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Cancers
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The Warburg Effect in Cancers
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The Warburg Effect in Cancers

A special issue of Cancers (ISSN 2072-6694). This special issue belongs to the section "Tumor Microenvironment".

Deadline for manuscript submissions: 30 June 2025 | Viewed by 8597

Special Issue Editors

Dr. Ying Liu

E-Mail Website
Guest Editor
Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
Interests: cancer metabolism; cytokine signaling; genetics and genomics; cancer therapeutics
Dr. Hui Feng

E-Mail Website
Guest Editor
Departments of Pharmacology and Medicine, Boston University Chobanian & Avedisian School of Medicine, Boston, MA 02118, USA
Interests: cancer metabolism; endoplasmic reticulum-associated degradation; tumor immunology; zebrafish genetics; cancer therapeutics

Special Issue Information

Dear Colleagues,

Nearly a century ago, Otto Warburg observed that cancer cells utilize aerobic glycolysis, a phenomenon later referred to as the “Warburg effect”. This altered metabolism is characterized by the elevated rates of glucose uptake and the fermentation of glucose to lactate, even in the presence of oxygen and fully functional mitochondria. The Warburg effect can facilitate tumor cell growth and metastasis through multiple mechanisms. It enables cancer cells to generate ATP and metabolic intermediates to synthesize nucleotide acids, proteins, and lipids, building blocks essential for cell proliferation. In addition, aerobic glycolysis helps maintain redox homeostasis by reducing ROS production in the mitochondria. Interestingly, accumulating evidence indicates that this metabolic alteration can reshape the tumor microenvironment through lactate secretion by tumor cells, leading to cancer cell proliferation and metastasis. Despite these major advances, a comprehensive understanding of how the Warburg Effect impacts cancer is needed to develop diagnostic tools and effective therapies for cancers.

This Special Issue will focus on the Warburg effect and its role in tumorigenesis, highlighting new findings and fresh insights into the metabolic reprogramming of cancer cells, how it may impact the tumor microenvironment, and strategies for therapeutic intervention.

Dr. Ying Liu
Dr. Hui Feng
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cancers is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • aerobic glycolysis
  • redox balance
  • tumor microenvironment
  • tumor initiation
  • tumor metastasis
  • cancer diagnosis
  • patient prognosis
 

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Published Papers (5 papers)

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Research

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29 pages, 6547 KiB  
Article
Deciphering the Metabolic Basis and Molecular Circuitry of the Warburg Paradox in Lymphoma
by Dashnamoorthy Ravi, Athena Kritharis and Andrew M. Evens
Cancers 2024, 16(21), 3606; https://doi.org/10.3390/cancers16213606 - 25 Oct 2024
Viewed by 969
Abstract
Background/Objectives: Warburg’s metabolic paradox illustrates that malignant cells require both glucose and oxygen to survive, even after converting glucose into lactate. It remains unclear whether sparing glucose from oxidation intersects with TCA cycle continuity and if this confers any metabolic advantage in [...] Read more.
Background/Objectives: Warburg’s metabolic paradox illustrates that malignant cells require both glucose and oxygen to survive, even after converting glucose into lactate. It remains unclear whether sparing glucose from oxidation intersects with TCA cycle continuity and if this confers any metabolic advantage in proliferating cancers. This study seeks to understand the mechanistic basis of Warburg’s paradox and its overall implications for lymphomagenesis. Methods: Using metabolomics, we first examined the metabolomic profiles, glucose, and glutamine carbon labeling patterns in the metabolism during the cell cycle. We then investigated proliferation-specific metabolic features of malignant and nonmalignant cells. Finally, through bioinformatics and the identification of appropriate pharmacological targets, we established malignant-specific proliferative implications for the Warburg paradox associated with metabolic features in this study. Results: Our results indicate that pyruvate, lactate, and alanine levels surge during the S phase and are correlated with nucleotide synthesis. By using 13C1,2-Glucose and 13C6, 15N2-Glutamine isotope tracers, we observed that the transamination of pyruvate to alanine is elevated in lymphoma and coincides with the entry of glutamine carbon into the TCA cycle. Finally, by using fludarabine as a strong inhibitor of lymphoma, we demonstrate that disrupting the transamination of pyruvate to alanine correlates with the simultaneous suppression of glucose-derived nucleotide biosynthesis and glutamine carbon entry into the TCA cycle. Conclusions: We conclude that the transamination of pyruvate to alanine intersects with reduced glucose oxidation and maintains the TCA cycle as a critical metabolic feature of Warburg’s paradox and lymphomagenesis. Full article
(This article belongs to the Special Issue The Warburg Effect in Cancers)
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Review

