Fibrillar extracellular matrix produced by pericyte‐like cells facilitates glioma cell dissemination
Gliomagenesis induces profound changes in the composition of the extracellular matrix (ECM) of the brain. In this study, we identified a cellular population responsible for the increased deposition of collagen I and fibronectin in glioblastoma. Elevated levels of the fibrillar proteins collagen I an...
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| Veröffentlicht in: | Brain pathology (Zurich, Switzerland) Switzerland), 2024-11, Vol.34 (6), p.e13265-n/a |
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| creator | Vymola, Petr Garcia‐Borja, Elena Cervenka, Jakub Balaziova, Eva Vymolova, Barbora Veprkova, Jana Vodicka, Petr Skalnikova, Helena Tomas, Robert Netuka, David Busek, Petr Sedo, Aleksi |
| description | Gliomagenesis induces profound changes in the composition of the extracellular matrix (ECM) of the brain. In this study, we identified a cellular population responsible for the increased deposition of collagen I and fibronectin in glioblastoma. Elevated levels of the fibrillar proteins collagen I and fibronectin were associated with the expression of fibroblast activation protein (FAP), which is predominantly found in pericyte‐like cells in glioblastoma. FAP+ pericyte‐like cells were present in regions rich in collagen I and fibronectin in biopsy material and produced substantially more collagen I and fibronectin in vitro compared to other cell types found in the GBM microenvironment. Using mass spectrometry, we demonstrated that 3D matrices produced by FAP+ pericyte‐like cells are rich in collagen I and fibronectin and contain several basement membrane proteins. This expression pattern differed markedly from glioma cells. Finally, we have shown that ECM produced by FAP+ pericyte‐like cells enhances the migration of glioma cells including glioma stem‐like cells, promotes their adhesion, and activates focal adhesion kinase (FAK) signaling. Taken together, our findings establish FAP+ pericyte‐like cells as crucial producers of a complex ECM rich in collagen I and fibronectin, facilitating the dissemination of glioma cells through FAK activation.
FAP+ pericyte‐like cells drive the deposition of fibrillar extracellular matrix proteins such as collagen I and fibronectin in glioblastoma, facilitating glioma cell dissemination and activation of focal adhesion kinase. |
| doi_str_mv | 10.1111/bpa.13265 |
| format | Article |
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FAP+ pericyte‐like cells drive the deposition of fibrillar extracellular matrix proteins such as collagen I and fibronectin in glioblastoma, facilitating glioma cell dissemination and activation of focal adhesion kinase.</description><identifier>ISSN: 1015-6305</identifier><identifier>ISSN: 1750-3639</identifier><identifier>EISSN: 1750-3639</identifier><identifier>DOI: 10.1111/bpa.13265</identifier><identifier>PMID: 38705944</identifier><language>eng</language><publisher>Switzerland: John Wiley & Sons, Inc</publisher><subject>Adhesion ; Basement membranes ; Biopsy ; Brain Neoplasms - metabolism ; Brain Neoplasms - pathology ; Cell activation ; Cell Line, Tumor ; Cell migration ; Cell Movement - physiology ; Collagen ; collagen type I ; Collagen Type I - metabolism ; Endopeptidases ; Extracellular matrix ; Extracellular Matrix - metabolism ; Extracellular Matrix - pathology ; extracellular matrix proteins ; Fibroblast activation protein ; Fibronectin ; Fibronectins - metabolism ; Focal adhesion kinase ; Gelatinases - metabolism ; Glioblastoma ; Glioblastoma - metabolism ; Glioblastoma - pathology ; Glioma ; Glioma - metabolism ; Glioma - pathology ; Glioma cells ; Humans ; Kinases ; Mass spectrometry ; Mass spectroscopy ; Membrane proteins ; Membrane Proteins - metabolism ; Microenvironments ; pericytes ; Pericytes - metabolism ; Pericytes - pathology ; Population studies ; Proteins ; proteomics ; Serine Endopeptidases - metabolism ; Tumor Microenvironment - physiology</subject><ispartof>Brain pathology (Zurich, Switzerland), 2024-11, Vol.34 (6), p.e13265-n/a</ispartof><rights>2024 The Authors. published by John Wiley & Sons Ltd on behalf of International Society of Neuropathology.