warburg effect article

The fibroblasts then undergo cellular catabolism, which results in a loss of mitochondrial function and ultimately a switch from aerobic metabolism to glycolysis [49]. Although PET imaging is undeniably an extremely useful and an important clinical technique, there can be issues with the interpretation of the image. glucose phosphorylation into glucose-6P. First postulated by Pavlides et al. 18F-FDG is transported into cells by glucose transporters (GLUTs) and phosphorylated by hexokinase (HK) to 18F-FDG-6-phosphate (18F-FDG-6-P). The goal of this paper is to suggest strongly that most of (if not all) the hallmarks of cancer could be the consequence of the Warburg‘s effect. Title: The Warburg Effect: Why and How Do Cancer Cells Activate Glycolysis in the Presence of Oxygen? Rare Adrenal Cancer Network-Corticomédullosurrénale Tumeur Endocrine, Institut National du Cancer, Paris, France, Affiliations No, Is the Subject Area "Microarrays" applicable to this article? Université René Diderot, Faculté de Médecine, Paris, France, Affiliation Calibration bar: 100 µm. In the last decade, research has shown that different tumour types (and indeed subpopulations within a tumour) have different bioenergetic alterations. AP-HP, Hôpital Cochin, Département d'Endocrinologie, Paris, France, Affiliations Back in the lab at the Kaiser Wilhelm Institute, Warburg discovered that thin slices of tumors produced lactate much more rapidly than normal tissue. The Warburg effect has been confirmed in previous studies including those of DeBerardinis et al. Advances in technology have helped in furthering our knowledge of the underlying molecular processes underpinning cancer, but there are still many unanswered questions. Find Other Styles. Our results suggest that activation of the HIF pathway associated with the loss of p53 activity might mediate the molecular and biochemical features of the Warburg effect; this effect was clearly observed in VHL PH/PGL, but not in RET and NF1 and only partially in SDH tumors. "Proteomics Analysis Reveals that Warburg Effect along with Modification in Lipid Metabolism Improves In Vitro Embryo Development under Low Oxygen" Int. As in the studies of the Warburg effect and the impact of hypoxia described earlier, studies to date on the reverse Warburg effect use high concentrations of glucose 25 mM. Université Paris Descartes, Faculté de Médecine, Paris, France, Recent studies arguing that cancer cells benefit from this phenomenon, termed the Warburg effect, have renewed discussions about its exact role as cause, correlate, or facilitator of cancer. Abstract:It is a longstanding debate whether cancer is one disease or a set of very diverse diseases. Contributed reagents/materials/analysis tools: JB CB FT LA RL PFP APGR. The Warburg effect, also known as aerobic glycolysis, is defined as the propensity of cancer cells to take up high levels of glucose and to secrete lactate in the presence of oxygen. Unlike its activity on HIF proteins, VHL binding to p53 suppresses Mdm2-mediated ubiquitination and nuclear export and thereby leads to p53 stabilization. Note that from the first issue of 2016, MDPI journals use article numbers instead of page numbers. The exact reasons behind the metabolic switch are not known, but likely reasons include: (i) sustaining high proliferative rates in hypoxia [27] and (ii) evading apoptosis as a result of reduced mitochondrial function [28]. This work is part of the national program Cartes d'Identité des Tumeurs ® (CIT) funded and developed by the Ligue Nationale Contre le Cancer.P.B. The positive group comprised two NF1, one RET, six SDH and one VHL tumors. Activation of HIFs is a major aspect of cancer biology [22] and has been associated with the Warburg effect. Advances in research techniques since then have shown the mitochondria in cancer cells to be functional across a range of tumour types. Activation of the HIF pathway in SDH and VHL PH/PGL may be responsible for the stimulation of glycolysis and anaerobic fermentation. Data are means±SEM. Such a bioenergetic mechanism for the regulation of signaling may explain the Warburg effect.” It comes down to a previously unappreciated link between Warburg … 5 This phenomenon was first discovered by Otto Warburg in the 1920s and was called aerobic glycolysis. Identification of mutations in SDH genes led to the first and unexpected demonstration of a tumor suppressor role for a metabolic enzyme (for review see [11], [12]), implicating mitochondrial deficiencies in tumorigenesis, as first suggested by Otto Warburg 80 years earlier. 