a range of physiological concentrations of nutrients in individual live cells. The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission. Because EGF stimulated proliferation more strongly than insulin (Figure 2—figure supplement 1A), these metabolic parameters correlated poorly with proliferative rate. (H) Diagram of approximate phase relationship between NADH, AMPK, and Akt indices derived from the data collected in (F) and (G). Additionally, in response to ATP depletion, the energy-sensing kinase AMP-activated protein kinase (AMPK) stimulates glucose uptake and suppresses energy-consuming processes (Hardie, 2008). For labeling experiments, cells were incubated with 0 µM, 10 µM, or 50 µM IA for 6 hr after which the culture medium was replaced with medium containing [U-13C6]glucose for 10 min prior to metabolite extraction. High sugar levels stimulate the pancreas to produce insulin, which enhances the entry of glucose into the cell and increases the production of the critical glycolysis enzymes. Regulation of Glycolysis and Gluconeogenesis - Duration: 8:02. Regulation of glycolysis Three regulatory enzymes: Hexokinase & glucokinase Phosphofructokinase Pyruvate kinase Catalysing the irreversible reactions regulate glycolysis. The negative control with abrogated NADH binding was constructed by introducing the mutations Y98D in both subunits of Rex and I189F in the first subunit of Rex in pMSCV-Peredox-mCherry-NLS. Fluorescence filters were from Chroma (Bellows Falls, VT): T-Sapphire (89000 ET Sedat Quad; or ET405/20x, T425LPXR, and ET525/50 m), YFP (89002 ET ECFP/EYFP; or 41028), and RFP (49008 ET mCherry; or 41043 HcRed). Cross-correlation analysis indicated that such inverse events were highly overrepresented in the population relative to their expected occurrences at random (Figure 6E), suggesting that AMPK fluctuations may result at least in part from rises and falls in Akt activity and the associated rate of glucose uptake. Armando Hasudungan 197,723 … To maintain compatibility with red-wavelength reporters for dual imaging and to simplify cell tracking, we generated a nuclear-targeted Peredox fused to the YFP mCitrine (Figure 1E). Analysis of fluctuations in both reporters on a cell-by-cell basis revealed a high frequency of inverse events, with a pulse in AMPK index mirrored by a decrease in Akt index (Figure 6D). For example, dihydroxyacetone phosphate is the precursor to the glycerol component of lipids. Removing #book# It is also worth noting an alternative explanation for this correlation, which is that the cell-specific factors leading to higher reporter expression in certain cells may also modify their metabolic behavior. MCF10A-Peredox cells were imaged in iGM2 as in Figure 4D and were treated at time 0 with 10 µM IA. MCF10A-Peredox cells treated with lactate, or pyruvate in combination with iodoacetate (IA) as a glycolytic blockade, exhibited rapid (<3 min) changes to reach maximal and minimal sensor responses, respectively (Figure 1F and G), indicative of cytosolic NADH-NAD+ redox sensing. Terms in this set (79) Glycolysis products. In the context of tumor microenvironments with fluctuating nutrient and oxygen supply, such instability is likely deleterious and may create selective pressure for genetic alterations to enhance glycolysis, such as activating mutations in the PI3K/Akt pathway, which are among the most frequent mutations across all cancer types. The muscle acts quickly, but for only a short time. We then used this framework to examine how metabolic adaptation functions in proliferating cells. Quantification of pulse score for each condition is shown in (B). Metabolite extracts were derivatized by a two-step process. Despite its relative inefficiency in ATP yield per molecule of glucose, glycolysis can, at least under certain conditions, produce ATP at a faster rate than oxidative phosphorylation if sufficient glucose is available; this ability is best documented in muscle cells during anaerobic activity but could conceivably extend to other situations such as hypoxic cells within a tumor (Liberti and Locasale, 2016). 