Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development
There is a growing body of evidence supporting the significant impact of microbiota on heart development. Alternative polyadenylation (APA) is a crucial mechanism for gene expression regulation and has been implicated in postnatal heart development. Nonetheless, whether microbiota can influence post...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2023.1310409/full |
| _version_ | 1827383245302398976 |
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| author | Xiang Liu Xiang Liu Yijia Shao Linjiang Han Linjiang Han Yuanting Zhu Yuanting Zhu Jiazichao Tu Jiazichao Tu Jianrui Ma Jianrui Ma Ruyue Zhang Ruyue Zhang Zhen Yang Jimei Chen Jimei Chen |
| author_facet | Xiang Liu Xiang Liu Yijia Shao Linjiang Han Linjiang Han Yuanting Zhu Yuanting Zhu Jiazichao Tu Jiazichao Tu Jianrui Ma Jianrui Ma Ruyue Zhang Ruyue Zhang Zhen Yang Jimei Chen Jimei Chen |
| author_sort | Xiang Liu |
| collection | DOAJ |
| description | There is a growing body of evidence supporting the significant impact of microbiota on heart development. Alternative polyadenylation (APA) is a crucial mechanism for gene expression regulation and has been implicated in postnatal heart development. Nonetheless, whether microbiota can influence postnatal heart development through the regulation of APA remains unclear. Therefore, we conducted APA sequencing on heart tissues collected from specific pathogen-free (SPF) mice and germ-free (GF) mice at three different developmental stages: within the first 24 h after birth (P1), 7-day-old SPF mice, and 7-day-old GF mice. This approach allowed us to obtain a comprehensive genome-wide profile of APA sites in the heart tissue samples. In this study, we made a significant observation that GF mice exhibited noticeably longer 3ʹ untranslated region (3ʹ UTR) lengths. Furthermore, we confirmed significant alterations in the 3ʹ UTR lengths of mitochondria-related genes, namely Rala, Timm13, and Uqcc3. Interestingly, the GF condition resulted in a marked decrease in mitochondrial cristae density and a reduction in the level of Tomm20 in postnatal hearts. Moreover, we discovered a connection between Rala and Src, which further implicated their association with other differentially expressed genes (DEGs). Notably, most of the DEGs were significantly downregulated in GF mice, with the exceptions being Thbs1 and Egr1. Importantly, the GF condition demonstrated a correlation with a lower infiltration of immune cells, whereby the levels of resting NK cells, Th17 cells, immature dendritic cells, and plasma cells in GF mice were comparable to those observed in P1 mice. Furthermore, we established significant correlations between these immune cells and Rala as well as the related DEGs. Our findings clearly indicated that microbiota plays a vital role in postnatal heart development by affecting APA switching, mitochondria and immune cell infiltrations. |
| first_indexed | 2024-03-08T14:37:24Z |
| format | Article |
| id | doaj.art-8ec6b8d0030a45c6b63b841f81f5c6d8 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-03-08T14:37:24Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-8ec6b8d0030a45c6b63b841f81f5c6d82024-01-12T04:16:24ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2024-01-011110.3389/fcell.2023.13104091310409Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart developmentXiang Liu0Xiang Liu1Yijia Shao2Linjiang Han3Linjiang Han4Yuanting Zhu5Yuanting Zhu6Jiazichao Tu7Jiazichao Tu8Jianrui Ma9Jianrui Ma10Ruyue Zhang11Ruyue Zhang12Zhen Yang13Jimei Chen14Jimei Chen15Department of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangzhou, ChinaDepartment of Geriatrics, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDepartment of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangzhou, ChinaDepartment of Emergency Medicine, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDepartment of Cardiology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDepartment of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangzhou, ChinaDepartment of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangzhou, ChinaDepartment of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangzhou, ChinaDepartment of Emergency Medicine, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDepartment of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangzhou, ChinaThere is a growing body of evidence supporting the significant impact of microbiota on heart development. Alternative polyadenylation (APA) is a crucial mechanism for gene expression regulation and has been implicated in postnatal heart development. Nonetheless, whether microbiota can influence postnatal heart development through the regulation of APA remains unclear. Therefore, we conducted APA sequencing on heart tissues collected from specific pathogen-free (SPF) mice and germ-free (GF) mice at three different developmental stages: within the first 24 h after birth (P1), 7-day-old SPF mice, and 7-day-old GF mice. This approach allowed us to obtain a comprehensive genome-wide profile of APA sites in the heart tissue samples. In this study, we made a significant observation that GF mice exhibited noticeably longer 3ʹ untranslated region (3ʹ UTR) lengths. Furthermore, we confirmed significant alterations in the 3ʹ UTR lengths of mitochondria-related genes, namely Rala, Timm13, and Uqcc3. Interestingly, the GF condition resulted in a marked decrease in mitochondrial cristae density and a reduction in the level of Tomm20 in postnatal hearts. Moreover, we discovered a connection between Rala and Src, which further implicated their association with other differentially expressed genes (DEGs). Notably, most of the DEGs were significantly downregulated in GF mice, with the exceptions being Thbs1 and Egr1. Importantly, the GF condition demonstrated a correlation with a lower infiltration of immune cells, whereby the levels of resting NK cells, Th17 cells, immature dendritic cells, and plasma cells in GF mice were comparable to those observed in P1 mice. Furthermore, we established significant correlations between these immune cells and Rala as well as the related DEGs. Our findings clearly indicated that microbiota plays a vital role in postnatal heart development by affecting APA switching, mitochondria and immune cell infiltrations.https://www.frontiersin.org/articles/10.3389/fcell.2023.1310409/fullmicrobiotaheart developmentalternative polyadenylationmitochondrionimmune cell |
| spellingShingle | Xiang Liu Xiang Liu Yijia Shao Linjiang Han Linjiang Han Yuanting Zhu Yuanting Zhu Jiazichao Tu Jiazichao Tu Jianrui Ma Jianrui Ma Ruyue Zhang Ruyue Zhang Zhen Yang Jimei Chen Jimei Chen Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development Frontiers in Cell and Developmental Biology microbiota heart development alternative polyadenylation mitochondrion immune cell |
| title | Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development |
| title_full | Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development |
| title_fullStr | Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development |
| title_full_unstemmed | Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development |
| title_short | Microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development |
| title_sort | microbiota affects mitochondria and immune cell infiltrations via alternative polyadenylation during postnatal heart development |
| topic | microbiota heart development alternative polyadenylation mitochondrion immune cell |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2023.1310409/full |
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