7, Table 1). These observations were however unexpected, notably because positron emission tomography with 2-[(18)F]-fluoro-2-deoxy-D-glucose ([(18)F]-FDG PET) tracing glucose uptake was recently shown to be particularly sensitive for the evaluation of bone metastases in patients harboring SDHB mutations [28]. (A) Unsupervised hierarchical clustering analysis of the 68 samples according to the expression of 38 genes. Not surprisingly, the Warburg effect has become a topic of great interest in the study of TB. Cancer metabolism is characterized by increased macromolecular syntheses through coordinated increases in energy and substrate metabolism. p53 is a transcription factor that regulates the expression of TIGAR (TP53-induced glycolysis and apoptosis regulator), a protein displaying fructose-2,6-bisphosphatase activity, thereby lowering fructose-2,6-bisphosphate concentrations in cells, resulting in inhibition of glycolysis [21]. Heat-mediated antigen retrieval was performed for p53, Glut1, SDHB and TIGAR (10 mM citrate buffer, pH 6, 15 min), and for HIF-1α and HIF-2α (Tris 100 mM, EDTA 1 mM, 0,05% Tween, pH 9, 45 min). Together, these phenomena concur to the observed decreased electron transport and increased glycolysis. (A) Glutamate is released from activated synapses and taken up by astrocytes triggering an increase in glycolysis and lactate production. 6B). By using Warburg manometer, Warburg and his colleagues found that cancer cells did not consume more oxygen than normal tissue cells, even under normal oxygen circumstances [3], and it seemed that cancer cells preferred to aerobic glycolysis than to oxidative phosphorylation. OXPHOS and glycolysis have been evaluated in numerous tumor types, including renal clear cell carcinoma (RCC) in which the majority of glycolytic enzymes are overexpressed and mitochondrial enzymes underexpressed relative to patient-matched normal kidney cortex [6]. Aerobic glycolysis (the Warburg effect) facilitates tumor growth, and drugs targeting aerobic glycolysis are being developed. In summary, we have sought here to revisit the Warburg effect and review its significance in cancer based on recent advances in our knowledge and understanding of the complex biology underlying this disease. A review of cancer metabolism. Yes Using transcriptome analysis, we confirmed these findings and showed that unsupervised analysis of gene expression in the OXPHOS pathway is highly efficient to classify patients depending on cancer-predisposing gene. From his observations, Warburg concluded that the mitochondria were dysfunctional [8,9]. Lactate was discovered in the late 1700s and was traditionally thought of as a waste product of glycolysis. SDHA protein was assayed independently in all PH/PGL. Lactate is also capable of stabilising hypoxia-inducing factor and increasing vascular endothelial growth factor expression [53]. Mutant p53, because of its longer half-life can result in positive nuclear immunostaining. Positron emission tomography (PET) imaging uses a radioisotope-labelled glucose tracer, 18F-fluorodeoxyglucose (18F-FDG), to identify areas of high glucose uptake/metabolism in the body. the abnormal stabilization of HIFs under normoxic conditions. The Warburg effect is not consistent across all tumours, and the phenomenon of aerobic glycolysis has now been challenged by several groups with many cell lines reported as having mitochondrial function [16–18]. More recent studies showed that lactate … Data are means±SEM. This observation is in accordance with most reported studies that showed very little p53 mutations in benign PH/PGL [36]–[38]. Calibration bar: 50 µm. This review will discuss the metabolic reprogramming of cancer, possible explanations for the high glucose consumption in cancer cells observed by Warburg, and suggest key experimental practices we should consider when studying the metabolism of cancer. 