Cited by 131Ovarian cancer diagnosis and treatmentCancer, Hypoxia, and MetabolismCancer Cells and Metastasis

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Collagen Remodeling in the Hypoxic Tumor-Mesothelial Niche Promotes Ovarian Cancer Metastasis

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Natarajan, Suchitra, Foreman, Kaitlyn M., Soriano, Michaela I., Rossen, Ninna S., Shehade, Hussein, Fregoso, Daniel R., Eggold, Joshua T., Krishnan, Venkatesh, Dorigo, Oliver, Krieg, Adam J., Heilshorn, Sarah C., Sinha, Subarna, Fuh, Katherine C., Rankin, Erinn B.·2019·Cancer Research

DOI 10.1158/0008-5472.can-18-2616PMC PMC6822898

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Abstract

Peritoneal metastases are the leading cause of morbidity and mortality in high-grade serous ovarian cancer (HGSOC). Accumulating evidence suggests that mesothelial cells are an important component of the metastatic microenvironment in HGSOC. However, the mechanisms by which mesothelial cells promote metastasis are unclear. Here, we report that the HGSOC tumor-mesothelial niche was hypoxic, and hypoxic signaling enhanced collagen I deposition by mesothelial cells. Specifically, hypoxic signaling increased expression of lysyl oxidase (LOX) in mesothelial and ovarian cancer cells to promote collagen crosslinking and tumor cell invasion. The mesothelial niche was enriched with fibrillar collagen in human and murine omental metastases. Pharmacologic inhibition of LOX reduced tumor burden and collagen remodeling in murine omental metastases. These findings highlight an important role for hypoxia and mesothelial cells in the modification of the extracellular matrix and tumor invasion in HGSOC. Significance: This study identifies HIF/LOX signaling as a potential therapeutic target to inhibit collagen remodeling and tumor progression in HGSOC.

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Authors: Natarajan, S., Foreman, K. M., Soriano, M. I., Rossen, N. S., Shehade, H., Fregoso, D. R., Eggold, J. T., Krishnan, V., Dorigo, O., Krieg, A. J., Heilshorn, S. C., Sinha, S., Fuh, K. C., & Rankin, E. B.
Affiliations: Stanford University (US)
Oregon Health & Science University (US)
SRI International (US)
Washington University in St. Louis (US)
Corresponding author: Rankin, Erinn B.
ORCID: Natarajan, Suchitra
Foreman, Kaitlyn M.
Soriano, Michaela I.
Rossen, Ninna S.
Shehade, Hussein
Fregoso, Daniel R.
Eggold, Joshua T.
Krishnan, Venkatesh
Dorigo, Oliver
Krieg, Adam J.
Heilshorn, Sarah C.
Fuh, Katherine C.
Rankin, Erinn B.
Venue: Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2019-05-01
Volume: 79
Issue: 9
Pages: 2271-2284
ISSN: 0008-5472 (ISSN-L)
1538-7445
DOI: 10.1158/0008-5472.can-18-2616
PMC: PMC6822898
OpenAlex: W2921266140
Cited by: 129
References: 54
Citations by year: 2026: 11 · 2025: 18 · 2024: 15 · 2023: 18 · 2022: 20 · 2021: 20 · 2020: 24 · 2019: 3
FWCI: 16.26
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Cancer Research (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Defense for Health Affairs (W81XWH-15-1-0097)
Topics: Health Sciences › Medicine › Oncology › Ovarian cancer diagnosis and treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: high-grade serous ovarian cancer, peritoneal carcinomatosis, mesothelial cells, hypoxia, collagen remodeling, collagen I deposition, lysyl oxidase, collagen cross-linking, extracellular matrix, tumor invasion, HIF signaling, omental metastases, therapeutic target
MeSH terms: Endothelial PAS Domain-Containing Protein 1, Adult, Aged, Aged, 80 and over, Animals, Hypoxia, Collagen, Epithelium, Extracellular Matrix, Female, Humans, Protein-Lysine 6-Oxidase, Middle Aged, Ovarian Neoplasms, Peritoneal Neoplasms, Prognosis, Tumor Cells, Cultured, Signal Transduction, Gene Expression Regulation, Neoplastic, Mice, SCID, Mice, Inbred NOD, Apoptosis, Cystadenocarcinoma, Serous, Xenograft Model Antitumor Assays, Cell Proliferation, Mice, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit, Tumor Microenvironment

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Collagen Remodeling in the Hypoxic Tumor-Mesothelial Niche Promotes Ovarian Cancer Metastasis

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