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 in | PloS one Vol. 6; no. 11; p. e27222 |
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Main Authors | , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
02.11.2011
Public Library of Science (PLoS) |
Subjects | |
Online Access | Get full text |
ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/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. |
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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 |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22073292$$D View this record in MEDLINE/PubMed |
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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 |
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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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