2) We have taken a new experimental approach, presented in Figure 3—figure supplement 2, in which we directly compare reporter-expressing and non-reporter-expressing (parental) MCF10A cells under the same conditions, performing an immunofluorescence time course to detect phosphorylation of the physiological AMPK target ACC. Glycolysis is the process of breaking down glucose into pyruvate, producing two molecules of ATP (per 1 molecule of glucose) in the process. Prior to imaging, cells were placed in iGM lacking pyruvate, with 2.5 mM glutamine, 3.4 mM glucose, and 20 ng/ml EGF or 10 μg/ml insulin. cpbuck356. Because the Peredox signal showed a higher degree of frame-to-frame variance that is not likely to be biologically relevant, the ‘smooth’ parameter was set to six for this analysis to prevent identification of spurious pulses. (B) Distribution of the average period of AMPK pulses for cells with five or more pulses, calculated as average peak-to-peak spacing following IA treatment as shown in Figure 3A. Immunofluorescence detection of phosphorylated ACC (pACC), an AMPK substrate, showed indistinguishable staining patterns in parental and reporter-expressing cells (Figure 3—figure supplement 2). Extracellular acidification rates were measured under the basal condition, followed by sequential addition of 5 mM glucose, 1 μM oligomycin, and 50 mM 2-deoxyglucose (2-DG)(Nicholls et al., 2010). https://doi.org/10.1016/j.tibs.2015.12.001, Multiplexed fluorescence imaging of ERK and Akt activities and cell-cycle progression, Akt-dependent activation of the heart 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFKFB2) isoenzyme by amino acids, Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells, Akt-dependent transformation: there is more to growth than just surviving, Encoding and decoding cellular information through signaling dynamics, https://doi.org/10.1016/j.cell.2013.02.005, Mitogenic activity of neu differentiation factor/heregulin mimics that of epidermal growth factor and insulin-like growth factor-I in human mammary epithelial cells, Hexokinase-II positively regulates glucose starvation-induced autophagy through TORC1 inhibition, https://doi.org/10.1016/j.molcel.2013.12.019, Akt phosphorylates HK-II at Thr-473 and increases mitochondrial HK-II association to protect cardiomyocytes, Visualizing spatiotemporal dynamics of multicellular cell-cycle progression, https://doi.org/10.1016/j.cell.2007.12.033, Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation, Differential effects of iodoacetamide and iodoacetate on glycolysis and glutathione metabolism of cultured astrocytes, https://doi.org/10.3389/neuro.14.001.2009, Receptor level mechanisms are required for epidermal growth factor (EGF)-stimulated extracellular signal-regulated kinase (ERK) activity pulses, Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells, https://doi.org/10.1016/j.cell.2015.07.017, Optogenetic reporters: Fluorescent protein-based genetically encoded indicators of signaling and metabolism in the brain, https://doi.org/10.1016/B978-0-444-59426-6.00012-4, Imaging energy status in live cells with a fluorescent biosensor of the intracellular ATP-to-ADP ratio, DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein, Building and breeding molecules to spy on cells and tumors, https://doi.org/10.1016/j.febslet.2004.11.025, A fluorescent reporter of AMPK activity and cellular energy stress, https://doi.org/10.1016/j.cmet.2011.03.006, Understanding the Warburg effect: the metabolic requirements of cell proliferation, Aerobic glycolysis during lymphocyte proliferation, Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking, Akt and ERK control the proliferative response of mammary epithelial cells to the growth factors IGF-1 and EGF through the cell cycle inhibitor p57Kip2, https://doi.org/10.1126/scisignal.2001986, Glycolytic oscillations in isolated rabbit ventricular myocytes, Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling, A hyperactive piggyBac transposase for mammalian applications, SoNar, a highly responsive NAD+/NADH sensor, allows high-throughput metabolic screening of anti-tumor agents, https://doi.org/10.1016/j.cmet.2015.04.009, Curcumin promotes AApoAII amyloidosis and peroxisome proliferation in mice by activating the PPARα signaling pathway, Mutations in SKI in Shprintzen–Goldberg syndrome lead to attenuated TGF-β responses through SKI stabilization, A novel motif of Rad51 serves as an interaction hub for recombination auxiliary factors, Department of Pathology, Brigham and Women’s Hospital, Boston, United States, Ralph DeBerardinis, UT Southwestern Medical Center, United States. 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( See Figure 4—figure supplement 1A ) to remove spurious noise imaged in iGM as in Figure,! You may still download the video for offline viewing of transparency, eLife the! Most tissues-Low Km ( reaches maximum velocity at low [ glucose ] ) by...

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