Proteomic Analysis Implicates Dominant Alterations of RNA Metabolism and the Proteasome Pathway in the Cellular Response to Carbon-Ion Irradiation
Radiotherapy with heavy ions is considered advantageous compared to irradiation with photons due to the characteristics of the Braggs peak and the high linear energy transfer (LET) value. To understand the mechanisms of cellular responses to different LET values and dosages of heavy ion radiation, w...
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| Veröffentlicht in: | PloS one 2016-10, Vol.11 (10), p.e0163896 |
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| description | Radiotherapy with heavy ions is considered advantageous compared to irradiation with photons due to the characteristics of the Braggs peak and the high linear energy transfer (LET) value. To understand the mechanisms of cellular responses to different LET values and dosages of heavy ion radiation, we analyzed the proteomic profiles of mouse embryo fibroblast MEF cells exposed to two doses from different LET values of heavy ion 12C. Total proteins were extracted from these cells and examined by Q Exactive with Liquid Chromatography (LC)-Electrospray Ionization (ESI) Tandem MS (MS/MS). Using bioinformatics approaches, differentially expressed proteins with 1.5 or 2.0-fold changes between different dosages of exposure were compared. With the higher the dosage and/or LET of ion irradiation, the worse response the cells were in terms of protein expression. For instance, compared to the control (0 Gy), 771 (20.2%) proteins in cells irradiated at 0.2 Gy of carbon-ion radiation with 12.6 keV/μm, 313 proteins (8.2%) in cells irradiated at 2 Gy of carbon-ion radiation with 12.6 keV/μm, and 243 proteins (6.4%) in cells irradiated at 2 Gy of carbon-ion radiation with 31.5 keV/μm exhibited changes of 1.5-fold or greater. Gene ontology (GO) analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis, Munich Information Center for Protein Sequences (MIPS) analysis, and BioCarta analysis all indicated that RNA metabolic processes (RNA splicing, destabilization and deadenylation) and proteasome pathways may play key roles in the cellular response to heavy-ion irradiation. Proteasome pathways ranked highest among all biological processes associated with heavy carbon-ion irradiation. In addition, network analysis revealed that cellular pathways involving proteins such as Col1a1 and Fn1 continued to respond to high dosages of heavy-ion irradiation, suggesting that these pathways still protect cells against damage. However, pathways such as those involving Ikbkg1 responded better at lower dosages than at higher dosages, implying that cell damage would occur when the networks involving these proteins stop responding. Our investigation provides valuable proteomic information for elucidating the mechanism of biological effects induced by carbon ions in general. |
| doi_str_mv | 10.1371/journal.pone.0163896 |
| format | Article |
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To understand the mechanisms of cellular responses to different LET values and dosages of heavy ion radiation, we analyzed the proteomic profiles of mouse embryo fibroblast MEF cells exposed to two doses from different LET values of heavy ion 12C. Total proteins were extracted from these cells and examined by Q Exactive with Liquid Chromatography (LC)-Electrospray Ionization (ESI) Tandem MS (MS/MS). Using bioinformatics approaches, differentially expressed proteins with 1.5 or 2.0-fold changes between different dosages of exposure were compared. With the higher the dosage and/or LET of ion irradiation, the worse response the cells were in terms of protein expression. For instance, compared to the control (0 Gy), 771 (20.2%) proteins in cells irradiated at 0.2 Gy of carbon-ion radiation with 12.6 keV/μm, 313 proteins (8.2%) in cells irradiated at 2 Gy of carbon-ion radiation with 12.6 keV/μm, and 243 proteins (6.4%) in cells irradiated at 2 Gy of carbon-ion radiation with 31.5 keV/μm exhibited changes of 1.5-fold or greater. Gene ontology (GO) analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis, Munich Information Center for Protein Sequences (MIPS) analysis, and BioCarta analysis all indicated that RNA metabolic processes (RNA splicing, destabilization and deadenylation) and proteasome pathways may play key roles in the cellular response to