The non-canonical poly(A) polymerase FAM46C promotes erythropoiesis
The post-transcriptional regulation of mRNA is a crucial component of gene expression. The disruption of this process has detrimental effects on the normal development and gives rise to various diseases. Searching for novel post-transcriptional regulators and exploring their roles are essential for...
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| Veröffentlicht in: | Journal of genetics and genomics 2024-06, Vol.51 (6), p.594-607 |
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| container_title | Journal of genetics and genomics |
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| creator | Yang, Ke Zhu, Tianqi Yin, Jiaying Zhang, Qiaoli Li, Jing Fan, Hong Han, Gaijing Xu, Weiyin Liu, Nan Lv, Xiang |
| description | The post-transcriptional regulation of mRNA is a crucial component of gene expression. The disruption of this process has detrimental effects on the normal development and gives rise to various diseases. Searching for novel post-transcriptional regulators and exploring their roles are essential for understanding development and disease. Through a multimodal analysis of red blood cell trait genome-wide association studies (GWAS) and transcriptomes of erythropoiesis, we identify FAM46C, a non-canonical RNA poly(A) polymerase, as a necessary factor for proper red blood cell development. FAM46C is highly expressed in the late stages of the erythroid lineage, and its developmental upregulation is controlled by an erythroid-specific enhancer. We demonstrate that FAM46C stabilizes mRNA and regulates erythroid differentiation in a polymerase activity-dependent manner. Furthermore, we identify transcripts of lysosome and mitochondria components as highly confident in vivo targets of FAM46C, which aligns with the need of maturing red blood cells for substantial clearance of organelles and maintenance of cellular redox homeostasis. In conclusion, our study unveils a unique role of FAM46C in positively regulating lysosome and mitochondria components, thereby promoting erythropoiesis. |
| doi_str_mv | 10.1016/j.jgg.2024.02.003 |
| format | Article |
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The disruption of this process has detrimental effects on the normal development and gives rise to various diseases. Searching for novel post-transcriptional regulators and exploring their roles are essential for understanding development and disease. Through a multimodal analysis of red blood cell trait genome-wide association studies (GWAS) and transcriptomes of erythropoiesis, we identify FAM46C, a non-canonical RNA poly(A) polymerase, as a necessary factor for proper red blood cell development. FAM46C is highly expressed in the late stages of the erythroid lineage, and its developmental upregulation is controlled by an erythroid-specific enhancer. We demonstrate that FAM46C stabilizes mRNA and regulates erythroid differentiation in a polymerase activity-dependent manner. Furthermore, we identify transcripts of lysosome and mitochondria components as highly confident in vivo targets of FAM46C, which aligns with the need of maturing red blood cells for substantial clearance of organelles and maintenance of cellular redox homeostasis. In conclusion, our study unveils a unique role of FAM46C in positively regulating lysosome and mitochondria components, thereby promoting erythropoiesis.</description><identifier>ISSN: 1673-8527</identifier><identifier>DOI: 10.1016/j.jgg.2024.02.003</identifier><identifier>PMID: 38403115</identifier><language>eng</language><publisher>China: Elsevier Ltd</publisher><subject>Animals ; Cell Differentiation - genetics ; Erythroblasts ; Erythrocytes - metabolism ; Erythroid-specific enhancer ; Erythropoiesis - genetics ; FAM46C ; Genome-Wide Association Study ; Humans ; Lysosomes - genetics ; Lysosomes - metabolism ; Mice ; Mitochondria - genetics ; Mitochondria - metabolism ; Poly(A) polymerase ; Polynucleotide Adenylyltransferase - genetics ; Polynucleotide Adenylyltransferase - metabolism ; Post-transcriptional regulation ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; TENT5C ; Transcriptome - genetics</subject><ispartof>Journal of genetics and genomics, 2024-06, Vol.51 (6), p.594-607</ispartof><rights>2024 Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China</rights><rights>Copyright © 2024 Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China. Published by Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c305t-6e6dabf31f5685070723718c208505f2ecbf56dedc8bcd344f7008fb77fb5f363</cites><orcidid>0000-0002-8314-0900 ; 0000-0002-2938-5624</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.jgg.2024.02.003$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38403115$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Ke</creatorcontrib><creatorcontrib>Zhu, Tianqi</creatorcontrib><creatorcontrib>Yin, Jiaying</creatorcontrib><creatorcontrib>Zhang, Qiaoli</creatorcontrib><creatorcontrib>Li, Jing</creatorcontrib><creatorcontrib>Fan, Hong</creatorcontrib><creatorcontrib>Han, Gaijing</creatorcontrib><creatorcontrib>Xu, Weiyin</creatorcontrib><creatorcontrib>Liu, Nan</creatorcontrib><creatorcontrib>Lv, Xiang</creatorcontrib><title>The non-canonical poly(A) polymerase FAM46C promotes erythropoiesis</title><title>Journal of genetics and genomics</title><addtitle>J Genet Genomics</addtitle><description>The post-transcriptional regulation of mRNA is a crucial component of gene