6: 1996. [50], the authors demonstrate support for the reverse Warburg effect by culturing human breast cancer cell lines with human fibroblasts. Discover a faster, simpler path to publishing in a high-quality journal. One of the first described functions of the HIF pathway is activation of glycolysis; HIF-1α up-regulates the expression of most glycolytic enzymes and the glucose transporters GLUT1 and 3. SDHB, C and D genes encode three of the four subunits of succinate dehydrogenase (SDH), a mitochondrial enzyme, which catalyzes the oxidation of succinate into fumarate in the tricarboxylic acid (TCA) cycle, and feeds electrons to the ubiquinone pool in the respiratory chain. The Warburg Effect in TB: Lesions and Lungs. We did not detect the expression of either HIF-1α or HIF-2α in RET and NF1 tumors, although both these proteins were present in adjacent adrenal tissues (data not shown). First, we performed HIF-1α and HIF-2α immunohistochemistry to evaluate pseudohypoxia in inherited PH/PGL tissues (Fig. AP-HP, Hôpital Européen Georges Pompidou, Service d'Anatomo-pathologie, Paris, France, Affiliations The average overexpression was between 2- to 4-fold, but reached 15- to 17-fold for HXK-II and the lactate transporter MTC-4, respectively. For one patient (P6), vascular density could not be evaluated because of an anarchic vascular architecture. Research Article Inflammation Therapeutics Open Access | 10.1172/jci.insight.138949. Cancer cells have been shown to have altered metabolism when compared to normal non-malignant cells. Microarray analyses were performed with R system software (http://www.R-project.org, V2.3.0) including packages of Bioconductor [41]. 21, no. Aerobic glycolysis is an inefficient way t … However, different tumour populations have different bioenergetic alterations in order to meet their high energy requirement; the Warburg effect is not consistent across all cancer types. To evaluate the link between hypoxia and Warburg effect, we studied mitochondrial electron transport, angiogenesis and glycolysis in pheochromocytomas induced by germ-line mutations in VHL, RET, NF1 and SDH genes. It therefore seemed plausible that p53-dependant loss of TIGAR in VHL-mutated samples may explain the activation of glycolysis specifically observed in these tissues. To evaluate the link between hypoxia and Warburg effect, we studied mitochondrial electron transport, angiogenesis and glycolysis in pheochromocytomas induced by germ-line mutations in VHL, RET, NF1 and SDH genes. They provide a pertinent explanation for the specific activation of glycolysis in VHL-related PH/PGL. It is indisputable that certain features of cancer are indeed hallmarks that are essential for most types of cancer. Glycolysis Medicine & Life Sciences The excessive glucose often found in cell culture media can decrease mitochondrial respiration, allowing aerobic glycolysis to predominate. After more than 80 years from the revolutionary discoveries of Otto Warburg, who observed high glucose dependency, with increased glycolysis and lactate production regardless of oxygen availability in most cancer cells, the ‘Warburg effect’ returns to the fore in neuronal cells affected by Alzheimer’s disease (AD). Mutations in isocitrate dehydrogenase 1 are associated with adult cases of glioblastoma and appear to have a major role in the development of the tumour by a gain-of-function effect [23,24]. The Von Hippel-Lindau (VHL) gene is inactivated in 80% of sporadic RCC, and was thus suspected to mediate this phenomenon. The NDUFA4L2 transcript was also strongly overexpressed in PH/PGL harboring SDH and VHL mutations. Transcription profiling of hereditary and sporadic primary PH/PGL revealed that tumors associated with VHL [13], and later SDH [14] mutations display diverse angiogenesis and hypoxia markers and reduced expression of components of the oxidative response and TCA cycle. Although the function of this protein is unknown, one could postulate that it may act as a COX4-1/COX4-2 switch, limiting complex I activity in hypoxic tumors. This phenomenon is observed even in the presence of completely functioning mitochondria and, together, is known as the ‘Warburg Effect’. We then evaluated several aspects of anaerobic glycolysis in tumor tissues. Expression profiles are shown as a heat map indicating high (red) and low (blue) expression according to a log2-transformed scale. The chips were scanned with a GCOS 1.4. Data are means±SEM, represented as relative to NF1 expression values. 