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13 pages, 288 KiB  
Review
Is Cancer Metabolism an Atavism?
by Eric Fanchon and Angélique Stéphanou
Cancers 2024, 16(13), 2415; https://doi.org/10.3390/cancers16132415 - 29 Jun 2024
Viewed by 1379
Abstract
The atavistic theory of cancer posits that cancer emerges and progresses through the reversion of cellular phenotypes to more ancestral types with genomic and epigenetic changes deactivating recently evolved genetic modules and activating ancient survival mechanisms. This theory aims at explaining the known [...] Read more.
The atavistic theory of cancer posits that cancer emerges and progresses through the reversion of cellular phenotypes to more ancestral types with genomic and epigenetic changes deactivating recently evolved genetic modules and activating ancient survival mechanisms. This theory aims at explaining the known cancer hallmarks and the paradox of cancer’s predictable progression despite the randomness of genetic mutations. Lineweaver and colleagues recently proposed the Serial Atavism Model (SAM), an enhanced version of the atavistic theory, which suggests that cancer progression involves multiple atavistic reversions where cells regress through evolutionary stages, losing recently evolved traits first and reactivating primitive ones later. The Warburg effect, where cancer cells upregulate glycolysis and lactate production in the presence of oxygen instead of using oxidative phosphorylation, is one of the key feature of the SAM. It is associated with the metabolism of ancient cells living on Earth before the oxygenation of the atmosphere. This review addresses the question of whether cancer metabolism can be considered as an atavistic reversion. By analyzing several known characteristics of cancer metabolism, we reach the conclusion that this version of the atavistic theory does not provide an adequate conceptual frame for cancer research. Cancer metabolism spans a whole spectrum of metabolic states which cannot be fully explained by a sequential reversion to an ancient state. Moreover, we interrogate the nature of cancer metabolism and discuss its characteristics within the framework of the SAM. Full article
(This article belongs to the Special Issue The Warburg Effect in Cancers)
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20 pages, 3078 KiB  
Review
Importance of Michaelis Constants for Cancer Cell Redox Balance and Lactate Secretion—Revisiting the Warburg Effect
by Michael Niepmann
Cancers 2024, 16(13), 2290; https://doi.org/10.3390/cancers16132290 - 21 Jun 2024
Cited by 1 | Viewed by 1430
Abstract
Cancer cells metabolize a large fraction of glucose to lactate, even under a sufficient oxygen supply. This phenomenon—the “Warburg Effect”—is often regarded as not yet understood. Cancer cells change gene expression to increase the uptake and utilization of glucose for biosynthesis pathways and [...] Read more.
Cancer cells metabolize a large fraction of glucose to lactate, even under a sufficient oxygen supply. This phenomenon—the “Warburg Effect”—is often regarded as not yet understood. Cancer cells change gene expression to increase the uptake and utilization of glucose for biosynthesis pathways and glycolysis, but they do not adequately up-regulate the tricarboxylic acid (TCA) cycle and oxidative phosphorylation (OXPHOS). Thereby, an increased glycolytic flux causes an increased production of cytosolic NADH. However, since the corresponding gene expression changes are not neatly fine-tuned in the cancer cells, cytosolic NAD+ must often be regenerated by loading excess electrons onto pyruvate and secreting the resulting lactate, even under sufficient oxygen supply. Interestingly, the Michaelis constants (KM values) of the enzymes at the pyruvate junction are sufficient to explain the priorities for pyruvate utilization in cancer cells: 1. mitochondrial OXPHOS for efficient ATP production, 2. electrons that exceed OXPHOS capacity need to be disposed of and secreted as lactate, and 3. biosynthesis reactions for cancer cell growth. In other words, a number of cytosolic electrons need to take the “emergency exit” from the cell by lactate secretion to maintain the cytosolic redox balance. Full article
(This article belongs to the Special Issue The Warburg Effect in Cancers)
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26 pages, 1929 KiB  
Review
Metabolic Signature of Warburg Effect in Cancer: An Effective and Obligatory Interplay between Nutrient Transporters and Catabolic/Anabolic Pathways to Promote Tumor Growth
by Marilyn Mathew, Nhi T. Nguyen, Yangzom D. Bhutia, Sathish Sivaprakasam and Vadivel Ganapathy
Cancers 2024, 16(3), 504; https://doi.org/10.3390/cancers16030504 - 24 Jan 2024
Cited by 10 | Viewed by 3256 | Correction
Abstract
Aerobic glycolysis in cancer cells, originally observed by Warburg 100 years ago, which involves the production of lactate as the end product of glucose breakdown even in the presence of adequate oxygen, is the foundation for the current interest in the cancer-cell-specific reprograming [...] Read more.
Aerobic glycolysis in cancer cells, originally observed by Warburg 100 years ago, which involves the production of lactate as the end product of glucose breakdown even in the presence of adequate oxygen, is the foundation for the current interest in the cancer-cell-specific reprograming of metabolic pathways. The renewed interest in cancer cell metabolism has now gone well beyond the original Warburg effect related to glycolysis to other metabolic pathways that include amino acid metabolism, one-carbon metabolism, the pentose phosphate pathway, nucleotide synthesis, antioxidant machinery, etc. Since glucose and amino acids constitute the primary nutrients that fuel the altered metabolic pathways in cancer cells, the transporters that mediate the transfer of these nutrients and their metabolites not only across the plasma membrane but also across the mitochondrial and lysosomal membranes have become an integral component of the expansion of the Warburg effect. In this review, we focus on the interplay between these transporters and metabolic pathways that facilitates metabolic reprogramming, which has become a hallmark of cancer cells. The beneficial outcome of this recent understanding of the unique metabolic signature surrounding the Warburg effect is the identification of novel drug targets for the development of a new generation of therapeutics to treat cancer. Full article
(This article belongs to the Special Issue The Warburg Effect in Cancers)
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Other

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2 pages, 4193 KiB  
Correction
Correction: Mathew et al. Metabolic Signature of Warburg Effect in Cancer: An Effective and Obligatory Interplay between Nutrient Transporters and Catabolic/Anabolic Pathways to Promote Tumor Growth. Cancers 2024, 16, 504
by Marilyn Mathew, Nhi T. Nguyen, Yangzom D. Bhutia, Sathish Sivaprakasam and Vadivel Ganapathy
Cancers 2024, 16(9), 1627; https://doi.org/10.3390/cancers16091627 - 24 Apr 2024
Viewed by 679
Abstract
In the original publication [...] Full article
(This article belongs to the Special Issue The Warburg Effect in Cancers)
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