Collagen Remodeling in the Hypoxic Tumor-Mesothelial Niche Promotes Ovarian Cancer Metastasis
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...
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| Veröffentlicht in: | Cancer research (Chicago, Ill.) Ill.), 2019-05, Vol.79 (9), p.2271-2284 |
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| creator | 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 |
| description | 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.
http://cancerres.aacrjournals.org/content/canres/79/9/2271/F1.large.jpg. |
| doi_str_mv | 10.1158/0008-5472.CAN-18-2616 |
| format | Article |
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http://cancerres.aacrjournals.org/content/canres/79/9/2271/F1.large.jpg.</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Cell Proliferation</subject><subject>Collagen - metabolism</subject><subject>Cystadenocarcinoma, Serous - genetics</subject><subject>Cystadenocarcinoma, Serous - metabolism</subject><subject>Cystadenocarcinoma, Serous - secondary</subject><subject>Epithelium - physiopathology</subject><subject>Extracellular Matrix - metabolism</subject><subject>Female</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Humans</subject><subject>Hypoxia - physiopathology</subject><subject>Hypoxia-Inducible Factor 1, alpha Subunit - genetics</subject><subject>Hypoxia-Inducible Factor 1, alpha Subunit - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred NOD</subject><subject>Mice, SCID</subject><subject>Middle Aged</subject><subject>Ovarian Neoplasms - genetics</subject><subject>Ovarian Neoplasms - metabolism</subject><subject>Ovarian Neoplasms - pathology</subject><subject>Peritoneal Neoplasms - genetics</subject><subject>Peritoneal Neoplasms - metabolism</subject><subject>Peritoneal Neoplasms - secondary</subject><subject>Prognosis</subject><subject>Protein-Lysine 6-Oxidase - genetics</subject><subject>Protein-Lysine 6-Oxidase - metabolism</subject><subject>Signal Transduction</subject><subject>Tumor Cells, Cultured</subject><subject>Tumor Microenvironment</subject><subject>Xenograft Model Antitumor Assays</subject><issn>0008-5472</issn><issn>1538-7445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUd9LwzAQDqLonP4JSh59qebSpk1fBCn-gjlF5qOEtL1ukbaZSSf635vhHAoHx919993xfYScADsHEPKCMSYjkWT8vLiaRiAjnkK6Q0YgYhllSSJ2yWiLOSCH3r-FUgAT--QgZjLlGWQj8lrYttVz7OkzdrbG1vRzano6LJDefS3tp6nobNVZFz2gt6HbGt3SqanC_MnZzg7o6eOHdkb3tNB9hY4-4KB9COOPyF6jW4_HmzwmLzfXs-Iumjze3hdXk6gSPB8iHpeQ56WE8BQDrTPgEjljcS1LKJsERQMYs6RkKFNZVjrXJYgmEVmd13FSx2Ny-cO7XJUd1hX2g9OtWjrTafelrDbq_6Q3CzW3HyqVnMtcBoKzDYGz7yv0g-qMrzBI06NdecUhhyBmKkWAih9o5az3DpvtGWBqbY1ay67WsqtgjQKp1taEvdO_P263fr2IvwH-zIvB</recordid><startdate>20190501</startdate><enddate>20190501</enddate><creator>Natarajan, Suchitra</creator><creator>Foreman, Kaitlyn M</creator><creator>Soriano, Michaela I</creator><creator>Rossen, Ninna S</creator><creator>Shehade, Hussein</creator><creator>Fregoso, Daniel R</creator><creator>Eggold, Joshua T</creator><creator>Krishnan, Venkatesh</creator><creator>Dorigo, Oliver</creator><creator>Krieg, Adam J</creator><creator>Heilshorn, Sarah C</creator><creator>Sinha, Subarna</creator><creator>Fuh, Katherine C</creator><creator>Rankin, Erinn B</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0689-4848</orcidid><orcidid>https://orcid.org/0000-0002-3069-0378</orcidid><orcidid>https://orcid.org/0000-0001-5173-0773</orcidid></search><sort><creationdate>20190501</creationdate><title>Collagen Remodeling in the Hypoxic Tumor-Mesothelial Niche Promotes Ovarian Cancer Metastasis</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c529t-23b199b8162701aa7128e2003d8b1bf4e5f1e304b0e868bca9ab15f457d9d34d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Cell Proliferation</topic><topic>Collagen - metabolism</topic><topic>Cystadenocarcinoma, Serous - genetics</topic><topic>Cystadenocarcinoma, Serous - metabolism</topic><topic>Cystadenocarcinoma, Serous - secondary</topic><topic>Epithelium - physiopathology</topic><topic>Extracellular Matrix - metabolism</topic><topic>Female</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Humans</topic><topic>Hypoxia - physiopathology</topic><topic>Hypoxia-Inducible Factor 1, alpha Subunit - genetics</topic><topic>Hypoxia-Inducible Factor 1, alpha Subunit - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred NOD</topic><topic>Mice, SCID</topic><topic>Middle Aged</topic><topic>Ovarian Neoplasms - genetics</topic><topic>Ovarian Neoplasms - metabolism</topic><topic>Ovarian Neoplasms - pathology</topic><topic>Peritoneal Neoplasms - genetics</topic><topic>Peritoneal Neoplasms - metabolism</topic><topic>Peritoneal Neoplasms - secondary</topic><topic>Prognosis</topic><topic>Protein-Lysine 6-Oxidase - genetics</topic><topic>Protein-Lysine 6-Oxidase - metabolism</topic><topic>Signal Transduction</topic><topic>Tumor Cells, Cultured</topic><topic>Tumor Microenvironment</topic><topic>Xenograft Model Antitumor Assays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Natarajan, Suchitra</creatorcontrib><creatorcontrib>Foreman, Kaitlyn M</creatorcontrib><creatorcontrib>Soriano, Michaela I</creatorcontrib><creatorcontrib>Rossen, Ninna S</creatorcontrib><creatorcontrib>Shehade, Hussein</creatorcontrib><creatorcontrib>Fregoso, Daniel R</creatorcontrib><creatorcontrib>Eggold, Joshua T</creatorcontrib><creatorcontrib>Krishnan, Venkatesh</creatorcontrib><creatorcontrib>Dorigo, Oliver</creatorcontrib><creatorcontrib>Krieg, Adam J</creatorcontrib><creatorcontrib>Heilshorn, Sarah C</creatorcontrib><creatorcontrib>Sinha, Subarna</creatorcontrib><creatorcontrib>Fuh, Katherine C</creatorcontrib><creatorcontrib>Rankin, Erinn B</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cancer research (Chicago, Ill.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Natarajan, Suchitra</au><au>Foreman, Kaitlyn M</au><au>Soriano, Michaela I</au><au>Rossen, Ninna S</au><au>Shehade, Hussein</au><au>Fregoso, Daniel R</au><au>Eggold, Joshua T</au><au>Krishnan, Venkatesh</au><au>Dorigo, Oliver</au><au>Krieg, Adam J</au><au>Heilshorn, Sarah C</au><au>Sinha, Subarna</au><au>Fuh, Katherine C</au><au>Rankin, Erinn B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Collagen Remodeling in the Hypoxic Tumor-Mesothelial Niche Promotes Ovarian Cancer Metastasis</atitle><jtitle>Cancer research (Chicago, Ill.)</jtitle><addtitle>Cancer Res</addtitle><date>2019-05-01</date><risdate>2019</risdate><volume>79</volume><issue>9</issue><spage>2271</spage><epage>2284</epage><pages>2271-2284</pages><issn>0008-5472</issn><eissn>1538-7445</eissn><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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| subjects | Adult Aged Aged, 80 and over Animals Apoptosis Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Cell Proliferation Collagen - metabolism Cystadenocarcinoma, Serous - genetics Cystadenocarcinoma, Serous - metabolism Cystadenocarcinoma, Serous - secondary Epithelium - physiopathology Extracellular Matrix - metabolism Female Gene Expression Regulation, Neoplastic Humans Hypoxia - physiopathology Hypoxia-Inducible Factor 1, alpha Subunit - genetics Hypoxia-Inducible Factor 1, alpha Subunit - metabolism Mice Mice, Inbred NOD Mice, SCID Middle Aged Ovarian Neoplasms - genetics Ovarian Neoplasms - metabolism Ovarian Neoplasms - pathology Peritoneal Neoplasms - genetics Peritoneal Neoplasms - metabolism Peritoneal Neoplasms - secondary Prognosis Protein-Lysine 6-Oxidase - genetics Protein-Lysine 6-Oxidase - metabolism Signal Transduction Tumor Cells, Cultured Tumor Microenvironment Xenograft Model Antitumor Assays |
| title | Collagen Remodeling in the Hypoxic Tumor-Mesothelial Niche Promotes Ovarian Cancer Metastasis |
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