Autophagy is required for PDAC glutamine metabolism
Macroautophagy (autophagy) is believed to maintain energy homeostasis by degrading unnecessary cellular components and molecules. Its implication in regulating cancer metabolism recently started to be uncovered. However, the precise roles of autophagy in cancer metabolism are still unclear. Here, we...
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Published in | Scientific reports Vol. 6; no. 1; p. 37594 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Nature Publishing Group UK
28.11.2016
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Abstract | Macroautophagy (autophagy) is believed to maintain energy homeostasis by degrading unnecessary cellular components and molecules. Its implication in regulating cancer metabolism recently started to be uncovered. However, the precise roles of autophagy in cancer metabolism are still unclear. Here, we show that autophagy plays a critical role in glutamine metabolism, which is required for tumor survival. Pancreatic ductal adenocarcinoma (PDAC) cells require both autophagy and typical glutamine transporters to maintain intracellular glutamine levels. Glutamine deprivation, but not that of glucose, led to the activation of macropinocytosis-associated autophagy through TFEB induction and translocation into the nucleus. In contrast, glutamine uptake increased as a compensatory response to decreased intracellular glutamine levels upon autophagy inhibition. Moreover, autophagy inhibition and glutamine deprivation did not induce cell death, while glutamine deprivation dramatically activated apoptotic cell death upon autophagy inhibition. Interestingly, the addition of α-ketoglutarate significantly rescued the apoptotic cell death caused by the combination of the inhibition of autophagy with glutamine deprivation. Our data suggest that macropinocytosis-associated autophagy is a critical process providing glutamine for anaplerosis of the TCA cycle in PDAC. Thus, targeting both autophagy and glutamine metabolism to completely block glutamine supply may provide new therapeutic approaches to treat refractory tumors. |
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AbstractList | Macroautophagy (autophagy) is believed to maintain energy homeostasis by degrading unnecessary cellular components and molecules. Its implication in regulating cancer metabolism recently started to be uncovered. However, the precise roles of autophagy in cancer metabolism are still unclear. Here, we show that autophagy plays a critical role in glutamine metabolism, which is required for tumor survival. Pancreatic ductal adenocarcinoma (PDAC) cells require both autophagy and typical glutamine transporters to maintain intracellular glutamine levels. Glutamine deprivation, but not that of glucose, led to the activation of macropinocytosis-associated autophagy through TFEB induction and translocation into the nucleus. In contrast, glutamine uptake increased as a compensatory response to decreased intracellular glutamine levels upon autophagy inhibition. Moreover, autophagy inhibition and glutamine deprivation did not induce cell death, while glutamine deprivation dramatically activated apoptotic cell death upon autophagy inhibition. Interestingly, the addition of α-ketoglutarate significantly rescued the apoptotic cell death caused by the combination of the inhibition of autophagy with glutamine deprivation. Our data suggest that macropinocytosis-associated autophagy is a critical process providing glutamine for anaplerosis of the TCA cycle in PDAC. Thus, targeting both autophagy and glutamine metabolism to completely block glutamine supply may provide new therapeutic approaches to treat refractory tumors. Abstract Macroautophagy (autophagy) is believed to maintain energy homeostasis by degrading unnecessary cellular components and molecules. Its implication in regulating cancer metabolism recently started to be uncovered. However, the precise roles of autophagy in cancer metabolism are still unclear. Here, we show that autophagy plays a critical role in glutamine metabolism, which is required for tumor survival. Pancreatic ductal adenocarcinoma (PDAC) cells require both autophagy and typical glutamine transporters to maintain intracellular glutamine levels. Glutamine deprivation, but not that of glucose, led to the activation of macropinocytosis-associated autophagy through TFEB induction and translocation into the nucleus. In contrast, glutamine uptake increased as a compensatory response to decreased intracellular glutamine levels upon autophagy inhibition. Moreover, autophagy inhibition and glutamine deprivation did not induce cell death, while glutamine deprivation dramatically activated apoptotic cell death upon autophagy inhibition. Interestingly, the addition of α-ketoglutarate significantly rescued the apoptotic cell death caused by the combination of the inhibition of autophagy with glutamine deprivation. Our data suggest that macropinocytosis-associated autophagy is a critical process providing glutamine for anaplerosis of the TCA cycle in PDAC. Thus, targeting both autophagy and glutamine metabolism to completely block glutamine supply may provide new therapeutic approaches to treat refractory tumors. |
ArticleNumber | 37594 |
Author | Lee, So-Yeon Cheong, Heesun Choi, Jungwon Seo, Ju-Won Kang, Min-Ji Son, Jaekyoung Sung, Suhyun Yoo, Hyun Ju |
Author_xml | – sequence: 1 givenname: Ju-Won surname: Seo fullname: Seo, Ju-Won organization: Department of Biomedical Sciences, University of Ulsan College of Medicine – sequence: 2 givenname: Jungwon surname: Choi fullname: Choi, Jungwon organization: Division of Cancer Biology, Comparative Biomedicine Research Branch, National Cancer Center – sequence: 3 givenname: So-Yeon surname: Lee fullname: Lee, So-Yeon organization: Department of Biomedical Sciences, University of Ulsan College of Medicine – sequence: 4 givenname: Suhyun surname: Sung fullname: Sung, Suhyun organization: Division of Cancer Biology, Comparative Biomedicine Research Branch, National Cancer Center – sequence: 5 givenname: Hyun Ju surname: Yoo fullname: Yoo, Hyun Ju organization: Department of Convergence medicine, Biomedical research center, Asan Institute for Life Sciences, Asan Medical Center – sequence: 6 givenname: Min-Ji surname: Kang fullname: Kang, Min-Ji organization: Department of Biomedical Sciences, University of Ulsan College of Medicine – sequence: 7 givenname: Heesun surname: Cheong fullname: Cheong, Heesun organization: Division of Cancer Biology, Comparative Biomedicine Research Branch, National Cancer Center, Graduate School of Cancer Science & Policy, National Cancer Center – sequence: 8 givenname: Jaekyoung surname: Son fullname: Son, Jaekyoung organization: Department of Biomedical Sciences, University of Ulsan College of Medicine, Asan Institute for Life Sciences, Asan Medical Center, College of Medicine, University of Ulsan |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27892481$$D View this record in MEDLINE/PubMed |
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Snippet | Macroautophagy (autophagy) is believed to maintain energy homeostasis by degrading unnecessary cellular components and molecules. Its implication in regulating... Abstract Macroautophagy (autophagy) is believed to maintain energy homeostasis by degrading unnecessary cellular components and molecules. Its implication in... |
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SubjectTerms | 13/2 13/89 631/67/2327 631/80/82/39/2346 96/1 Adenocarcinoma Apoptosis Autophagy Cell death Energy balance Glutamine Homeostasis Humanities and Social Sciences Intracellular Ketoglutaric acid Metabolism multidisciplinary Pancreas Pancreatic cancer Phagocytosis Science Tricarboxylic acid cycle Tumors |
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Title | Autophagy is required for PDAC glutamine metabolism |
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