The miRNA Content of Bone Marrow-Derived Extracellular Vesicles Contributes to Protein Pathway Alterations Involved in Ionising Radiation-Induced Bystander Responses
Extracellular vesicles (EVs), through their cargo, are important mediators of bystander responses in the irradiated bone marrow (BM). MiRNAs carried by EVs can potentially alter cellular pathways in EV-recipient cells by regulating their protein content. Using the CBA/Ca mouse model, we characterise...
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| Veröffentlicht in: | International journal of molecular sciences 2023-05, Vol.24 (10), p.8607 |
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| creator | Csordás, Ilona Barbara Rutten, Eric Andreas Szatmári, Tünde Subedi, Prabal Cruz-Garcia, Lourdes Kis, Dávid Jezsó, Bálint Toerne, Christine von Forgács, Martina Sáfrány, Géza Tapio, Soile Badie, Christophe Lumniczky, Katalin |
| description | Extracellular vesicles (EVs), through their cargo, are important mediators of bystander responses in the irradiated bone marrow (BM). MiRNAs carried by EVs can potentially alter cellular pathways in EV-recipient cells by regulating their protein content. Using the CBA/Ca mouse model, we characterised the miRNA content of BM-derived EVs from mice irradiated with 0.1 Gy or 3 Gy using an nCounter analysis system. We also analysed proteomic changes in BM cells either directly irradiated or treated with EVs derived from the BM of irradiated mice. Our aim was to identify key cellular processes in the EV-acceptor cells regulated by miRNAs. The irradiation of BM cells with 0.1 Gy led to protein alterations involved in oxidative stress and immune and inflammatory processes. Oxidative stress-related pathways were also present in BM cells treated with EVs isolated from 0.1 Gy-irradiated mice, indicating the propagation of oxidative stress in a bystander manner. The irradiation of BM cells with 3 Gy led to protein pathway alterations involved in the DNA damage response, metabolism, cell death and immune and inflammatory processes. The majority of these pathways were also altered in BM cells treated with EVs from mice irradiated with 3 Gy. Certain pathways (cell cycle, acute and chronic myeloid leukaemia) regulated by miRNAs differentially expressed in EVs isolated from mice irradiated with 3 Gy overlapped with protein pathway alterations in BM cells treated with 3 Gy EVs. Six miRNAs were involved in these common pathways interacting with 11 proteins, suggesting the involvement of miRNAs in the EV-mediated bystander processes. In conclusion, we characterised proteomic changes in directly irradiated and EV-treated BM cells, identified processes transmitted in a bystander manner and suggested miRNA and protein candidates potentially involved in the regulation of these bystander processes. |
| doi_str_mv | 10.3390/ijms24108607 |
| format | Article |
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MiRNAs carried by EVs can potentially alter cellular pathways in EV-recipient cells by regulating their protein content. Using the CBA/Ca mouse model, we characterised the miRNA content of BM-derived EVs from mice irradiated with 0.1 Gy or 3 Gy using an nCounter analysis system. We also analysed proteomic changes in BM cells either directly irradiated or treated with EVs derived from the BM of irradiated mice. Our aim was to identify key cellular processes in the EV-acceptor cells regulated by miRNAs. The irradiation of BM cells with 0.1 Gy led to protein alterations involved in oxidative stress and immune and inflammatory processes. Oxidative stress-related pathways were also present in BM cells treated with EVs isolated from 0.1 Gy-irradiated mice, indicating the propagation of oxidative stress in a bystander manner. The irradiation of BM cells with 3 Gy led to protein pathway alterations involved in the DNA damage response, metabolism, cell death and immune and inflammatory processes. The majority of these pathways were also altered in BM cells treated with EVs from mice irradiated with 3 Gy. Certain pathways (cell cycle, acute and chronic myeloid leukaemia) regulated by miRNAs differentially expressed in EVs isolated from mice irradiated with 3 Gy overlapped with protein pathway alterations in BM cells treated with 3 Gy EVs. Six miRNAs were involved in these common pathways interacting with 11 proteins, suggesting the involvement of miRNAs in the EV-mediated bystander processes. In conclusion, we characterised proteomic changes in directly irradiated and EV-treated BM cells, identified processes transmitted in a bystander manner and suggested miRNA and protein candidates potentially involved in the regulation of these bystander processes.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms24108607</identifier><identifier>PMID: 37239971</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Analysis ; Animals ; Bone marrow ; Bone Marrow - metabolism ; Cell cycle ; Cell death ; Chronic myeloid leukemia ; Communication ; DNA damage ; Extracellular vesicles ; Extracellular Vesicles - metabolism ; Inflammation ; Ionizing radiation ; Leukemia ; Mice ; Mice, Inbred CBA ; MicroRNA ; MicroRNAs ; MicroRNAs - genetics ; MicroRNAs - metabolism ; miRNA ; Oxidative stress ; Phosphorylation ; Physiological aspects ; Proteins ; Proteomics ; Radiation ; Radiation effects ; Radiation, Ionizing ; Scientific equipment and supplies industry ; Signal transduction ; Stem cells ; Stress propagation ; Vesicles</subject><ispartof>International journal of molecular sciences, 2023-05, Vol.24 (10), p.8607</ispartof><rights>COPYRIGHT 2023 MDPI AG</rights><rights>2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 by the authors. 