</rights><rights>2024 The Authors. Brain Pathology published by John Wiley & Sons Ltd on behalf of International Society of Neuropathology.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4045-550af938b5681d617c022e12221de20b7ed49de45a7c12427d813f6d88b993e43</cites><orcidid>0000-0002-9947-2045 ; 0000-0002-6605-9158 ; 0000-0001-6863-0496 ; 0000-0002-5267-2920 ; 0000-0001-8609-4789 ; 0000-0001-6619-9938 ; 0000-0003-3721-9295 ; 0000-0002-5736-6797 ; 0000-0002-3247-5436 ; 0000-0002-6100-1125 ; 0000-0003-0591-5018 ; 0000-0002-3979-7358</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11483521/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11483521/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11541,27901,27902,45550,45551,46027,46451,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38705944$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vymola, Petr</creatorcontrib><creatorcontrib>Garcia‐Borja, Elena</creatorcontrib><creatorcontrib>Cervenka, Jakub</creatorcontrib><creatorcontrib>Balaziova, Eva</creatorcontrib><creatorcontrib>Vymolova, Barbora</creatorcontrib><creatorcontrib>Veprkova, Jana</creatorcontrib><creatorcontrib>Vodicka, Petr</creatorcontrib><creatorcontrib>Skalnikova, Helena</creatorcontrib><creatorcontrib>Tomas, Robert</creatorcontrib><creatorcontrib>Netuka, David</creatorcontrib><creatorcontrib>Busek, Petr</creatorcontrib><creatorcontrib>Sedo, Aleksi</creatorcontrib><title>Fibrillar extracellular matrix produced by pericyte‐like cells facilitates glioma cell dissemination</title><title>Brain pathology (Zurich, Switzerland)</title><addtitle>Brain Pathol</addtitle><description>Gliomagenesis induces profound changes in the composition of the extracellular matrix (ECM) of the brain. In this study, we identified a cellular population responsible for the increased deposition of collagen I and fibronectin in glioblastoma. Elevated levels of the fibrillar proteins collagen I and fibronectin were associated with the expression of fibroblast activation protein (FAP), which is predominantly found in pericyte‐like cells in glioblastoma. FAP+ pericyte‐like cells were present in regions rich in collagen I and fibronectin in biopsy material and produced substantially more collagen I and fibronectin in vitro compared to other cell types found in the GBM microenvironment. Using mass spectrometry, we demonstrated that 3D matrices produced by FAP+ pericyte‐like cells are rich in collagen I and fibronectin and contain several basement membrane proteins. This expression pattern differed markedly from glioma cells. Finally, we have shown that ECM produced by FAP+ pericyte‐like cells enhances the migration of glioma cells including glioma stem‐like cells, promotes their adhesion, and activates focal adhesion kinase (FAK) signaling. Taken together, our findings establish FAP+ pericyte‐like cells as crucial producers of a complex ECM rich in collagen I and fibronectin, facilitating the dissemination of glioma cells through FAK activation.
FAP+ pericyte‐like cells drive the deposition of fibrillar extracellular matrix proteins such as collagen I and fibronectin in glioblastoma, facilitating glioma cell dissemination and activation of focal adhesion kinase.</description><subject>Adhesion</subject><subject>Basement membranes</subject><subject>Biopsy</subject><subject>Brain Neoplasms - metabolism</subject><subject>Brain Neoplasms - pathology</subject><subject>Cell activation</subject><subject>Cell Line, Tumor</subject><subject>Cell migration</subject><subject>Cell Movement - physiology</subject><subject>Collagen</subject><subject>collagen type I</subject><subject>Collagen Type I - metabolism</subject><subject>Endopeptidases</subject><subject>Extracellular matrix</subject><subject>Extracellular Matrix - metabolism</subject><subject>Extracellular Matrix - pathology</subject><subject>extracellular matrix proteins</subject><subject>Fibroblast activation protein</subject><subject>Fibronectin</subject><subject>Fibronectins - metabolism</subject><subject>Focal adhesion kinase</subject><subject>Gelatinases - metabolism</subject><subject>Glioblastoma</subject><subject>Glioblastoma - metabolism</subject><subject>Glioblastoma - pathology</subject><subject>Glioma</subject><subject>Glioma - metabolism</subject><subject>Glioma - pathology</subject><subject>Glioma cells</subject><subject>Humans</subject><subject>Kinases</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Membrane proteins</subject><subject>Membrane Proteins - metabolism</subject><subject>Microenvironments</subject><subject>pericytes</subject><subject>Pericytes - metabolism</subject><subject>Pericytes - pathology</subject><subject>Population studies</subject><subject>Proteins</subject><subject>proteomics</subject><subject>Serine Endopeptidases - metabolism</subject><subject>Tumor Microenvironment - physiology</subject><issn>1015-6305</issn><issn>1750-3639</issn><issn>1750-3639</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kctu1TAQhi0E6o0ueAEUiQ1dpPX4kssKlaoFpEp0UdaWY0-KixMHO4GeXR-hz9gnwaenVIDEbDyj-fRrfv-EvAJ6CLmOukkfAmeVfEZ2oJa05BVvn-eegiwrTuU22U3pmlJoq1ZukW3e1FS2QuyQ_sx10XmvY4E3c9QGvV_W06Dn6G6KKQa7GLRFtyomjM6sZry_vfPuGxZrNhW9Ns67Wc-YiivvwqAfFoV1KeHgRj27ML4kL3rtE-4_vnvky9np5cnH8vzzh08nx-elEVTIUkqq-5Y3nawasBXUhjKGwBgDi4x2NVrRWhRS1waYYLVtgPeVbZqubTkKvkfebXSnpRvQGhyzJ6-m6AYdVypop_7ejO6rugo_FIBouGSQFd4-KsTwfcE0q8GltSE9YliSyr8JgkkOVUbf_INehyWO2Z_iADVIIWWTqYMNZWJIKWL_dA1QtY5P5fjUQ3yZff3n-U_k77wycLQBfjqPq_8rqfcXxxvJX2UKpmw</recordid><startdate>202411</startdate><enddate>202411</enddate><creator>Vymola, Petr</creator><creator>Garcia‐Borja, Elena</creator><creator>Cervenka, Jakub</creator><creator>Balaziova, Eva</creator><creator>Vymolova, Barbora</creator><creator>Veprkova, Jana</creator><creator>Vodicka, Petr</creator><creator>Skalnikova, Helena</creator><creator>Tomas, Robert</creator><creator>Netuka, David</creator><creator>Busek, Petr</creator><creator>Sedo, Aleksi</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><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>7TK</scope><scope>JQ2</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9947-2045</orcidid><orcidid>https://orcid.org/0000-0002-6605-9158</orcidid><orcidid>https://orcid.org/0000-0001-6863-0496</orcidid><orcidid>https://orcid.org/0000-0002-5267-2920</orcidid><orcidid>https://orcid.org/0000-0001-8609-4789</orcidid><orcidid>https://orcid.org/0000-0001-6619-9938</orcidid><orcidid>https://orcid.org/0000-0003-3721-9295</orcidid><orcidid>https://orcid.org/0000-0002-5736-6797</orcidid><orcidid>https://orcid.org/0000-0002-3247-5436</orcidid><orcidid>https://orcid.org/0000-0002-6100-1125</orcidid><orcidid>https://orcid.org/0000-0003-0591-5018</orcidid><orcidid>https://orcid.org/0000-0002-3979-7358</orcidid></search><sort><creationdate>202411</creationdate><title>Fibrillar extracellular matrix produced by pericyte‐like cells facilitates glioma cell dissemination</title><author>Vymola, Petr ; Garcia‐Borja, Elena ; Cervenka, Jakub ; Balaziova, Eva ; Vymolova, Barbora ; Veprkova, Jana ; Vodicka, Petr ; Skalnikova, Helena ; Tomas, Robert ; Netuka, David ; Busek, Petr ; Sedo, Aleksi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4045-550af938b5681d617c022e12221de20b7ed49de45a7c12427d813f6d88b993e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adhesion</topic><topic>Basement membranes</topic><topic>Biopsy</topic><topic>Brain Neoplasms - metabolism</topic><topic>Brain Neoplasms - pathology</topic><topic>Cell activation</topic><topic>Cell Line, Tumor</topic><topic>Cell migration</topic><topic>Cell Movement - physiology</topic><topic>Collagen</topic><topic>collagen type I</topic><topic>Collagen Type I - metabolism</topic><topic>Endopeptidases</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - metabolism</topic><topic>Extracellular Matrix - pathology</topic><topic>extracellular matrix proteins</topic><topic>Fibroblast activation protein</topic><topic>Fibronectin</topic><topic>Fibronectins - metabolism</topic><topic>Focal adhesion kinase</topic><topic>Gelatinases - metabolism</topic><topic>Glioblastoma</topic><topic>Glioblastoma - metabolism</topic><topic>Glioblastoma - pathology</topic><topic>Glioma</topic><topic>Glioma - metabolism</topic><topic>Glioma - pathology</topic><topic>Glioma cells</topic><topic>Humans</topic><topic>Kinases</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Membrane proteins</topic><topic>Membrane Proteins - metabolism</topic><topic>Microenvironments</topic><topic>pericytes</topic><topic>Pericytes - metabolism</topic><topic>Pericytes - pathology</topic><topic>Population studies</topic><topic>Proteins</topic><topic>proteomics</topic><topic>Serine Endopeptidases - metabolism</topic><topic>Tumor Microenvironment - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vymola, Petr</creatorcontrib><creatorcontrib>Garcia‐Borja, Elena</creatorcontrib><creatorcontrib>Cervenka, Jakub</creatorcontrib><creatorcontrib>Balaziova, Eva</creatorcontrib><creatorcontrib>Vymolova, Barbora</creatorcontrib><creatorcontrib>Veprkova, Jana</creatorcontrib><creatorcontrib>Vodicka, Petr</creatorcontrib><creatorcontrib>Skalnikova, Helena</creatorcontrib><creatorcontrib>Tomas, Robert</creatorcontrib><creatorcontrib>Netuka, David</creatorcontrib><creatorcontrib>Busek, Petr</creatorcontrib><creatorcontrib>Sedo, Aleksi</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Brain pathology (Zurich, Switzerland)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vymola, Petr</au><au>Garcia‐Borja, Elena</au><au>Cervenka, Jakub</au><au>Balaziova, Eva</au><au>Vymolova, Barbora</au><au>Veprkova, Jana</au><au>Vodicka, Petr</au><au>Skalnikova, Helena</au><au>Tomas, Robert</au><au>Netuka, David</au><au>Busek, Petr</au><au>Sedo, Aleksi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fibrillar extracellular matrix produced by pericyte‐like cells facilitates glioma cell dissemination</atitle><jtitle>Brain pathology (Zurich, Switzerland)</jtitle><addtitle>Brain Pathol</addtitle><date>2024-11</date><risdate>2024</risdate><volume>34</volume><issue>6</issue><spage>e13265</spage><epage>n/a</epage><pages>e13265-n/a</pages><issn>1015-6305</issn><issn>1750-3639</issn><eissn>1750-3639</eissn><abstract>Gliomagenesis induces profound changes in the composition of the extracellular matrix (ECM) of the brain. In this study, we identified a cellular population responsible for the increased deposition of collagen I and fibronectin in glioblastoma. Elevated levels of the fibrillar proteins collagen I and fibronectin were associated with the expression of fibroblast activation protein (FAP), which is predominantly found in pericyte‐like cells in glioblastoma. FAP+ pericyte‐like cells were present in regions rich in collagen I and fibronectin in biopsy material and produced substantially more collagen I and fibronectin in vitro compared to other cell types found in the GBM microenvironment. Using mass spectrometry, we demonstrated that 3D matrices produced by FAP+ pericyte‐like cells are rich in collagen I and fibronectin and contain several basement membrane proteins. This expression pattern differed markedly from glioma cells. Finally, we have shown that ECM produced by FAP+ pericyte‐like cells enhances the migration of glioma cells including glioma stem‐like cells, promotes their adhesion, and activates focal adhesion kinase (FAK) signaling. Taken together, our findings establish FAP+ pericyte‐like cells as crucial producers of a complex ECM rich in collagen I and fibronectin, facilitating the dissemination of glioma cells through FAK activation.
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| source | MEDLINE; Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Adhesion Basement membranes Biopsy Brain Neoplasms - metabolism Brain Neoplasms - pathology Cell activation Cell Line, Tumor Cell migration Cell Movement - physiology Collagen collagen type I Collagen Type I - metabolism Endopeptidases Extracellular matrix Extracellular Matrix - metabolism Extracellular Matrix - pathology extracellular matrix proteins Fibroblast activation protein Fibronectin Fibronectins - metabolism Focal adhesion kinase Gelatinases - metabolism Glioblastoma Glioblastoma - metabolism Glioblastoma - pathology Glioma Glioma - metabolism Glioma - pathology Glioma cells Humans Kinases Mass spectrometry Mass spectroscopy Membrane proteins Membrane Proteins - metabolism Microenvironments pericytes Pericytes - metabolism Pericytes - pathology Population studies Proteins proteomics Serine Endopeptidases - metabolism Tumor Microenvironment - physiology |
| title | Fibrillar extracellular matrix produced by pericyte‐like cells facilitates glioma cell dissemination |
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