A Role for the Mitochondrial Pyruvate Carrier as a Repressor of the Warburg Effect and Colon Cancer Cell Growth

Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2...

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Published in	Molecular cell Vol. 56; no. 3; pp. 400 - 413
Main Authors	Schell, John C., Olson, Kristofor A., Jiang, Lei, Hawkins, Amy J., Van Vranken, Jonathan G., Xie, Jianxin, Egnatchik, Robert A., Earl, Espen G., DeBerardinis, Ralph J., Rutter, Jared
Format	Journal Article
Language	English
Published	United States Elsevier Inc 06.11.2014
Subjects	agar Animals Anion Transport Proteins - metabolism cell growth Cell Proliferation Colonic Neoplasms colorectal neoplasms genes Glycolysis HEK293 Cells HT29 Cells Humans Mice, Nude mitochondria Mitochondria - metabolism Mitochondrial Membrane Transport Proteins - metabolism Mitochondrial Proteins - metabolism neoplasm cells Neoplasm Transplantation oxidation Oxidation-Reduction prognosis pyruvic acid stem cells
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Abstract	Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2 genes, modulates fractional pyruvate oxidation. MPC1 is deleted or underexpressed in multiple cancers and correlates with poor prognosis. Cancer cells re-expressing MPC1 and MPC2 display increased mitochondrial pyruvate oxidation, with no changes in cell growth in adherent culture. MPC re-expression exerted profound effects in anchorage-independent growth conditions, however, including impaired colony formation in soft agar, spheroid formation, and xenograft growth. We also observed a decrease in markers of stemness and traced the growth effects of MPC expression to the stem cell compartment. We propose that reduced MPC activity is an important aspect of cancer metabolism, perhaps through altering the maintenance and fate of stem cells. [Display omitted] •MPC1 downregulation/deletion in many cancers correlates with poor survival•The MPC complex is a node by which cancer cells regulate pyruvate metabolism•Re-expressing MPC1+2 in colon cancer cells reduces growth in 3D and xenografts•The deleterious effects of MPC re-expression manifest in the stem cell compartment Cancer cells enforce the metabolic perturbation known as the Warburg effect by reducing pyruvate utilization via loss of the mitochondrial pyruvate carrier (MPC). Re-expression of the MPC restores mitochondrial pyruvate oxidation and limits colon cancer cell growth in anchorage-independent culture and xenografts due to defects in the proliferating cell population.
AbstractList	Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2 genes, modulates fractional pyruvate oxidation. MPC1 is deleted or underexpressed in multiple cancers and correlates with poor prognosis. Cancer cells re-expressing MPC1 and MPC2 display increased mitochondrial pyruvate oxidation, with no changes in cell growth in adherent culture. MPC re-expression exerted profound effects in anchorage-independent growth conditions, however, including impaired colony formation in soft agar, spheroid formation, and xenograft growth. We also observed a decrease in markers of stemness and traced the growth effects of MPC expression to the stem cell compartment. We propose that reduced MPC activity is an important aspect of cancer metabolism, perhaps through altering the maintenance and fate of stem cells. Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2 genes, modulates fractional pyruvate oxidation. MPC1 is deleted or underexpressed in multiple cancers and correlates with poor prognosis. Cancer cells re-expressing MPC1 and MPC2 display increased mitochondrial pyruvate oxidation, with no changes in cell growth in adherent culture. MPC re-expression exerted profound effects in anchorage-independent growth conditions, however, including impaired colony formation in soft agar, spheroid formation, and xenograft growth. We also observed a decrease in markers of stemness and traced the growth effects of MPC expression to the stem cell compartment. We propose that reduced MPC activity is an important aspect of cancer metabolism, perhaps through altering the maintenance and fate of stem cells.Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2 genes, modulates fractional pyruvate oxidation. MPC1 is deleted or underexpressed in multiple cancers and correlates with poor prognosis. Cancer cells re-expressing MPC1 and MPC2 display increased mitochondrial pyruvate oxidation, with no changes in cell growth in adherent culture. MPC re-expression exerted profound effects in anchorage-independent growth conditions, however, including impaired colony formation in soft agar, spheroid formation, and xenograft growth. We also observed a decrease in markers of stemness and traced the growth effects of MPC expression to the stem cell compartment. We propose that reduced MPC activity is an important aspect of cancer metabolism, perhaps through altering the maintenance and fate of stem cells. Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2 genes, modulates fractional pyruvate oxidation. MPC1 is deleted or underexpressed in multiple cancers and correlates with poor prognosis. Cancer cells re-expressing MPC1 and MPC2 display increased mitochondrial pyruvate oxidation, with no changes in cell growth in adherent culture. MPC re-expression exerted profound effects in anchorage-independent growth conditions, however, including impaired colony formation in soft agar, spheroid formation, and xenograft growth. We also observed a decrease in markers of stemness and traced the growth effects of MPC expression to the stem cell compartment. We propose that reduced MPC activity is an important aspect of cancer metabolism, perhaps through altering the maintenance and fate of stem cells. Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the pyruvate generated from glycolysis. We show herein that the mitochondrial pyruvate carrier (MPC), composed of the products of the MPC1 and MPC2 genes, modulates fractional pyruvate oxidation. MPC1 is deleted or underexpressed in multiple cancers and correlates with poor prognosis. Cancer cells re-expressing MPC1 and MPC2 display increased mitochondrial pyruvate oxidation, with no changes in cell growth in adherent culture. MPC re-expression exerted profound effects in anchorage-independent growth conditions, however, including impaired colony formation in soft agar, spheroid formation, and xenograft growth. We also observed a decrease in markers of stemness and traced the growth effects of MPC expression to the stem cell compartment. We propose that reduced MPC activity is an important aspect of cancer metabolism, perhaps through altering the maintenance and fate of stem cells. [Display omitted] •MPC1 downregulation/deletion in many cancers correlates with poor survival•The MPC complex is a node by which cancer cells regulate pyruvate metabolism•Re-expressing MPC1+2 in colon cancer cells reduces growth in 3D and xenografts•The deleterious effects of MPC re-expression manifest in the stem cell compartment Cancer cells enforce the metabolic perturbation known as the Warburg effect by reducing pyruvate utilization via loss of the mitochondrial pyruvate carrier (MPC). Re-expression of the MPC restores mitochondrial pyruvate oxidation and limits colon cancer cell growth in anchorage-independent culture and xenografts due to defects in the proliferating cell population.
