Cited by 125Cancer Cells and MetastasisAngiogenesis and VEGF in CancerCancer, Lipids, and Metabolism

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Oncogenic KRAS Drives Lipofibrogenesis to Promote Angiogenesis and Colon Cancer Progression

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Hsu, Wen-Hao, LaBella, Kyle A., Lin, Yiyun, Xu, Ping, Lee, Rumi, Hsieh, Cheng-En, Yang, Lei, Zhou, Ashley, Blecher, Jonathan M., Wu, Chang-Jiun, Lin, Kangyu, Shang, Xiaoying, Jiang, Shan, Spring, Denise J., Xia, Yan, Chen, Peiwen, Shen, John Paul, Kopetz, Scott, DePinho, Ronald A.·2023·Cancer Discovery

DOI 10.1158/2159-8290.cd-22-1467PMC PMC10807546

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Abstract

Oncogenic KRAS (KRAS*) contributes to many cancer hallmarks. In colorectal cancer, KRAS* suppresses antitumor immunity to promote tumor invasion and metastasis. Here, we uncovered that KRAS* transforms the phenotype of carcinoma-associated fibroblasts (CAF) into lipid-laden CAFs, promoting angiogenesis and tumor progression. Mechanistically, KRAS* activates the transcription factor CP2 (TFCP2) that upregulates the expression of the proadipogenic factors BMP4 and WNT5B, triggering the transformation of CAFs into lipid-rich CAFs. These lipid-rich CAFs, in turn, produce VEGFA to spur angiogenesis. In KRAS*-driven colorectal cancer mouse models, genetic or pharmacologic neutralization of TFCP2 reduced lipid-rich CAFs, lessened tumor angiogenesis, and improved overall survival. Correspondingly, in human colorectal cancer, lipid-rich CAF and TFCP2 signatures correlate with worse prognosis. This work unveils a new role for KRAS* in transforming CAFs, driving tumor angiogenesis and disease progression, providing an actionable therapeutic intervention for KRAS*-driven colorectal cancer. Significance: This study identified a molecular mechanism contributing to KRAS*-driven colorectal cancer progression via fibroblast transformation in the tumor microenvironment to produce VEGFA driving tumor angiogenesis. In preclinical models, targeting the KRAS*–TFCP2–VEGFA axis impaired tumor progression, revealing a potential novel therapeutic option for patients with KRAS*-driven colorectal cancer. This article is featured in Selected Articles from This Issue, p. 2489

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“These lipid-enriched CAFs produce VEGFA, fostering angiogenesis and supporting tumor growth [26].”

See all 125

Authors: Hsu, W.-H., LaBella, K. A., Lin, Y., Xu, P., Lee, R., Hsieh, C.-E., Yang, L., Zhou, A., Blecher, J. M., Wu, C.-J., Lin, K., Shang, X., Jiang, S., Spring, D. J., Xia, Y., Chen, P., Shen, J. P., Kopetz, S., & DePinho, R. A.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
3Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, Texas.
ORCID: Hsu, Wen-Hao
LaBella, Kyle A.
Lin, Yiyun
Xu, Ping
Lee, Rumi
Hsieh, Cheng-En
Yang, Lei
Zhou, Ashley
Blecher, Jonathan M.
Wu, Chang-Jiun
Lin, Kangyu
Shang, Xiaoying
Jiang, Shan
Spring, Denise J.
Xia, Yan
Chen, Peiwen
Shen, John Paul
Kopetz, Scott
DePinho, Ronald A.
Venue: Cancer Discovery
Publisher: American Association for Cancer Research (AACR)
Published: 2023-09-27
Volume: 13
Issue: 12
Pages: 2652-2673
ISSN: 2159-8274 (ISSN-L)
2159-8290
DOI: 10.1158/2159-8290.cd-22-1467
PMC: PMC10807546
OpenAlex: W4387115132
Cited by: 125
References: 81
Citations by year: 2026: 42 · 2025: 53 · 2024: 28 · 2023: 2
FWCI: 15.18
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Cancer Discovery (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Digital Commons-TMC (Texas Medical Center) (submittedVersion)
Funders: Cancer Prevention and Research Institute of Texas (RP210028)
National Institutes of Health (F99 CA274661, R01 CA231360)
Topics: Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
Keywords: oncogenic KRAS, colorectal cancer, cancer-associated fibroblasts, angiogenesis, VEGF-A, TFCP2, BMP4, Wnt5b, tumor microenvironment, tumor progression, antitumor immunity, prognostic signature, KRAS-targeted therapy
MeSH terms: Cancer-Associated Fibroblasts, Angiogenesis, Animals, Colonic Neoplasms, DNA-Binding Proteins, Fibroblasts, Humans, Lipids, Transcription Factors, Colorectal Neoplasms, Proto-Oncogene Proteins p21(ras), Mice, Tumor Microenvironment

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Oncogenic KRAS Drives Lipofibrogenesis to Promote Angiogenesis and Colon Cancer Progression

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