Cited by 801Autophagy in Disease and TherapyCalcium signaling and nucleotide metabolismCancer, Hypoxia, and Metabolism

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Transcriptional control of autophagy-lysosome function drives pancreatic cancer metabolism

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Perera, Rushika M., Stoykova, Svetlana, Nicolay, Brandon N., Ross, Kenneth N., Fitamant, Julien, Boukhali, Myriam, Lengrand, Justine, Deshpande, Vikram, Selig, Martin K., Ferrone, Cristina R., Settleman, Jeff, Stephanopoulos, Gregory, Dyson, Nicholas J., Zoncu, Roberto, Ramaswamy, Sridhar, Haas, Wilhelm, Bardeesy, Nabeel·2015·Nature

DOI 10.1038/nature14587PMC PMC5086585

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Abstract

Activation of cellular stress response pathways to maintain metabolic homeostasis is emerging as a critical growth and survival mechanism in many cancers. The pathogenesis of pancreatic ductal adenocarcinoma (PDA) requires high levels of autophagy, a conserved self-degradative process. However, the regulatory circuits that activate autophagy and reprogram PDA cell metabolism are unknown. Here we show that autophagy induction in PDA occurs as part of a broader transcriptional program that coordinates activation of lysosome biogenesis and function, and nutrient scavenging, mediated by the MiT/TFE family of transcription factors. In human PDA cells, the MiT/TFE proteins--MITF, TFE3 and TFEB--are decoupled from regulatory mechanisms that control their cytoplasmic retention. Increased nuclear import in turn drives the expression of a coherent network of genes that induce high levels of lysosomal catabolic function essential for PDA growth. Unbiased global metabolite profiling reveals that MiT/TFE-dependent autophagy-lysosome activation is specifically required to maintain intracellular amino acid pools. These results identify the MiT/TFE proteins as master regulators of metabolic reprogramming in pancreatic cancer and demonstrate that transcriptional activation of clearance pathways converging on the lysosome is a novel hallmark of aggressive malignancy.

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Commisso, C. et al. Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells. Nature 497, 633–637 (2013) · DOI · Paper page
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Additional file 5 of Genetic assessment of pathogenic germline alterations in lysosomal genes among Asian patients with pancreatic ductal adenocarcinoma
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Additional file 1 of Genetic assessment of pathogenic germline alterations in lysosomal genes among Asian patients with pancreatic ductal adenocarcinoma
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Additional file 2 of Genetic assessment of pathogenic germline alterations in lysosomal genes among Asian patients with pancreatic ductal adenocarcinoma
Koh, Y., Kim, H., Joo, S. Y., Song, S., Choi, Y. H., Kim, H. R., Moon, B., Byun, J., Hong, J., Shin, D.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26627830
Additional file 3 of Paradoxical downregulation of LPAR3 exerts tumor-promoting activity through autophagy induction in Ras-transformed cells
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Additional file 4 of Genetic assessment of pathogenic germline alterations in lysosomal genes among Asian patients with pancreatic ductal adenocarcinoma
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Additional file 3 of Genetic assessment of pathogenic germline alterations in lysosomal genes among Asian patients with pancreatic ductal adenocarcinoma
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Additional file 6 of Genetic assessment of pathogenic germline alterations in lysosomal genes among Asian patients with pancreatic ductal adenocarcinoma
Koh, Y., Kim, H., Joo, S. Y., Song, S., Choi, Y. H., Kim, H. R., Moon, B., Byun, J., Hong, J., Shin, D.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26627842
Additional file 4 of Paradoxical downregulation of LPAR3 exerts tumor-promoting activity through autophagy induction in Ras-transformed cells
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Additional file 1 of Paradoxical downregulation of LPAR3 exerts tumor-promoting activity through autophagy induction in Ras-transformed cells
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Authors: Perera, R. M., Stoykova, S., Nicolay, B. N., Ross, K. N., Fitamant, J., Boukhali, M., Lengrand, J., Deshpande, V., Selig, M. K., Ferrone, C. R., Settleman, J., Stephanopoulos, G., Dyson, N. J., Zoncu, R., Ramaswamy, S., Haas, W., & Bardeesy, N.
Affiliations: Harvard University (US)
Massachusetts General Hospital (US)
Massachusetts Institute of Technology (US)
University of California, Berkeley (US)
Corresponding author: Bardeesy, Nabeel
ORCID: Perera, Rushika M.
Nicolay, Brandon N.
Ross, Kenneth N.
Boukhali, Myriam
Deshpande, Vikram
Selig, Martin K.
Ferrone, Cristina R.
Stephanopoulos, Gregory
Dyson, Nicholas J.
Zoncu, Roberto
Haas, Wilhelm
Bardeesy, Nabeel
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2015-07-13
Volume: 524
Issue: 7565
Pages: 361-365
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature14587
PMC: PMC5086585
OpenAlex: W1678795445
Cited by: 799
References: 49
Citations by year: 2026: 42 · 2025: 59 · 2024: 64 · 2023: 62 · 2022: 84 · 2021: 107 · 2020: 85 · 2019: 76 · 2018: 77 · 2017: 65 · 2016: 63 · 2015: 13
FWCI: 57.07
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
PMC
Funders: Hirshberg Foundation for Pancreatic Cancer Research
National Institutes of Health (P50CA1270003)
National Cancer Institute (P50CA127003, P50CA1270003, R01CA133557, DP2CA195761, P01CA117969)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: autophagy, lysosomal biogenesis, pancreatic ductal adenocarcinoma, cancer metabolism, metabolic reprogramming, TFEB, TFE3, MITF, nuclear import, amino acid metabolism, cellular stress response, lysosomal catabolism
MeSH terms: Amino Acids, Animals, Autophagy, Energy Metabolism, Female, Homeostasis, Humans, Lysosomes, Neoplasm Transplantation, Pancreatic Neoplasms, Transcription Factors, Transcription, Genetic, Gene Expression Regulation, Neoplastic, Carcinoma, Pancreatic Ductal, Active Transport, Cell Nucleus, Cell Line, Tumor, Mice, Microphthalmia-Associated Transcription Factor, Basic Helix-Loop-Helix Leucine Zipper Transcription Factors, Heterografts

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