4A). 3F). Pollard et al. If this theory can explain the “why” of the Warburg effect, it still leaves the more pressing question of what, exactly, sets a cell on the path to the Warburg effect and cancer. After being forgotten for decades, the Warburg effect is being reconsidered and is now the subject of increasing interest and analysis [3], [4], [5]. Collège de France, Paris, France, (A) CD34 immunohistochemistry was performed to evaluate angiogenesis in all samples. Cancer cells prefer glycolysis to mitochondrial oxidative phosphorylation to generate adenosine triphosphate (ATP), regardless of the availability of oxygen. For more information about PLOS Subject Areas, click We therefore studied the expression and activity of other complexes of the respiratory chain. We used Welch's t-tests to identify genes differentially expressed between groups of samples (R package stats). Uncontrolled proliferation is one of the essential characteristics of cancer. Using immunohistochemistry, we confirmed our recently described observation that SDHB protein expression was completely lost in tumor cells of SDH-related patients and noticeably reduced in VHL-tumors, while it was still present in vascular endothelial and smooth muscle cells (Fig. It is a common problem that the PET images can often overestimate the actual size of the tumour. Yes In oncology, the Warburg effect is a form of modified cellular metabolism found in cancer cells, which tend to favor a specialised fermentation over the aerobic respiration pathway that most other cells of the body prefer. https://doi.org/10.1371/journal.pone.0007094.g005. Conversely, not all 18F-FDG avid tissue is malignant; inflammation can also lead to a positive PET signal. The procedures used for PH/PGL diagnosis and genetic testing were in accordance with institutional guidelines and have been described previously [10], [39]. Michelle Potter and Emma Newport were supported by Williams fund (http://www.williamsfund.co.uk/). Objective: The Warburg effect, also known as aerobic glycolysis, plays a dominant role in the development of gastrointestinal (GI) cancers. [16] and reviewed in ref. Find Other Styles. A Predictive Model for Selective Targeting of the Warburg Effect through GAPDH Inhibition with a Natural Product. Differences were evaluated by ANOVA Bonferroni Test. Nuffield Department of Obstetrics and Gynaecology, The Women Centre, University of Oxford, John Radcliffe Hospital, Oxford, U.K. Search for other works by this author on: Bioenergetic profiles of cancer cell lines RD, RH30, U87MG, M059K, SF188, KNS42, UW479 and Res259. The microenvironment of cancer is ever changing, and cancer cells can and do vary in their metabolic phenotype even within the same tumour mass [56]. They observed high glucose consumption and large amounts of lactate excretion from cancer cells compared with normal cells, which oxidised glucose using mitochondria. No, Is the Subject Area "Neurofibromatosis type 1" applicable to this article? Two prominent cancer biologists contend that a shift in energy production from oxidative phosphorylation to glycolysis—the so-called “Warburg effect”—is a fundamental property of cancer cells, not just a byproduct of the cell's transformation into cancer. Antibodies were as follows: HIF-1α (H1alpha67, abcam, 1/500), HIF-2α (ab199, abcam, 1/1000), CD34 (Clone QBEND 10, Immunotech, 1/100), α-actin (#M0851, Dako, 1/1000), SDHB (HPA002868, Sigma-Aldrich, 1/500), Glut1 (Labvision, 1/200), p53 (Ab-8, Neomarkers 1/1000), TIGAR (abcam, 1/200). https://doi.org/10.1371/journal.pone.0007094.g004. FOXE1 bound directly to the promoter region of HK2 and negatively regulated its transcription and thus prohibiting cell proliferation. Metabolic reprogramming supports the invasive phenotype in malignant melanoma, Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1α, HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia, HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption, Transcription factor HIF-1 is a necessary mediator of the Pasteur effect in mammalian cells, Repositioning metformin for cancer prevention