“Energetic” Cancer Stem Cells (e-CSCs): A New Hyper-Metabolic and Proliferative Tumor Cell Phenotype, Driven by Mitochondrial Energy

Here, we provide the necessary evidence that mitochondrial metabolism drives the anchorage-independent proliferation of CSCs. Two human breast cancer cell lines, MCF7 [ER(+)] and MDA-MB-468 (triple-negative), were used as model systems. To directly address the issue of metabolic heterogeneity in can...

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Vydané v:Frontiers in oncology Ročník 8; s. 677
Hlavní autori: Fiorillo, Marco, Sotgia, Federica, Lisanti, Michael P.
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: Switzerland Frontiers Media S.A 05.02.2019
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Abstract Here, we provide the necessary evidence that mitochondrial metabolism drives the anchorage-independent proliferation of CSCs. Two human breast cancer cell lines, MCF7 [ER(+)] and MDA-MB-468 (triple-negative), were used as model systems. To directly address the issue of metabolic heterogeneity in cancer, we purified a new distinct sub-population of CSCs, based solely on their energetic profile. We propose the term "energetic" cancer stem cells (e-CSCs), to better describe this novel cellular phenotype. In a single step, we first isolated an auto-fluorescent cell sub-population, based on their high flavin-content, using flow-cytometry. Then, these cells were further subjected to a detailed phenotypic characterization. More specifically, e-CSCs were more glycolytic, with higher mitochondrial mass and showed significantly elevated oxidative metabolism. e-CSCs also demonstrated an increased capacity to undergo cell cycle progression, as well as enhanced anchorage-independent growth and ALDH-positivity. Most importantly, these e-CSCs could be effectively targeted by treatments with either (i) OXPHOS inhibitors (DPI) or (ii) a CDK4/6 inhibitor (Ribociclib). Finally, we were able to distinguish two distinct phenotypic sub-types of e-CSCs, depending on whether they were grown as 2D-monolayers or as 3D-spheroids. Remarkably, under 3D anchorage-independent growth conditions, e-CSCs were strictly dependent on oxidative mitochondrial metabolism. Unbiased proteomics analysis demonstrated the up-regulation of gene products specifically related to the anti-oxidant response, mitochondrial energy production, and mitochondrial biogenesis. Therefore, mitochondrial inhibitors should be further developed as promising anti-cancer agents, to directly target and eliminate the "fittest" e-CSCs. Our results have important implications for using e-CSCs, especially those derived from 3D-spheroids, (i) in tumor tissue bio-banking and (ii) as a new cellular platform for drug development.
AbstractList Here, we provide the necessary evidence that mitochondrial metabolism drives the anchorage-independent proliferation of CSCs. Two human breast cancer cell lines, MCF7 [ER(+)] and MDA-MB-468 (triple-negative), were used as model systems. To directly address the issue of metabolic heterogeneity in cancer, we purified a new distinct sub-population of CSCs, based solely on their energetic profile. We propose the term "energetic" cancer stem cells (e-CSCs), to better describe this novel cellular phenotype. In a single step, we first isolated an auto-fluorescent cell sub-population, based on their high flavin-content, using flow-cytometry. Then, these cells were further subjected to a detailed phenotypic characterization. More specifically, e-CSCs were more glycolytic, with higher mitochondrial mass and showed significantly elevated oxidative metabolism. e-CSCs also demonstrated an increased capacity to undergo cell cycle progression, as well as enhanced anchorage-independent growth and ALDH-positivity. Most importantly, these e-CSCs could be effectively targeted by treatments with either (i) OXPHOS inhibitors (DPI) or (ii) a CDK4/6 inhibitor (Ribociclib). Finally, we were able to distinguish two distinct phenotypic sub-types of e-CSCs, depending on whether they were grown as 2D-monolayers or as 3D-spheroids. Remarkably, under 3D anchorage-independent growth conditions, e-CSCs were strictly dependent on oxidative mitochondrial metabolism. Unbiased proteomics analysis demonstrated the up-regulation of gene products specifically related to the anti-oxidant response, mitochondrial energy production, and mitochondrial biogenesis. Therefore, mitochondrial inhibitors should be further developed as promising anti-cancer agents, to directly target and eliminate the "fittest" e-CSCs. Our results have important implications for using e-CSCs, especially those derived from 3D-spheroids, (i) in tumor tissue bio-banking and (ii) as a new cellular platform for drug development.
