Extracellular Metabolic Energetics Can Promote Cancer Progression
Open accessAbstract
Colorectal cancer primarily metastasizes to the liver and globally kills over 600,000 people annually. By functionally screening 661 microRNAs (miRNAs) in parallel during liver colonization, we have identified miR-551a and miR-483 as robust endogenous suppressors of liver colonization and metastasis. These miRNAs convergently target creatine kinase, brain-type (CKB), which phosphorylates the metabolite creatine, to generate phosphocreatine. CKB is released into the extracellular space by metastatic cells encountering hepatic hypoxia and catalyzes production of phosphocreatine, which is imported through the SLC6A8 transporter and used to generate ATP—fueling metastatic survival. Combinatorial therapeutic viral delivery of miR-551a and miR-483-5p through single-dose adeno-associated viral (AAV) delivery significantly suppressed colon cancer metastasis, as did CKB inhibition with a small-molecule inhibitor. Importantly, human liver metastases express higher CKB and SLC6A8 levels and reduced miR-551a/miR-483 levels relative to primary tumors. We identify the extracellular space as an important compartment for malignant energetic catalysis and therapeutic targeting.
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Hypoxic colorectal cancer cell lines release CKB into the extracellular space, where it catalyzes production of PCr using extracellular ATP as phosphate source.
“A number of hypoxic colorectal cancer cell lines have been found to release CKB into the extracellular space, where it catalyzed the production of PCr using extracellular ATP as the phosphate source [60].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [60]
The Results section on extracellular CKB reports release from metastatic LvM3b colorectal cancer cells and evidence that CKB uses extracellular ATP to produce phosphocreatine. The Discussion also states this mechanism directly. The cited passages do not establish CKB release from a number of cell lines specifically while they were hypoxic; hypoxia is examined separately as a challenge to cancer-cell survival. (LLM, conf=0.82)
Experimental — accuracy not yet measuredPCr is imported into cancer cells via SLC6A8 and generates ATP, enabling metastatic cancer cells to sustain energetic requirements despite hypoxic O2 levels in normal liver.
“This PCr was then imported into the cancer cells via SLC6A8 and generated ATP, thus enabling metastatic cancer cells to sustain their energetic requirements despite the physiologically hypoxic O2 levels in the normal liver [60].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [60]
Mice inoculated with colorectal cancer cells and treated with cyclocreatine showed significant reduction in liver metastases.
“The in vivo importance of this mechanism was demonstrated when mice inoculated with colorectal cancer cells and treated with cyclocreatine, an inhibitor of creatine metabolism, showed significant reduction in liver metastases [60].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [60]
Colon cancer cells experience hypoxia early after hepatic dissemination.
“Using a HIF-1 transcriptional luciferase reporter mouse, they determined that colon cancer cells experience hypoxia early after hepatic dissemination.”
From Hypoxic control of metastasis (2016) · cites this paper as [109]
Disseminated cancer cells increase their release of CKB, which helps them survive within the hypoxic microenvironment of the liver.
“They found that the disseminated cancer cells increase their release of the enzyme creatine kinase brain-type (CKB), which helps them survive within the hypoxic microenvironment of the liver (109).”
From Hypoxic control of metastasis (2016) · cites this paper as [109]
Hepatic hypoxia is a barrier for colon cancer cells early in metastatic dissemination, and cells overcome this metabolic stress by generating ATP from phosphocreatine reserves.
“suggesting that hepatic hypoxia is a barrier for colon cancer cells early in metastatic dissemination and that cells overcome this metabolic stress by generating ATP from phosphocreatine reserves (Fig. 3) (109).”
From Hypoxic control of metastasis (2016) · cites this paper as [109]
Depletion of CKB increased caspase-mediated cell death in hypoxic tumor cells within the liver.
“Depletion of CKB increased caspase-mediated cell death in hypoxic tumor cells within the liver”
From Hypoxic control of metastasis (2016) · cites this paper as [109]
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- Authors
- Loo, J. M., Scherl, A., Nguyen, A., Man, F. Y., Weinberg, E., Zeng, Z., Saltz, L., Paty, P. B., & Tavazoie, S. F.
- Affiliations
- Rockefeller University (US)
- Memorial Sloan Kettering Cancer Center (US)
- Corresponding author
- Tavazoie, Sohail F.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-01
- Volume
- 160
- Issue
- 3
- Pages
- 393-406
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4312495
- OpenAlex
- W1965265512
- Cited by
- 393
- References
- 56
- Citations by year
- 2026: 19 · 2025: 38 · 2024: 26 · 2023: 35 · 2022: 39 · 2021: 55 · 2020: 42 · 2019: 35 · 2018: 32 · 2017: 23 · 2016: 33 · 2015: 16
- FWCI
- 11.46
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Commons - RU (Rockefeller University) (submittedVersion, cc-by-nc-sa)
- Markus Library
- Funders
- National Institutes of Health (1dp2od006506-01)
- Weill Cornell Medical College
- National Institute of General Medical Sciences (T32GM007739)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- colorectal cancer, liver metastasis, microRNA, miR-483, phosphocreatine, SLC6A8, hepatic hypoxia, small molecule inhibitors
- MeSH terms
- Animals, Energy Metabolism, Extracellular Matrix, Humans, Liver Neoplasms, Male, Neoplasm Metastasis, Nerve Tissue Proteins, Colorectal Neoplasms, Gene Expression Regulation, Neoplastic, Mice, SCID, Mice, Inbred NOD, MicroRNAs, Cell Line, Tumor, Plasma Membrane Neurotransmitter Transport Proteins, Mice, Creatine Kinase, BB Form
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