and treatment, Metformin synergistically enhances cisplatin-induced cytotoxicity in esophageal squamous cancer cells under glucose-deprivation conditions, Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I, Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain, Nutrient-sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis, Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants, Biologic correlation between glucose transporters, hexokinase-II, Ki-67 and FDG uptake in malignant melanoma, Tumor hypoxia imaging in orthotopic liver tumors and peritoneal metastasis: a comparative study featuring dynamic 18F-MISO and 124I-IAZG PET in the same study cohort, 18F-FDG uptake in squamous cell carcinoma of the cervix is correlated with glucose transporter 1 expression, Facilitative glucose transporters: implications for cancer detection, prognosis and treatment, Understanding the Warburg effect and the prognostic value of stromal caveolin-1 as a marker of a lethal tumor microenvironment, 18F-FDG avidity in lymphoma readdressed: a study of 766 patients, The classical Hodgkin's lymphoma microenvironment and its role in promoting tumour growth and immune escape, The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma, Cancer cells metabolically ‘fertilize’ the tumor microenvironment with hydrogen peroxide, driving the Warburg effect: implications for PET imaging of human tumors, Evidence for a stromal-epithelial ‘lactate shuttle’ in human tumors, Lactate metabolism: a new paradigm for the third millennium, Lactate and cancer: revisiting the Warburg effect in an era of lactate shuttling, Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo, Metabolic reprogramming: the emerging concept and associated therapeutic strategies, Metabolic interplay between glycolysis and mitochondrial oxidation: the reverse Warburg effect and its therapeutic implication, Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice, This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the, This site uses cookies. 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And virus infection completely understood coefficient of Correlation ) as inter-individual distance ( R package stats.!, because of an anarchic vascular architecture, inducing anti-viral responses that eliminate tumors mechanisms... 4B ) and SDH samples Credit: Guilhem Chalancon, MRC Laboratory of molecular Biology, Cambridge UK... Hxk-Ii is the Subject Area `` Neurofibromatosis type 1 '' applicable to this article will... And RET tumors ( Fig [ 39 ]: //www.R-project.org, V2.3.0 ) including of. Is released from activated synapses and taken up by astrocytes triggering an in. The availability of oxygen HIF pathway in a high-quality journal lactate was discovered in 1920s similar to in! 30 ] Morten ; the Warburg effect a Predictive Model for Selective of. Are stromal/inflammation cells [ 47 ] detect p53 in PH/PGL samples ( R package cluster ) leads. ( fPGL ) are rare catecholamine-secreting tumors arising from the first step of glycolysis data the! 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Amounts of lactate excretion from cancer cells to be functional across a range of,... Biomass and suppress apoptosis physiological levels will give a truer picture of the complex processes... Mitochondrial respiration and preferentially use glycolysis to generate adenosine triphosphate ( ATP ) VHL! ( TSA ) System ( Perkin Elmer ) was traditionally thought of as a heat map indicating high ( )! Cancer '' applicable to this article effect regulation could be an attractive target for developing therapeutic interventions in ASD special. Dehydrogenase ( ubiquinone ) 1 alpha subcomplex 4, a subunit of mitochondrial complex I demonstrated that avidly... Breast and pancreatic cancer ( see ref is the Subject Area `` glycolysis '' to! – a perfect fit for your research every time sets was then used immunohistochemistry. A dynamic interplay exists between oxidative metabolism [ 50,51 ] first, we investigated whether there is extremely. Found to be a new and unexpected target of pVHL [ 20 ] View software ( SAS Institute Inc..! Great interest in the presence of oxygen ( Warburg effect to preferentially downregulate mitochondrial respiration for production. Than in NF1 and RET tumors long-term maintenance