Coordinated transcriptional and catabolic programs support iron-dependent adaptation to RAS-MAPK pathway inhibition in pancreatic cancer
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Abstract
The mechanisms underlying metabolic adaptation of pancreatic ductal adenocarcinoma (PDA) cells to pharmacologic inhibition of RAS–MAPK signaling are largely unknown. Using transcriptome and chromatin immunoprecipitation profiling of PDA cells treated with the MEK inhibitor (MEKi) trametinib, we identify transcriptional antagonism between c-MYC and the master transcription factors for lysosome gene expression, the MiT/TFE proteins. Under baseline conditions, c-MYC and MiT/TFE factors compete for binding to lysosome gene promoters to fine-tune gene expression. Treatment of PDA cells or patient organoids with MEKi leads to c-MYC downregulation and increased MiT/TFE-dependent lysosome biogenesis. Quantitative proteomics of immunopurified lysosomes uncovered reliance on ferritinophagy, the selective degradation of the iron storage complex ferritin, in MEKi-treated cells. Ferritinophagy promotes mitochondrial iron–sulfur cluster protein synthesis and enhanced mitochondrial respiration. Accordingly, suppressing iron utilization sensitizes PDA cells to MEKi, highlighting a critical and targetable reliance on lysosome-dependent iron supply during adaptation to KRAS–MAPK inhibition. Significance: Reduced c-MYC levels following MAPK pathway suppression facilitate the upregulation of autophagy and lysosome biogenesis. Increased autophagy–lysosome activity is required for increased ferritinophagy-mediated iron supply, which supports mitochondrial respiration under therapy stress. Disruption of ferritinophagy synergizes with KRAS–MAPK inhibition and blocks PDA growth, thus highlighting a key targetable metabolic dependency. See related commentary by Jain and Amaravadi, p. 2023. See related article by Santana-Codina et al., p. 2180. This article is highlighted in the In This Issue feature, p. 2007
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Increased NCOA4 accelerates tumorigenesis in mice, and genetic ablation delays tumor growth that is eventually overcome by compensatory iron acquisition pathways.
“Increased expression of NCOA4 accelerates tumorigenesis in mice, and genetic ablation leads to delayed tumor growth that is eventually overcome through development of compensatory iron acquisition pathways216”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [216]
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Self-citationConcomitant Targeting of MDM2 and MEK: A New Translatable Combinatorial Strategy?
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Ferritinophagy is a Druggable Vulnerability of Quiescent Leukemic Stem CellsPreprint
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- Authors
- Ravichandran, M., Hu, J., Cai, C., Ward, N. P., Venida, A., Foakes, C., Kuljanin, M., Yang, A., Hennessey, C. J., Yang, Y., Desousa, B. R., Rademaker, G., Staes, A. A. L., Cakir, Z., Jain, I. H., Aguirre, A. J., Mancias, J. D., Shen, Y., DeNicola, G. M., & Perera, R. M.
- Affiliations
- University of California, San Francisco (US)
- Moffitt Cancer Center (US)
- Dana-Farber Cancer Institute (US)
- Gladstone Institutes (US)
- Broad Institute (US)
- Corresponding author
- Perera, Rushika M.
- ORCID
- Ravichandran, Mirunalini
- Hu, Jingjie
- Cai, Charles
- Ward, Nathan P.
- Venida, Anthony
- Foakes, Callum
- Kuljanin, Miljan
- Yang, Annan
- Hennessey, Connor J.
- Yang, Yang
- Desousa, Brandon R.
- Rademaker, Gilles
- Staes, Annelot A.L.
- Cakir, Zeynep
- Jain, Isha H.
- Aguirre, Andrew J.
- Mancias, Joseph D.
- Shen, Yin
- DeNicola, Gina M.
- Perera, Rushika M.
- Venue
- Cancer Discovery
- Published
- 2022-06-30
- Volume
- 12
- Issue
- 9
- Pages
- 2198-2219
- ISSN
- 2159-8274 (ISSN-L)
- 2159-8290
- PMC
- PMC9444964
- OpenAlex
- W4283739590
- Cited by
- 80
- References
- 77
- Citations by year
- 2026: 15 · 2025: 21 · 2024: 14 · 2023: 26 · 2022: 4
- FWCI
- 11.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cancer Discovery (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- ORBi (University of Liège) (submittedVersion)
- Funders
- NCI (R01CA240603, R01CA260249, R37CA230042)
- NIH Director’s New Innovator Award (DP2CA216364)
- NIH NCI (K08 CA21842002, P50CA127003)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- pancreatic ductal adenocarcinoma, trametinib, MEK inhibitors, c-Myc, lysosomal biogenesis, autophagy, ferritinophagy, iron metabolism, mitochondrial respiration, metabolic adaptation, KRAS
- MeSH terms
- Biological Availability, Humans, Iron, Iron-Sulfur Proteins, Pancreatic Neoplasms, Sulfur, Transcription Factors, Proto-Oncogene Proteins p21(ras), Carcinoma, Pancreatic Ductal, Protein Kinase Inhibitors, Nuclear Receptor Coactivators
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