Author	Schell, John C. Rutter, Jared Egnatchik, Robert A. Earl, Espen G. Olson, Kristofor A. Van Vranken, Jonathan G. DeBerardinis, Ralph J. Jiang, Lei Hawkins, Amy J. Xie, Jianxin
AuthorAffiliation	2 Children’s Medical Center Research Institute, UT Southwestern Medical Center, 5323 Harry Hines Blvd, Dallas TX 75390-8502, USA 1 Department of Biochemistry, University of Utah School of Medicine, 15 N. Medical Drive East, Salt Lake City, UT 84112-5650, USA 3 Cell Signaling Technology, Inc., Danvers, MA 01923, USA
AuthorAffiliation_xml	– name: 3 Cell Signaling Technology, Inc., Danvers, MA 01923, USA – name: 1 Department of Biochemistry, University of Utah School of Medicine, 15 N. Medical Drive East, Salt Lake City, UT 84112-5650, USA – name: 2 Children’s Medical Center Research Institute, UT Southwestern Medical Center, 5323 Harry Hines Blvd, Dallas TX 75390-8502, USA
Author_xml	– sequence: 1 givenname: John C. surname: Schell fullname: Schell, John C. organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT 84112-5650, USA – sequence: 2 givenname: Kristofor A. surname: Olson fullname: Olson, Kristofor A. organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT 84112-5650, USA – sequence: 3 givenname: Lei surname: Jiang fullname: Jiang, Lei organization: Children’s Medical Center Research Institute, UT Southwestern Medical Center, Dallas, TX 75390-8502, USA – sequence: 4 givenname: Amy J. surname: Hawkins fullname: Hawkins, Amy J. organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT 84112-5650, USA – sequence: 5 givenname: Jonathan G. surname: Van Vranken fullname: Van Vranken, Jonathan G. organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT 84112-5650, USA – sequence: 6 givenname: Jianxin surname: Xie fullname: Xie, Jianxin organization: Cell Signaling Technology, Inc., Danvers, MA 01923, USA – sequence: 7 givenname: Robert A. surname: Egnatchik fullname: Egnatchik, Robert A. organization: Children’s Medical Center Research Institute, UT Southwestern Medical Center, Dallas, TX 75390-8502, USA – sequence: 8 givenname: Espen G. surname: Earl fullname: Earl, Espen G. organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT 84112-5650, USA – sequence: 9 givenname: Ralph J. surname: DeBerardinis fullname: DeBerardinis, Ralph J. organization: Children’s Medical Center Research Institute, UT Southwestern Medical Center, Dallas, TX 75390-8502, USA – sequence: 10 givenname: Jared surname: Rutter fullname: Rutter, Jared email: rutter@biochem.utah.edu organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT 84112-5650, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25458841$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work. Contact: Jared Rutter, rutter@biochem.utah.edu, Tel: 801-581-3340, Fax: 801-581-7959
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Snippet	Cancer cells are typically subject to profound metabolic alterations, including the Warburg effect wherein cancer cells oxidize a decreased fraction of the...
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SubjectTerms	agar Animals Anion Transport Proteins - metabolism cell growth Cell Proliferation Colonic Neoplasms colorectal neoplasms genes Glycolysis HEK293 Cells HT29 Cells Humans Mice, Nude mitochondria Mitochondria - metabolism Mitochondrial Membrane Transport Proteins - metabolism Mitochondrial Proteins - metabolism neoplasm cells Neoplasm Transplantation oxidation Oxidation-Reduction prognosis pyruvic acid stem cells
Title	A Role for the Mitochondrial Pyruvate Carrier as a Repressor of the Warburg Effect and Colon Cancer Cell Growth
URI	https://dx.doi.org/10.1016/j.molcel.2014.09.026 https://www.ncbi.nlm.nih.gov/pubmed/25458841 https://www.proquest.com/docview/1639486455 https://www.proquest.com/docview/2000213749 https://pubmed.ncbi.nlm.nih.gov/PMC4268416
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