Cited by 326Cancer, Lipids, and MetabolismPancreatic and Hepatic Oncology ResearchCancer, Hypoxia, and Metabolism

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Acetyl-CoA Metabolism Supports Multistep Pancreatic Tumorigenesis

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Carrer, Alessandro, Trefely, Sophie, Zhao, Steven, Campbell, Sydney L., Norgard, Robert J., Schultz, Kollin C., Sidoli, Simone, Parris, Joshua L.D., Affronti, Hayley C., Sivanand, Sharanya, Egolf, Shaun, Sela, Yogev, Trizzino, Marco, Gardini, Alessandro, Garcia, Benjamin A., Snyder, Nathaniel W., Stanger, Ben Z., Wellen, Kathryn E.·2019·Cancer Discovery

DOI 10.1158/2159-8290.cd-18-0567PMC PMC6643997

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Abstract

Pancreatic ductal adenocarcinoma (PDA) has a poor prognosis, and new strategies for prevention and treatment are urgently needed. We previously reported that histone H4 acetylation is elevated in pancreatic acinar cells harboring Kras mutations prior to the appearance of premalignant lesions. Because acetyl-CoA abundance regulates global histone acetylation, we hypothesized that altered acetyl-CoA metabolism might contribute to metabolic or epigenetic alterations that promote tumorigenesis. We found that acetyl-CoA abundance is elevated in KRAS-mutant acinar cells and that its use in the mevalonate pathway supports acinar-to-ductal metaplasia (ADM). Pancreas-specific loss of the acetyl-CoA–producing enzyme ATP-citrate lyase (ACLY) accordingly suppresses ADM and tumor formation. In PDA cells, growth factors promote AKT–ACLY signaling and histone acetylation, and both cell proliferation and tumor growth can be suppressed by concurrent BET inhibition and statin treatment. Thus, KRAS-driven metabolic alterations promote acinar cell plasticity and tumor development, and targeting acetyl-CoA–dependent processes exerts anticancer effects. Significance: Pancreatic cancer is among the deadliest of human malignancies. We identify a key role for the metabolic enzyme ACLY, which produces acetyl-CoA, in pancreatic carcinogenesis. The data suggest that acetyl-CoA use for histone acetylation and in the mevalonate pathway facilitates cell plasticity and proliferation, suggesting potential to target these pathways. See related commentary by Halbrook et al., p. 326. This article is highlighted in the In This Issue feature, p. 305

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Additional file 9 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 6 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 7 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 2 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 3 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 5 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 1 of Epigenetic reprogramming-induced guanidinoacetic acid synthesis promotes pancreatic cancer metastasis and transcription-activating histone modifications
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Additional file 3 of Comprehensive analysis of bulk and single-cell transcriptomic data reveals a novel signature associated with endoplasmic reticulum stress, lipid metabolism, and liver metastasis in pancreatic cancer
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Additional file 2 of Comprehensive analysis of bulk and single-cell transcriptomic data reveals a novel signature associated with endoplasmic reticulum stress, lipid metabolism, and liver metastasis in pancreatic cancer
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Additional file 5 of Comprehensive analysis of bulk and single-cell transcriptomic data reveals a novel signature associated with endoplasmic reticulum stress, lipid metabolism, and liver metastasis in pancreatic cancer
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Additional file 1 of Comprehensive analysis of bulk and single-cell transcriptomic data reveals a novel signature associated with endoplasmic reticulum stress, lipid metabolism, and liver metastasis in pancreatic cancer
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Additional file 1 of BCAA metabolism in pancreatic cancer affects lipid balance by regulating fatty acid import into mitochondria
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Additional file 1 of EMID2 is a novel biotherapeutic for aggressive cancers identified by in vivo screening
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Authors: Carrer, A., Trefely, S., Zhao, S., Campbell, S. L., Norgard, R. J., Schultz, K. C., Sidoli, S., Parris, J. L. D., Affronti, H. C., Sivanand, S., Egolf, S., Sela, Y., Trizzino, M., Gardini, A., Garcia, B. A., Snyder, N. W., Stanger, B. Z., & Wellen, K. E.
Affiliations: University of Pennsylvania (US)
Drexel University (US)
The Wistar Institute (US)
Corresponding author: Wellen, Kathryn E.
ORCID: Carrer, Alessandro
Trefely, Sophie
Zhao, Steven
Campbell, Sydney L.
Norgard, Robert J.
Schultz, Kollin C.
Sidoli, Simone
Parris, Joshua L.D.
Affronti, Hayley C.
Sivanand, Sharanya
Egolf, Shaun
Trizzino, Marco
Gardini, Alessandro
Garcia, Benjamin A.
Snyder, Nathaniel W.
Stanger, Ben Z.
Wellen, Kathryn E.
Venue: Cancer Discovery
Publisher: American Association for Cancer Research (AACR)
Published: 2019-03-01
Volume: 9
Issue: 3
Pages: 416-435
ISSN: 2159-8274 (ISSN-L)
2159-8290
DOI: 10.1158/2159-8290.cd-18-0567
PMC: PMC6643997
OpenAlex: W2911157836
Cited by: 313
References: 76
Citations by year: 2026: 23 · 2025: 49 · 2024: 62 · 2023: 47 · 2022: 44 · 2021: 42 · 2020: 31 · 2019: 15
FWCI: 10.44
Type: journal article
Language: en
Update notices: correction (2024-09-04)
Open access: green
www.ncbi.nlm.nih.gov
Locations: Cancer Discovery (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Padua Research Archive (University of Padova) (submittedVersion)
Funders: Pancreatic Cancer Action Network (14-20-25-WELL)
NIH (R01CA174761, R01CA228339, R03HD092630, GM110174, AI118891, CA196539, 1F31CA217070-01, F99CA222741, 4K00CA212455-03)
American Diabetes Association (#1-18-PDF-144)
UPenn Baccalaureate Research Education (R25-GM071745)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: acetyl-CoA metabolism, pancreatic ductal adenocarcinoma, pancreatic carcinogenesis, ATP citrate lyase, histone H4 acetylation, acinar-to-ductal metaplasia, KRAS mutation, mevalonate pathway, Akt signaling, BET inhibition, statins, cellular plasticity, epigenetic regulation, pancreatic acinar cells
MeSH terms: Acetyl Coenzyme A, Acetylation, Animals, Female, Histones, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Mutation, Pancreatic Neoplasms, Protein Processing, Post-Translational, Genes, ras, Signal Transduction, Mice, Knockout, Carcinoma, Pancreatic Ductal, Cell Proliferation, Acinar Cells, Carcinogenesis, Heterografts

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Acetyl-CoA Metabolism Supports Multistep Pancreatic Tumorigenesis

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