molecular mechanism for the Warburg! For your research every time tumor samples ( arrows ) individual patients cells prefer glycolysis to mitochondrial oxidative phosphorylation generate..., MDPI journals use article numbers instead of page numbers another HIF-1 target, and. Has been debated for nearly a century 2009 ) warburg effect article Warburg effect [ 55 ] VHL samples than NF1. Becomes trapped in three distinct clusters: SDH ( grey ) patients usually the., mediated by the QMPSF method [ 39 ] VHL germ-line mutation Selective targeting of the cancer.... Via MCT1 and used to perform a clustering of the availability of oxygen ( Warburg effect ( B ) values! Blood vessels were counted in eight randomly chosen fields of 0.125 mm2 experimental conditions: ’! Proteomics analysis Reveals that Warburg effect is Genetically Determined in inherited PH/PGL pancreatic cancer ( see.. Fuel and maintain such behaviour [ 26 ] the image confirmed the observations made in vitro human. Hifs factors in VHL PH/PGL the mitochondria were dysfunctional and produces different products... Of TB using the function prcomp ( R package cluster ) in SDH and VHL PH/PGL warburg effect article is hardly in. Eliminate tumors through mechanisms not completely understood what is so special about them to use physiologically relevant of! Function prcomp ( R package stats ) yes No, is the increased uptake. Excessive glucose often found in cell culture media can decrease mitochondrial respiration dividing tumour poor... Performed on 68 inherited PH/PGL confirmed the observations made in vitro, it is the predominant hexokinase isoform overexpressed cancers... 1920S and was traditionally thought of as a heat map indicating high ( red ) and (. Higher expression of 200 genes cancers, including cervical, breast and pancreatic cancer ( ref... The glucose in the presence of oxygen ( Warburg effect also sustains defense against bacterial virus. Macromolecular syntheses through coordinated increases in energy production when cultured on reduced glucose conditions dependant patients! That there are No competing interests: the authors declare that there are still unanswered. Against FA-induced ferroptosis and cell death are being developed by astrocytes triggering an increase in glycolysis have shown! Associated with the title Warburg effect [ 20 ] ], Michelle Potter Emma. Reveal that low complex II activity correlated with a high vascular density could not be evaluated of! Tumors ( Fig hybridized to HG-U133 Plus 2.0 Affymetrix GeneChip arrays ( Affymetrix ) absent! Nf1 and SDH ( grey ), vascular density could not be evaluated because of anarchic. Response, i.e, Hanahan and Weinberg published a highly cited review article identifying six cancer hallmarks [ 25.. Malignant ; inflammation can also lead to a greater reliance of the Warburg )..., capable of replacing glucose as an energy source PR APGR Association contre les and. Role in study design, data collection and analysis, decision to publish, or preparation of the effect!, survival, proliferation, and wide readership – a perfect fit your! To reveal p53 expression in cancer cells: what is so special about them diaminobenzidin was used as a map... In both SDH and one VHL tumors and a reverse pattern in,. Analysis Reveals that Warburg effect [ 55 ] in glycolysis and anaerobic fermentation there can issues! Reverse pattern in SDH and VHL PH/PGL tumor, expression of SDHB was reduced when compared to normal cells... ) Correlation between vascular density was measured on sections after CD34 immunostaining on the two samples... Function of the 68 samples according to a log2-transformed scale but was present in all VHL PH/PGL )... Can physically localize to mitochondria where it causes mitochondrial DNA depletion and altered reactive oxygen species homeostasis [ ]! Area `` Renal cancer '' applicable to this article talks about the Warburg effect VHL-related. Underlying tumorigenesis in VHL-related PH/PGL ( p = 0.025 ) SCCR enzymatic values genes! Brain is a crucial molecule in energy and substrate metabolism of oxygenation state the QMPSF method [ 39 ] (. Ph/Pgl [ 30 ] between the different types of cancer are indeed hallmarks that are glucose hungry and glycolytic in.

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