heavy-ion irradiation. Proteasome pathways ranked highest among all biological processes associated with heavy carbon-ion irradiation. In addition, network analysis revealed that cellular pathways involving proteins such as Col1a1 and Fn1 continued to respond to high dosages of heavy-ion irradiation, suggesting that these pathways still protect cells against damage. However, pathways such as those involving Ikbkg1 responded better at lower dosages than at higher dosages, implying that cell damage would occur when the networks involving these proteins stop responding. Our investigation provides valuable proteomic information for elucidating the mechanism of biological effects induced by carbon ions in general.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0163896</identifier><identifier>PMID: 27711237</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Advantages ; Animals ; Autophagy ; Bioinformatics ; Biological activity ; Biological effects ; Biology ; Biology and Life Sciences ; Cancer therapies ; Carbon ; Carbon - pharmacology ; Cell cycle ; Cell Line ; Cellular communication ; Chromatography ; Collaboration ; Collagen (type I) ; Comparative analysis ; Deoxyribonucleic acid ; Destabilization ; DNA ; DNA damage ; DNA methylation ; DNA repair ; Dose-Response Relationship, Radiation ; Drug dosages ; Encyclopedias ; Energy transfer ; Fibroblasts - metabolism ; Fibroblasts - radiation effects ; Fibronectins ; Gene expression ; Gene sequencing ; Genomes ; Heavy ion radiation ; Heavy Ion Radiotherapy ; Heavy ions ; Higher education ; Ion irradiation ; Ionization ; Ionizing radiation ; Irradiation ; Laboratories ; Linear energy transfer (LET) ; Liquid chromatography ; Medical research ; Medicine ; Medicine and Health Sciences ; Metabolism ; Mice ; Network analysis ; Oncology ; Photons ; Physical Sciences ; Physics ; Proteasome Endopeptidase Complex - metabolism ; Proteasomes ; Proteins ; Proteomics ; Radiation ; Radiation damage ; Radiation therapy ; Radiotherapy ; Research and Analysis Methods ; Ribonucleic acid ; RNA ; RNA - metabolism ; Splicing ; Studies ; X-rays</subject><ispartof>PloS one, 2016-10, Vol.11 (10), p.e0163896</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Wang et al 2016 Wang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-cc37edae808f480456b4678d5f9e47ea588a92d3a2b23baff239a5237e4948e33</citedby><cites>FETCH-LOGICAL-c758t-cc37edae808f480456b4678d5f9e47ea588a92d3a2b23baff239a5237e4948e33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5053480/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5053480/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27711237$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Chuang, Eric Y.</contributor><creatorcontrib>Wang, Yu</creatorcontrib><creatorcontrib>Guan, Hua</creatorcontrib><creatorcontrib>Xie, Da-Fei</creatorcontrib><creatorcontrib>Xie, Yi</creatorcontrib><creatorcontrib>Liu, Xiao-Dan</creatorcontrib><creatorcontrib>Wang, Qi</creatorcontrib><creatorcontrib>Sui, Li</creatorcontrib><creatorcontrib>Song, Man</creatorcontrib><creatorcontrib>Zhang, Hong</creatorcontrib><creatorcontrib>Zhou, Jianhua</creatorcontrib><creatorcontrib>Zhou, Ping-Kun</creatorcontrib><title>Proteomic Analysis Implicates Dominant Alterations of RNA Metabolism and the Proteasome Pathway in the Cellular Response to Carbon-Ion Irradiation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Radiotherapy with heavy ions is considered advantageous compared to irradiation with photons due to the characteristics of the Braggs peak and the high linear energy transfer (LET) value. To understand the mechanisms of cellular responses to different LET values and dosages of heavy ion radiation, we analyzed the proteomic profiles of mouse embryo fibroblast MEF cells exposed to two doses from different LET values of heavy ion 12C. Total proteins were extracted from these cells and examined by Q Exactive with Liquid Chromatography (LC)-Electrospray Ionization (ESI) Tandem MS (MS/MS). Using bioinformatics approaches, differentially expressed proteins with 1.5 or 2.0-fold changes between different dosages of exposure were compared. With the higher the dosage and/or LET of ion irradiation, the worse response the cells were in terms of protein expression. For instance, compared to the control (0 Gy), 771 (20.2%) proteins in cells irradiated at 0.2 Gy of carbon-ion radiation with 12.6 keV/μm, 