Glycolysis Inhibition Inactivates ABC Transporters to Restore Drug Sensitivity in Malignant Cells

Cancer cells eventually acquire drug resistance largely via the aberrant expression of ATP-binding cassette (ABC) transporters, ATP-dependent efflux pumps. Because cancer cells produce ATP mostly through glycolysis, in the present study we explored the effects of inhibiting glycolysis on the ABC tra...

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Published inPloS one Vol. 6; no. 11; p. e27222
Main Authors Nakano, Ayako, Tsuji, Daisuke, Miki, Hirokazu, Cui, Qu, Sayed, Salah Mohamed El, Ikegame, Akishige, Oda, Asuka, Amou, Hiroe, Nakamura, Shingen, Harada, Takeshi, Fujii, Shiro, Kagawa, Kumiko, Takeuchi, Kyoko, Sakai, Akira, Ozaki, Shuji, Okano, Kazuma, Nakamura, Takahiro, Itoh, Kohji, Matsumoto, Toshio, Abe, Masahiro
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 02.11.2011
Public Library of Science (PLoS)
Subjects
Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0027222

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Abstract Cancer cells eventually acquire drug resistance largely via the aberrant expression of ATP-binding cassette (ABC) transporters, ATP-dependent efflux pumps. Because cancer cells produce ATP mostly through glycolysis, in the present study we explored the effects of inhibiting glycolysis on the ABC transporter function and drug sensitivity of malignant cells. Inhibition of glycolysis by 3-bromopyruvate (3BrPA) suppressed ATP production in malignant cells, and restored the retention of daunorubicin or mitoxantrone in ABC transporter-expressing, RPMI8226 (ABCG2), KG-1 (ABCB1) and HepG2 cells (ABCB1 and ABCG2). Interestingly, although side population (SP) cells isolated from RPMI8226 cells exhibited higher levels of glycolysis with an increased expression of genes involved in the glycolytic pathway, 3BrPA abolished Hoechst 33342 exclusion in SP cells. 3BrPA also disrupted clonogenic capacity in malignant cell lines including RPMI8226, KG-1, and HepG2. Furthermore, 3BrPA restored cytotoxic effects of daunorubicin and doxorubicin on KG-1 and RPMI8226 cells, and markedly suppressed subcutaneous tumor growth in combination with doxorubicin in RPMI8226-implanted mice. These results collectively suggest that the inhibition of glycolysis is able to overcome drug resistance in ABC transporter-expressing malignant cells through the inactivation of ABC transporters and impairment of SP cells with enhanced glycolysis as well as clonogenic cells.
AbstractList Cancer cells eventually acquire drug resistance largely via the aberrant expression of ATP-binding cassette (ABC) transporters, ATP-dependent efflux pumps. Because cancer cells produce ATP mostly through glycolysis, in the present study we explored the effects of inhibiting glycolysis on the ABC transporter function and drug sensitivity of malignant cells. Inhibition of glycolysis by 3-bromopyruvate (3BrPA) suppressed ATP production in malignant cells, and restored the retention of daunorubicin or mitoxantrone in ABC transporter-expressing, RPMI8226 (ABCG2), KG-1 (ABCB1) and HepG2 cells (ABCB1 and ABCG2). Interestingly, although side population (SP) cells isolated from RPMI8226 cells exhibited higher levels of glycolysis with an increased expression of genes involved in the glycolytic pathway, 3BrPA abolished Hoechst 33342 exclusion in SP cells. 3BrPA also disrupted clonogenic capacity in malignant cell lines including RPMI8226, KG-1, and HepG2. Furthermore, 3BrPA restored cytotoxic effects of daunorubicin and doxorubicin on KG-1 and RPMI8226 cells, and markedly suppressed subcutaneous tumor growth in combination with doxorubicin in RPMI8226-implanted mice. These results collectively suggest that the inhibition of glycolysis is able to overcome drug resistance in ABC transporter-expressing malignant cells through the inactivation of ABC transporters and impairment of SP cells with enhanced glycolysis as well as clonogenic cells.
Cancer cells eventually acquire drug resistance largely via the aberrant expression of ATP-binding cassette (ABC) transporters, ATP-dependent efflux pumps. Because cancer cells produce ATP mostly through glycolysis, in the present study we explored the effects of inhibiting glycolysis on the ABC transporter function and drug sensitivity of malignant cells. Inhibition of glycolysis by 3-bromopyruvate (3BrPA) suppressed ATP production in malignant cells, and restored the retention of daunorubicin or mitoxantrone in ABC transporter-expressing, RPMI8226 (ABCG2), KG-1 (ABCB1) and HepG2 cells (ABCB1 and ABCG2). Interestingly, although side population (SP) cells isolated from RPMI8226 cells exhibited higher levels of glycolysis with an increased expression of genes involved in the glycolytic pathway, 3BrPA abolished Hoechst 33342 exclusion in SP cells. 