Stress response regulation of mRNA translation: Implications for antioxidant enzyme expression in cancer
From tumorigenesis to advanced metastatic stages, tumor cells encounter stress, ranging from limited nutrient and oxygen supply within the tumor microenvironment to extrinsic and intrinsic oxidative stress. Thus, tumor cells seize regulatory pathways to rapidly adapt to distinct physiologic conditio...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2024-11, Vol.121 (46), p.e2317846121 |
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creator | Kim, Yeon Soo Kimball, Scot R Piskounova, Elena Begley, Thomas J Hempel, Nadine |
description | From tumorigenesis to advanced metastatic stages, tumor cells encounter stress, ranging from limited nutrient and oxygen supply within the tumor microenvironment to extrinsic and intrinsic oxidative stress. Thus, tumor cells seize regulatory pathways to rapidly adapt to distinct physiologic conditions to promote cellular survival, including manipulation of mRNA translation. While it is now well established that metastatic tumor cells must up-regulate their antioxidant capacity to effectively spread and that regulation of antioxidant enzymes is imperative to disease progression, relatively few studies have assessed how translation and the hijacking of RNA systems contribute to antioxidant responses of tumors. Here, we review the major stress signaling pathways involved in translational regulation and discuss how these are affected by oxidative stress to promote prosurvival changes that manipulate antioxidant enzyme expression. We describe how tumors elicit these adaptive responses and detail how stress-induced translation can be regulated by kinases, RNA-binding proteins, RNA species, and RNA modification systems. We also highlight opportunities for further studies focused on the role of mRNA translation and RNA systems in the regulation of antioxidant enzyme expression, which may be of particular importance in the context of metastatic progression and therapeutic resistance. |
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Thus, tumor cells seize regulatory pathways to rapidly adapt to distinct physiologic conditions to promote cellular survival, including manipulation of mRNA translation. While it is now well established that metastatic tumor cells must up-regulate their antioxidant capacity to effectively spread and that regulation of antioxidant enzymes is imperative to disease progression, relatively few studies have assessed how translation and the hijacking of RNA systems contribute to antioxidant responses of tumors. Here, we review the major stress signaling pathways involved in translational regulation and discuss how these are affected by oxidative stress to promote prosurvival changes that manipulate antioxidant enzyme expression. We describe how tumors elicit these adaptive responses and detail how stress-induced translation can be regulated by kinases, RNA-binding proteins, RNA species, and RNA modification systems. 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Published by PNAS. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c306t-ef064e7c6bd91a211e574dd603ef485c7cd0bcb32748343e0db20750fee5c0e03</cites><orcidid>0000-0002-9677-374X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39495917$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kim, Yeon Soo</creatorcontrib><creatorcontrib>Kimball, Scot R</creatorcontrib><creatorcontrib>Piskounova, Elena</creatorcontrib><creatorcontrib>Begley, Thomas J</creatorcontrib><creatorcontrib>Hempel, Nadine</creatorcontrib><title>Stress response regulation of mRNA translation: Implications for antioxidant enzyme expression in cancer</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>From tumorigenesis to advanced metastatic stages, tumor cells encounter stress, ranging from limited nutrient and oxygen supply within the tumor microenvironment to extrinsic and intrinsic oxidative stress. Thus, tumor cells seize regulatory pathways to rapidly adapt to distinct physiologic conditions to promote cellular survival, including manipulation of mRNA translation. While it is now well established that metastatic tumor cells must up-regulate their antioxidant capacity to effectively spread and that regulation of antioxidant enzymes is imperative to disease progression, relatively few studies have assessed how translation and the hijacking of RNA systems contribute to antioxidant responses of tumors. Here, we review the major stress signaling pathways involved in translational regulation and discuss how these are affected by oxidative stress to promote prosurvival changes that manipulate antioxidant enzyme expression. We describe how tumors elicit these adaptive responses and detail how stress-induced translation can be regulated by kinases, RNA-binding proteins, RNA species, and RNA modification systems. 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Kimball, Scot R ; Piskounova, Elena ; Begley, Thomas J ; Hempel, Nadine</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c306t-ef064e7c6bd91a211e574dd603ef485c7cd0bcb32748343e0db20750fee5c0e03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Antioxidants</topic><topic>Antioxidants - metabolism</topic><topic>Biological Sciences</topic><topic>Cell survival</topic><topic>Cellular stress response</topic><topic>Enzymes</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Humans</topic><topic>Kinases</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>mRNA</topic><topic>Neoplasms - genetics</topic><topic>Neoplasms - metabolism</topic><topic>Neoplasms - pathology</topic><topic>Oxidation resistance</topic><topic>Oxidative Stress</topic><topic>Protein Biosynthesis</topic><topic>RNA modification</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA-binding protein</topic><topic>Signal Transduction</topic><topic>Translation</topic><topic>Tumor cells</topic><topic>Tumor microenvironment</topic><topic>Tumorigenesis</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Yeon Soo</creatorcontrib><creatorcontrib>Kimball, Scot R</creatorcontrib><creatorcontrib>Piskounova, Elena</creatorcontrib><creatorcontrib>Begley, Thomas J</creatorcontrib><creatorcontrib>Hempel, Nadine</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kim, Yeon Soo</au><au>Kimball, Scot R</au><au>Piskounova, Elena</au><au>Begley, Thomas J</au><au>Hempel, Nadine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Stress response regulation of mRNA translation: Implications for antioxidant enzyme expression in cancer</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2024-11-12</date><risdate>2024</risdate><volume>121</volume><issue>46</issue><spage>e2317846121</spage><pages>e2317846121-</pages><issn>0027-8424</issn><issn>1091-6490</issn><eissn>1091-6490</eissn><abstract>From tumorigenesis to advanced metastatic stages, tumor cells encounter stress, ranging from limited nutrient and oxygen supply within the tumor microenvironment to extrinsic and intrinsic oxidative stress. 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subjects | Animals Antioxidants Antioxidants - metabolism Biological Sciences Cell survival Cellular stress response Enzymes Gene expression Gene Expression Regulation, Neoplastic Humans Kinases Metastases Metastasis mRNA Neoplasms - genetics Neoplasms - metabolism Neoplasms - pathology Oxidation resistance Oxidative Stress Protein Biosynthesis RNA modification RNA, Messenger - genetics RNA, Messenger - metabolism RNA-binding protein Signal Transduction Translation Tumor cells Tumor microenvironment Tumorigenesis Tumors |
title | Stress response regulation of mRNA translation: Implications for antioxidant enzyme expression in cancer |
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