313 proteins (8.2%) in cells irradiated at 2 Gy of carbon-ion radiation with 12.6 keV/μm, and 243 proteins (6.4%) in cells irradiated at 2 Gy of carbon-ion radiation with 31.5 keV/μm exhibited changes of 1.5-fold or greater. Gene ontology (GO) analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis, Munich Information Center for Protein Sequences (MIPS) analysis, and BioCarta analysis all indicated that RNA metabolic processes (RNA splicing, destabilization and deadenylation) and proteasome pathways may play key roles in the cellular response to heavy-ion irradiation. Proteasome pathways ranked highest among all biological processes associated with heavy carbon-ion irradiation. In addition, network analysis revealed that cellular pathways involving proteins such as Col1a1 and Fn1 continued to respond to high dosages of heavy-ion irradiation, suggesting that these pathways still protect cells against damage. However, pathways such as those involving Ikbkg1 responded better at lower dosages than at higher dosages, implying that cell damage would occur when the networks involving these proteins stop responding. Our investigation provides valuable proteomic information for elucidating the mechanism of biological effects induced by carbon ions in general.</description><subject>Advantages</subject><subject>Animals</subject><subject>Autophagy</subject><subject>Bioinformatics</subject><subject>Biological activity</subject><subject>Biological effects</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cancer therapies</subject><subject>Carbon</subject><subject>Carbon - pharmacology</subject><subject>Cell cycle</subject><subject>Cell Line</subject><subject>Cellular communication</subject><subject>Chromatography</subject><subject>Collaboration</subject><subject>Collagen (type I)</subject><subject>Comparative analysis</subject><subject>Deoxyribonucleic acid</subject><subject>Destabilization</subject><subject>DNA</subject><subject>DNA damage</subject><subject>DNA methylation</subject><subject>DNA repair</subject><subject>Dose-Response Relationship, Radiation</subject><subject>Drug dosages</subject><subject>Encyclopedias</subject><subject>Energy transfer</subject><subject>Fibroblasts - metabolism</subject><subject>Fibroblasts - radiation effects</subject><subject>Fibronectins</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Genomes</subject><subject>Heavy ion radiation</subject><subject>Heavy Ion Radiotherapy</subject><subject>Heavy ions</subject><subject>Higher education</subject><subject>Ion irradiation</subject><subject>Ionization</subject><subject>Ionizing radiation</subject><subject>Irradiation</subject><subject>Laboratories</subject><subject>Linear energy transfer (LET)</subject><subject>Liquid chromatography</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Network analysis</subject><subject>Oncology</subject><subject>Photons</subject><subject>Physical Sciences</subject><subject>Physics</subject><subject>Proteasome Endopeptidase Complex - metabolism</subject><subject>Proteasomes</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Radiation</subject><subject>Radiation damage</subject><subject>Radiation therapy</subject><subject>Radiotherapy</subject><subject>Research and Analysis Methods</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA - 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metabolism</topic><topic>Proteasomes</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Radiation</topic><topic>Radiation damage</topic><topic>Radiation therapy</topic><topic>Radiotherapy</topic><topic>Research and Analysis Methods</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA - metabolism</topic><topic>Splicing</topic><topic>Studies</topic><topic>X-rays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Yu</creatorcontrib><creatorcontrib>Guan, Hua</creatorcontrib><creatorcontrib>Xie, Da-Fei</creatorcontrib><creatorcontrib>Xie, Yi</creatorcontrib><creatorcontrib>Liu, Xiao-Dan</creatorcontrib><creatorcontrib>Wang, Qi</creatorcontrib><creatorcontrib>Sui, Li</creatorcontrib><creatorcontrib>Song, Man</creatorcontrib><creatorcontrib>Zhang, Hong</creatorcontrib><creatorcontrib>Zhou, Jianhua</creatorcontrib><creatorcontrib>Zhou, Ping-Kun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Yu</au><au>Guan, Hua</au><au>Xie, Da-Fei</au><au>Xie, Yi</au><au>Liu, Xiao-Dan</au><au>Wang, Qi</au><au>Sui, Li</au><au>Song, Man</au><au>Zhang, Hong</au><au>Zhou, Jianhua</au><au>Zhou, Ping-Kun</au><au>Chuang, Eric Y.