3BrPA also disrupted clonogenic capacity in malignant cell lines including RPMI8226, KG-1, and HepG2. Furthermore, 3BrPA restored cytotoxic effects of daunorubicin and doxorubicin on KG-1 and RPMI8226 cells, and markedly suppressed subcutaneous tumor growth in combination with doxorubicin in RPMI8226-implanted mice. These results collectively suggest that the inhibition of glycolysis is able to overcome drug resistance in ABC transporter-expressing malignant cells through the inactivation of ABC transporters and impairment of SP cells with enhanced glycolysis as well as clonogenic cells.Cancer cells eventually acquire drug resistance largely via the aberrant expression of ATP-binding cassette (ABC) transporters, ATP-dependent efflux pumps. Because cancer cells produce ATP mostly through glycolysis, in the present study we explored the effects of inhibiting glycolysis on the ABC transporter function and drug sensitivity of malignant cells. Inhibition of glycolysis by 3-bromopyruvate (3BrPA) suppressed ATP production in malignant cells, and restored the retention of daunorubicin or mitoxantrone in ABC transporter-expressing, RPMI8226 (ABCG2), KG-1 (ABCB1) and HepG2 cells (ABCB1 and ABCG2). Interestingly, although side population (SP) cells isolated from RPMI8226 cells exhibited higher levels of glycolysis with an increased expression of genes involved in the glycolytic pathway, 3BrPA abolished Hoechst 33342 exclusion in SP cells. 3BrPA also disrupted clonogenic capacity in malignant cell lines including RPMI8226, KG-1, and HepG2. Furthermore, 3BrPA restored cytotoxic effects of daunorubicin and doxorubicin on KG-1 and RPMI8226 cells, and markedly suppressed subcutaneous tumor growth in combination with doxorubicin in RPMI8226-implanted mice. These results collectively suggest that the inhibition of glycolysis is able to overcome drug resistance in ABC transporter-expressing malignant cells through the inactivation of ABC transporters and impairment of SP cells with enhanced glycolysis as well as clonogenic cells.
Audience Academic
Author Amou, Hiroe
Ikegame, Akishige
Nakano, Ayako
Takeuchi, Kyoko
Tsuji, Daisuke
Okano, Kazuma
Cui, Qu
Harada, Takeshi
Itoh, Kohji
Nakamura, Shingen
Sayed, Salah Mohamed El
Abe, Masahiro
Kagawa, Kumiko
Oda, Asuka
Matsumoto, Toshio
Miki, Hirokazu
Sakai, Akira
Fujii, Shiro
Ozaki, Shuji
Nakamura, Takahiro
AuthorAffiliation 5 Department of Hematology and Oncology, RIRBM, Hiroshima University, Hiroshima, Japan
1 Department of Medicine and Bioregulatory Sciences, University of Tokushima Graduate School of Medicine, Tokushima, Japan
University of Nebraska – Lincoln, United States of America
2 Department of Medicinal Biotechnology, Institute for Medicinal Research, University of Tokushima Graduate School of Pharmaceutical Sciences, Tokushima, Japan
3 Department of Pediatrics, University of Tokushima Graduate School of Medicine, Tokushima, Japan
6 Division of Internal Medicine, Tokushima Prefectural Hospital, Tokushima, Japan
4 Division of Transfusion Medicine, Tokushima University Hospital, Tokushima, Japan
AuthorAffiliation_xml – name: 1 Department of Medicine and Bioregulatory Sciences, University of Tokushima Graduate School of Medicine, Tokushima, Japan
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– name: 6 Division of Internal Medicine, Tokushima Prefectural Hospital, Tokushima, Japan
– name: University of Nebraska – Lincoln, United States of America
– name: 4 Division of Transfusion Medicine, Tokushima University Hospital, Tokushima, Japan
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22073292$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2011 Public Library of Science
2011 Nakano et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Nakano et al. 2011
Copyright_xml – notice: COPYRIGHT 2011 Public Library of Science
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– notice: Nakano et al. 2011
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Conceived and designed the experiments: AN MA TM. Performed the experiments: AN DT QC HM AO HA SN KO TN SMES. Analyzed the data: AN DT KI SO TM MA. Contributed reagents/materials/analysis tools: AN HM AO AI HA TH SF KK KT AS SO MA TM . Wrote the paper: AN TM MA.
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Snippet Cancer cells eventually acquire drug resistance largely via the aberrant expression of ATP-binding cassette (ABC) transporters, ATP-dependent efflux pumps....
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SubjectTerms ABC transporter
ABC transporters
Aberration
Adenosine Triphosphate - biosynthesis
Anthracyclines
Antineoplastic Agents - pharmacology
ATP
ATP-Binding Cassette Transporters - antagonists & inhibitors
Base Sequence
Biology
Biotechnology
Breast cancer
Cancer
Cancer therapies
Cell Line, Tumor
Cytotoxicity
Daunorubicin
Daunorubicin - pharmacology
Deactivation
DNA Primers
Doxorubicin
Doxorubicin - pharmacology
Drug resistance
Drug therapy
Efflux
Flow Cytometry
Gene expression
Glucose metabolism
Glycolysis
Glycoproteins
Humans
Inactivation
Inhibition
Kinases
Laboratory animals
Leukemia
Liver cancer
Medicine
Metabolism
Mitochondria
Mitoxantrone
Mitoxantrone - pharmacology
Pharmaceutical sciences
Real-Time Polymerase Chain Reaction
Sensitivity
Stem cells
Tumors
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Title Glycolysis Inhibition Inactivates ABC Transporters to Restore Drug Sensitivity in Malignant Cells
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