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c480t-5ebec67b8b66112f6b87190b59ddcdd12e1c82e66d454a9b126529a49dde89a03</citedby><cites>FETCH-LOGICAL-c480t-5ebec67b8b66112f6b87190b59ddcdd12e1c82e66d454a9b126529a49dde89a03</cites><orcidid>0000-0002-1306-4797 ; 0000-0001-8661-1854 ; 0000-0002-5661-3776 ; 0000-0003-2542-6860 ; 0000-0003-4572-5008</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/PMC10218377/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10218377/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37239971$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Csordás, Ilona Barbara</creatorcontrib><creatorcontrib>Rutten, Eric Andreas</creatorcontrib><creatorcontrib>Szatmári, Tünde</creatorcontrib><creatorcontrib>Subedi, Prabal</creatorcontrib><creatorcontrib>Cruz-Garcia, Lourdes</creatorcontrib><creatorcontrib>Kis, Dávid</creatorcontrib><creatorcontrib>Jezsó, Bálint</creatorcontrib><creatorcontrib>Toerne, Christine von</creatorcontrib><creatorcontrib>Forgács, Martina</creatorcontrib><creatorcontrib>Sáfrány, Géza</creatorcontrib><creatorcontrib>Tapio, Soile</creatorcontrib><creatorcontrib>Badie, Christophe</creatorcontrib><creatorcontrib>Lumniczky, Katalin</creatorcontrib><title>The miRNA Content of Bone Marrow-Derived Extracellular Vesicles Contributes to Protein Pathway Alterations Involved in Ionising Radiation-Induced Bystander Responses</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Extracellular vesicles (EVs), through their cargo, are important mediators of bystander responses in the irradiated bone marrow (BM). MiRNAs carried by EVs can potentially alter cellular pathways in EV-recipient cells by regulating their protein content. Using the CBA/Ca mouse model, we characterised the miRNA content of BM-derived EVs from mice irradiated with 0.1 Gy or 3 Gy using an nCounter analysis system. We also analysed proteomic changes in BM cells either directly irradiated or treated with EVs derived from the BM of irradiated mice. Our aim was to identify key cellular processes in the EV-acceptor cells regulated by miRNAs. The irradiation of BM cells with 0.1 Gy led to protein alterations involved in oxidative stress and immune and inflammatory processes. Oxidative stress-related pathways were also present in BM cells treated with EVs isolated from 0.1 Gy-irradiated mice, indicating the propagation of oxidative stress in a bystander manner. The irradiation of BM cells with 3 Gy led to protein pathway alterations involved in the DNA damage response, metabolism, cell death and immune and inflammatory processes. The majority of these pathways were also altered in BM cells treated with EVs from mice irradiated with 3 Gy. Certain pathways (cell cycle, acute and chronic myeloid leukaemia) regulated by miRNAs differentially expressed in EVs isolated from mice irradiated with 3 Gy overlapped with protein pathway alterations in BM cells treated with 3 Gy EVs. Six miRNAs were involved in these common pathways interacting with 11 proteins, suggesting the involvement of miRNAs in the EV-mediated bystander processes. 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MiRNAs carried by EVs can potentially alter cellular pathways in EV-recipient cells by regulating their protein content. Using the CBA/Ca mouse model, we characterised the miRNA content of BM-derived EVs from mice irradiated with 0.1 Gy or 3 Gy using an nCounter analysis system. We also analysed proteomic changes in BM cells either directly irradiated or treated with EVs derived from the BM of irradiated mice. Our aim was to identify key cellular processes in the EV-acceptor cells regulated by miRNAs. The irradiation of BM cells with 0.1 Gy led to protein alterations involved in oxidative stress and immune and inflammatory processes. Oxidative stress-related pathways were also present in BM cells treated with EVs isolated from 0.1 Gy-irradiated mice, indicating the propagation of oxidative stress in a bystander manner. The irradiation of BM cells with 3 Gy led to protein pathway alterations involved in the DNA damage response, metabolism, cell death and immune and inflammatory processes. The majority of these pathways were also altered in BM cells treated with EVs from mice irradiated with 3 Gy. Certain pathways (cell cycle, acute and chronic myeloid leukaemia) regulated by miRNAs differentially expressed in EVs isolated from mice irradiated with 3 Gy overlapped with protein pathway alterations in BM cells treated with 3 Gy EVs. Six miRNAs were involved in these common pathways interacting with 11 proteins, suggesting the involvement of miRNAs in the EV-mediated bystander processes. In conclusion, we characterised proteomic changes in directly irradiated and EV-treated BM cells, identified processes transmitted in a bystander manner and suggested miRNA and protein candidates potentially involved in the regulation of these bystander processes.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>37239971</pmid><doi>10.3390/ijms24108607</doi><orcidid>https://orcid.org/0000-0002-1306-4797</orcidid><orcidid>https://orcid.org/0000-0001-8661-1854</orcidid><orcidid>https://orcid.org/0000-0002-5661-3776</orcidid><orcidid>https://orcid.org/0000-0003-2542-6860</orcidid><orcidid>https://orcid.org/0000-0003-4572-5008</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Animals Bone marrow Bone Marrow - metabolism Cell cycle Cell death Chronic myeloid leukemia Communication DNA damage Extracellular vesicles Extracellular Vesicles - metabolism Inflammation Ionizing radiation Leukemia Mice Mice, Inbred CBA MicroRNA MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA Oxidative stress Phosphorylation Physiological aspects Proteins Proteomics Radiation Radiation effects Radiation, Ionizing Scientific equipment and supplies industry Signal transduction Stem cells Stress propagation Vesicles |
| title | The miRNA Content of Bone Marrow-Derived Extracellular Vesicles Contributes to Protein Pathway Alterations Involved in Ionising Radiation-Induced Bystander Responses |
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