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Proteomic Analysis Implicates Dominant Alterations of RNA Metabolism and the Proteasome Pathway in the Cellular Response to Carbon-Ion Irradiation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-10-06</date><risdate>2016</risdate><volume>11</volume><issue>10</issue><spage>e0163896</spage><pages>e0163896-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Radiotherapy with heavy ions is considered advantageous compared to irradiation with photons due to the characteristics of the Braggs peak and the high linear energy transfer (LET) value. To understand the mechanisms of cellular responses to different LET values and dosages of heavy ion radiation, we analyzed the proteomic profiles of mouse embryo fibroblast MEF cells exposed to two doses from different LET values of heavy ion 12C. Total proteins were extracted from these cells and examined by Q Exactive with Liquid Chromatography (LC)-Electrospray Ionization (ESI) Tandem MS (MS/MS). Using bioinformatics approaches, differentially expressed proteins with 1.5 or 2.0-fold changes between different dosages of exposure were compared. With the higher the dosage and/or LET of ion irradiation, the worse response the cells were in terms of protein expression. For instance, compared to the control (0 Gy), 771 (20.2%) proteins in cells irradiated at 0.2 Gy of carbon-ion radiation with 12.6 keV/μm, 313 proteins (8.2%) in cells irradiated at 2 Gy of carbon-ion radiation with 12.6 keV/μm, and 243 proteins (6.4%) in cells irradiated at 2 Gy of carbon-ion radiation with 31.5 keV/μm exhibited changes of 1.5-fold or greater. Gene ontology (GO) analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis, Munich Information Center for Protein Sequences (MIPS) analysis, and BioCarta analysis all indicated that RNA metabolic processes (RNA splicing, destabilization and deadenylation) and proteasome pathways may play key roles in the cellular response to heavy-ion irradiation. Proteasome pathways ranked highest among all biological processes associated with heavy carbon-ion irradiation. In addition, network analysis revealed that cellular pathways involving proteins such as Col1a1 and Fn1 continued to respond to high dosages of heavy-ion irradiation, suggesting that these pathways still protect cells against damage. However, pathways such as those involving Ikbkg1 responded better at lower dosages than at higher dosages, implying that cell damage would occur when the networks involving these proteins stop responding. Our investigation provides valuable proteomic information for elucidating the mechanism of biological effects induced by carbon ions in general.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27711237</pmid><doi>10.1371/journal.pone.0163896</doi><tpages>e0163896</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2016-10, Vol.11 (10), p.e0163896 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1826491178 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Advantages Animals Autophagy Bioinformatics Biological activity Biological effects Biology Biology and Life Sciences Cancer therapies Carbon Carbon - pharmacology Cell cycle Cell Line Cellular communication Chromatography Collaboration Collagen (type I) Comparative analysis Deoxyribonucleic acid Destabilization DNA DNA damage DNA methylation DNA repair Dose-Response Relationship, Radiation Drug dosages Encyclopedias Energy transfer Fibroblasts - metabolism Fibroblasts - radiation effects Fibronectins Gene expression Gene sequencing Genomes Heavy ion radiation Heavy Ion Radiotherapy Heavy ions Higher education Ion irradiation Ionization Ionizing radiation Irradiation Laboratories Linear energy transfer (LET) Liquid chromatography Medical research Medicine Medicine and Health Sciences Metabolism Mice Network analysis Oncology Photons Physical Sciences Physics Proteasome Endopeptidase Complex - metabolism Proteasomes Proteins Proteomics Radiation Radiation damage Radiation therapy Radiotherapy Research and Analysis Methods Ribonucleic acid RNA RNA - metabolism Splicing Studies X-rays |
| title | Proteomic Analysis Implicates Dominant Alterations of RNA Metabolism and the Proteasome Pathway in the Cellular Response to Carbon-Ion Irradiation |
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