Here, we provide the necessary evidence that mitochondrial metabolism drives the anchorage-independent proliferation of CSCs. Two human breast cancer cell lines, MCF7 [ER(+)] and MDA-MB-468 (triple-negative), were used as model systems. To directly address the issue of metabolic heterogeneity in cancer, we purified a new distinct sub-population of CSCs, based solely on their energetic profile. We propose the term "energetic" cancer stem cells (e-CSCs), to better describe this novel cellular phenotype. In a single step, we first isolated an auto-fluorescent cell sub-population, based on their high flavin-content, using flow-cytometry. Then, these cells were further subjected to a detailed phenotypic characterization. More specifically, e-CSCs were more glycolytic, with higher mitochondrial mass and showed significantly elevated oxidative metabolism. e-CSCs also demonstrated an increased capacity to undergo cell cycle progression, as well as enhanced anchorage-independent growth and ALDH-positivity. Most importantly, these e-CSCs could be effectively targeted by treatments with either (i) OXPHOS inhibitors (DPI) or (ii) a CDK4/6 inhibitor (Ribociclib). Finally, we were able to distinguish two distinct phenotypic sub-types of e-CSCs, depending on whether they were grown as 2D-monolayers or as 3D-spheroids. Remarkably, under 3D anchorage-independent growth conditions, e-CSCs were strictly dependent on oxidative mitochondrial metabolism. Unbiased proteomics analysis demonstrated the up-regulation of gene products specifically related to the anti-oxidant response, mitochondrial energy production, and mitochondrial biogenesis. Therefore, mitochondrial inhibitors should be further developed as promising anti-cancer agents, to directly target and eliminate the "fittest" e-CSCs. Our results have important implications for using e-CSCs, especially those derived from 3D-spheroids, (i) in tumor tissue bio-banking and (ii) as a new cellular platform for drug development.Here, we provide the necessary evidence that mitochondrial metabolism drives the anchorage-independent proliferation of CSCs. Two human breast cancer cell lines, MCF7 [ER(+)] and MDA-MB-468 (triple-negative), were used as model systems. To directly address the issue of metabolic heterogeneity in cancer, we purified a new distinct sub-population of CSCs, based solely on their energetic profile. We propose the term "energetic" cancer stem cells (e-CSCs), to better describe this novel cellular phenotype. In a single step, we first isolated an auto-fluorescent cell sub-population, based on their high flavin-content, using flow-cytometry. Then, these cells were further subjected to a detailed phenotypic characterization. More specifically, e-CSCs were more glycolytic, with higher mitochondrial mass and showed significantly elevated oxidative metabolism. e-CSCs also demonstrated an increased capacity to undergo cell cycle progression, as well as enhanced anchorage-independent growth and ALDH-positivity. Most importantly, these e-CSCs could be effectively targeted by treatments with either (i) OXPHOS inhibitors (DPI) or (ii) a CDK4/6 inhibitor (Ribociclib). Finally, we were able to distinguish two distinct phenotypic sub-types of e-CSCs, depending on whether they were grown as 2D-monolayers or as 3D-spheroids. Remarkably, under 3D anchorage-independent growth conditions, e-CSCs were strictly dependent on oxidative mitochondrial metabolism. Unbiased proteomics analysis demonstrated the up-regulation of gene products specifically related to the anti-oxidant response, mitochondrial energy production, and mitochondrial biogenesis. Therefore, mitochondrial inhibitors should be further developed as promising anti-cancer agents, to directly target and eliminate the "fittest" e-CSCs. Our results have important implications for using e-CSCs, especially those derived from 3D-spheroids, (i) in tumor tissue bio-banking and (ii) as a new cellular platform for drug development.
Author Fiorillo, Marco
Lisanti, Michael P.
Sotgia, Federica
AuthorAffiliation 1 Biomedical Research Centre (BRC), Translational Medicine, School of Environment and Life Sciences, University of Salford , Manchester , United Kingdom
2 The Department of Pharmacy, Health and Nutritional Sciences, The University of Calabria , Cosenza , Italy
AuthorAffiliation_xml – name: 1 Biomedical Research Centre (BRC), Translational Medicine, School of Environment and Life Sciences, University of Salford , Manchester , United Kingdom
– name: 2 The Department of Pharmacy, Health and Nutritional Sciences, The University of Calabria , Cosenza , Italy
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  givenname: Michael P.
  surname: Lisanti
  fullname: Lisanti, Michael P.
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Keywords Ribociclib
mitochondrial OXPHOS
cancer stem-like cells (CSCs)
metabolism
Diphenyleneiodonium (DPI)
glycolysis
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Reviewed by: Francesco De Francesco, Azienda Ospedaliero Universitaria Ospedali Riuniti, Italy; Cesar Cardenas, Universidad Mayor, Chile
Edited by: Massimo Bonora, Albert Einstein College of Medicine, United States
This article was submitted to Molecular and Cellular Oncology, a section of the journal Frontiers in Oncology
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Snippet Here, we provide the necessary evidence that mitochondrial metabolism drives the anchorage-independent proliferation of CSCs. Two human breast cancer cell...
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SubjectTerms cancer stem-like cells (CSCs)
Diphenyleneiodonium (DPI)
glycolysis
metabolism
mitochondrial OXPHOS
Oncology
Ribociclib
Title “Energetic” Cancer Stem Cells (e-CSCs): A New Hyper-Metabolic and Proliferative Tumor Cell Phenotype, Driven by Mitochondrial Energy
URI https://www.ncbi.nlm.nih.gov/pubmed/30805301
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