expression. The disruption of this process has detrimental effects on the normal development and gives rise to various diseases. Searching for novel post-transcriptional regulators and exploring their roles are essential for understanding development and disease. Through a multimodal analysis of red blood cell trait genome-wide association studies (GWAS) and transcriptomes of erythropoiesis, we identify FAM46C, a non-canonical RNA poly(A) polymerase, as a necessary factor for proper red blood cell development. FAM46C is highly expressed in the late stages of the erythroid lineage, and its developmental upregulation is controlled by an erythroid-specific enhancer. We demonstrate that FAM46C stabilizes mRNA and regulates erythroid differentiation in a polymerase activity-dependent manner. Furthermore, we identify transcripts of lysosome and mitochondria components as highly confident in vivo targets of FAM46C, which aligns with the need of maturing red blood cells for substantial clearance of organelles and maintenance of cellular redox homeostasis. In conclusion, our study unveils a unique role of FAM46C in positively regulating lysosome and mitochondria components, thereby promoting erythropoiesis.</description><subject>Animals</subject><subject>Cell Differentiation - genetics</subject><subject>Erythroblasts</subject><subject>Erythrocytes - metabolism</subject><subject>Erythroid-specific enhancer</subject><subject>Erythropoiesis - genetics</subject><subject>FAM46C</subject><subject>Genome-Wide Association Study</subject><subject>Humans</subject><subject>Lysosomes - genetics</subject><subject>Lysosomes - metabolism</subject><subject>Mice</subject><subject>Mitochondria - genetics</subject><subject>Mitochondria - metabolism</subject><subject>Poly(A) polymerase</subject><subject>Polynucleotide Adenylyltransferase - genetics</subject><subject>Polynucleotide Adenylyltransferase - metabolism</subject><subject>Post-transcriptional regulation</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>TENT5C</subject><subject>Transcriptome - genetics</subject><issn>1673-8527</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kDFPwzAQhT2AaCn8ABaUEYaEsx0nqZiqigJSEUuZrcQ5t46SuNgpUv89Li2MLPd0undPdx8hNxQSCjR7aJJmvU4YsDQBlgDwMzKmWc7jQrB8RC69bwBEMaXigox4kQKnVIzJfLXBqLd9rMpQjSrbaGvb_d3s_kc7dKXHaDF7S7N5tHW2swP6CN1-2Di7tQa98VfkXJetx-uTTsjH4mk1f4mX78-v89kyVhzEEGeY1WWlOdUiKwTkkDOe00IxCJ3QDFUVJjXWqqhUzdNU5wCFrvJcV0LzjE_I3TE33PG5Qz_IzniFbVv2aHdesilnQAsWdELo0aqc9d6hlltnutLtJQV54CUbGXjJAy8JTAZeYef2FL-rOqz_Nn5hBcPj0YDhyS-DTnplsFdYG4dqkLU1_8R_AwyLfC8</recordid><startdate>20240601</startdate><enddate>20240601</enddate><creator>Yang, Ke</creator><creator>Zhu, Tianqi</creator><creator>Yin, Jiaying</creator><creator>Zhang, Qiaoli</creator><creator>Li, Jing</creator><creator>Fan, Hong</creator><creator>Han, Gaijing</creator><creator>Xu, Weiyin</creator><creator>Liu, Nan</creator><creator>Lv, Xiang</creator><general>Elsevier Ltd</general><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><orcidid>https://orcid.org/0000-0002-8314-0900</orcidid><orcidid>https://orcid.org/0000-0002-2938-5624</orcidid></search><sort><creationdate>20240601</creationdate><title>The non-canonical poly(A) polymerase FAM46C promotes erythropoiesis</title><author>Yang, Ke ; 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The disruption of this process has detrimental effects on the normal development and gives rise to various diseases. Searching for novel post-transcriptional regulators and exploring their roles are essential for understanding development and disease. Through a multimodal analysis of red blood cell trait genome-wide association studies (GWAS) and transcriptomes of erythropoiesis, we identify FAM46C, a non-canonical RNA poly(A) polymerase, as a necessary factor for proper red blood cell development. FAM46C is highly expressed in the late stages of the erythroid lineage, and its developmental upregulation is controlled by an erythroid-specific enhancer. We demonstrate that FAM46C stabilizes mRNA and regulates erythroid differentiation in a polymerase activity-dependent manner. Furthermore, we identify transcripts of lysosome and mitochondria components as highly confident in vivo targets of FAM46C, which aligns with the need of maturing red blood cells for substantial clearance of organelles and maintenance of cellular redox homeostasis. In conclusion, our study unveils a unique role of FAM46C in positively regulating lysosome and mitochondria components, thereby promoting erythropoiesis.</abstract><cop>China</cop><pub>Elsevier Ltd</pub><pmid>38403115</pmid><doi>10.1016/j.jgg.2024.02.003</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-8314-0900</orcidid><orcidid>https://orcid.org/0000-0002-2938-5624</orcidid></addata></record> |
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| subjects | Animals Cell Differentiation - genetics Erythroblasts Erythrocytes - metabolism Erythroid-specific enhancer Erythropoiesis - genetics FAM46C Genome-Wide Association Study Humans Lysosomes - genetics Lysosomes - metabolism Mice Mitochondria - genetics Mitochondria - metabolism Poly(A) polymerase Polynucleotide Adenylyltransferase - genetics Polynucleotide Adenylyltransferase - metabolism Post-transcriptional regulation RNA, Messenger - genetics RNA, Messenger - metabolism TENT5C Transcriptome - genetics |
| title | The non-canonical poly(A) polymerase FAM46C promotes erythropoiesis |
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