Using the “reverse Warburg effect” to identify high-risk breast cancer patients: Stromal MCT4 predicts poor clinical outcome in triple-negative breast cancers
Open accessAbstract
We have recently proposed a new model of cancer metabolism to explain the role of aerobic glycolysis and L-lactate production in fueling tumor growth and metastasis. In this model, cancer cells secrete hydrogen peroxide (H2O2), initiating oxidative stress and aerobic glycolysis in the tumor stroma. This, in turn, drives L-lactate secretion from cancer-associated fibroblasts. Secreted L-lactate then fuels oxidative mitochondrial metabolism (OXPHOS) in epithelial cancer cells, by acting as a paracrine onco-metabolite. We have previously termed this type of two-compartment tumor metabolism the "Reverse Warburg Effect," as aerobic glycolysis takes place in stromal fibroblasts, rather than epithelial cancer cells. Here, we used MCT4 immuno-staining of human breast cancer tissue microarrays (TMAs; > 180 triple-negative patients) to directly assess the prognostic value of the "Reverse Warburg Effect." MCT4 expression is a functional marker of hypoxia, oxidative stress, aerobic glycolysis, and L-lactate efflux. Remarkably, high stromal MCT4 levels (score = 2) were specifically associated with decreased overall survival (< 18% survival at 10 y post-diagnosis). In contrast, patients with absent stromal MCT4 expression (score = 0), had 10-y survival rates of ~97% (p-value < 10 (-32) ). High stromal levels of MCT4 were strictly correlated with a loss of stromal Cav-1 (p-value < 10 (-14) ), a known marker of early tumor recurrence and metastasis. In fact, the combined use of stromal Cav-1 and stromal MCT4 allowed us to more precisely identify high-risk triple-negative breast cancer patients, consistent with the goal of individualized risk-assessment and personalized cancer treatment. However, epithelial MCT4 staining had no prognostic value, indicating that the "conventional" Warburg effect does not predict clinical outcome. Thus, the "Reverse Warburg Effect" or "parasitic" energy-transfer is a key determinant of poor overall patient survival. As MCT4 is a druggable-target, MCT4 inhibitors should be developed for the treatment of aggressive breast cancers, and possibly other types of human cancers. Similarly, we discuss how stromal MCT4 could be used as a biomarker for identifying high-risk cancer patients that could likely benefit from treatment with FDA-approved drugs or existing MCT-inhibitors (such as, AR-C155858, AR-C117977, and AZD-3965).
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Lactate produced by cancer-associated fibroblasts can enter the TCA cycle of cancer cells.
“It has been reported that lactate produced by cancer-associated fibroblasts can enter the TCA cycle of cancer cells (Bonuccelli et al., 2014; Witkiewicz et al., 2012), and lactate produced in hypoxic regions of a tumor can fuel respiration in well-oxygenated tumor cells (Kennedy et al., 2013; Sonveaux et al., 2008).”
From Targeting Metabolism for Cancer Therapy (2017) · cites this paper as Witkiewicz et al., 2012
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- Authors
- Witkiewicz, A. K., Whitaker-Menezes, D., Dasgupta, A., Philp, N. J., Lin, Z., Gandara, R., Sneddon, S., Martinez-Outschoorn, U. E., Sotgia, F., & Lisanti, M. P.
- Affiliations
- Thomas Jefferson University (US)
- Manchester Academic Health Science Centre (GB)
- Corresponding author
- Witkiewicz, Agnieszka K.
- Lisanti, Michael P.
- ORCID
- Venue
- Cell Cycle
- Publisher
- Informa UK Limited
- Published
- 2012-03-15
- Volume
- 11
- Issue
- 6
- Pages
- 1108-1117
- ISSN
- 1538-4101 (ISSN-L)
- 1551-4005
- PMC
- PMC3335917
- OpenAlex
- W2057690410
- Cited by
- 239
- References
- 71
- Citations by year
- 2026: 9 · 2025: 2 · 2024: 4 · 2023: 17 · 2022: 15 · 2021: 17 · 2020: 21 · 2019: 11 · 2018: 19 · 2017: 11 · 2016: 19 · 2015: 21 · 2014: 25 · 2013: 23 · 2012: 25
- FWCI
- 9.95
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Cell Cycle (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- National Cancer Institute (R01CA107382, R01 CA75503, R01-CA-86072, R01CA120876, R01 CA70896, R01CA086072, R01CA080250, R01CA075503, R01CA098779, R01CA070896, P30CA056036, P30 CA 56036)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR055660)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- reverse Warburg effect, triple-negative breast cancer, MCT4, cancer-associated fibroblasts, aerobic glycolysis, L-lactate, oxidative stress, hydrogen peroxide, caveolin-1, tumor stroma, overall survival, prognostic factors, cancer metabolism, metastasis, hypoxia, individual risk assessment, Warburg effect, oncometabolites, oxidative phosphorylation
- MeSH terms
- Adult, Aged, Breast Neoplasms, Epithelium, Female, Fibroblasts, Glycolysis, Humans, Hydrogen Peroxide, Immunoassay, Middle Aged, Muscle Proteins, Oxidative Phosphorylation, Predictive Value of Tests, Risk Factors, Staining and Labeling, Cohort Studies, Biomarkers, Stromal Cells, Oxidative Stress, Risk Assessment, Lactic Acid, Monocarboxylic Acid Transporters, Caveolin 1, Kaplan-Meier Estimate, Neoplasm Grading
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 ›
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