Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages
Mycobacterium avium complex (MAC) is a non-tuberculous mycobacterium widely distributed in the environment. Even though MAC infection is increasing in older women and immunocompromised patients, to our knowledge there has been no comprehensive analysis of the MAC-infected host-cell transcriptome—and...
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Frontiers Media S.A.
2024-04-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1374437/full |
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| author | Mitsunori Yoshida Andrew Taejun Kwon Xian-Yang Qin Hajime Nishimura Shiori Maeda Yuji Miyamoto Yasuhiro Yoshida Yoshihiko Hoshino Harukazu Suzuki |
| author_facet | Mitsunori Yoshida Andrew Taejun Kwon Xian-Yang Qin Hajime Nishimura Shiori Maeda Yuji Miyamoto Yasuhiro Yoshida Yoshihiko Hoshino Harukazu Suzuki |
| author_sort | Mitsunori Yoshida |
| collection | DOAJ |
| description | Mycobacterium avium complex (MAC) is a non-tuberculous mycobacterium widely distributed in the environment. Even though MAC infection is increasing in older women and immunocompromised patients, to our knowledge there has been no comprehensive analysis of the MAC-infected host-cell transcriptome—and particularly of long non-coding RNAs (lncRNAs). By using in vitro-cultured primary mouse bone-marrow-derived macrophages (BMDMs) and Cap analysis of gene expression, we analyzed the transcriptional and kinetic landscape of macrophage genes, with a focus on lncRNAs, during MAC infection. MAC infection of macrophages induced the expression of immune/inflammatory response genes and other genes similar to those involved in M1 macrophage activation, consistent with previous reports, although Nos2 (M1 activation) and Arg1 (M2 activation) had distinct expression profiles. We identified 31 upregulated and 30 downregulated lncRNA promoters corresponding respectively to 18 and 26 lncRNAs. Upregulated lncRNAs were clustered into two groups—early and late upregulated—predicted to be associated with immune activation and the immune response to infection, respectively. Furthermore, an Ingenuity Pathway Analysis revealed canonical pathways and upstream transcription regulators associated with differentially expressed lncRNAs. Several differentially expressed lncRNAs reported elsewhere underwent expressional changes upon M1 or M2 preactivation and subsequent MAC infection. Finally, we showed that expressional change of lncRNAs in MAC-infected BMDMs was mediated by toll-like receptor 2, although there may be other mechanisms that sense MAC infection. We identified differentially expressed lncRNAs in MAC-infected BMDMs, revealing diverse features that imply the distinct roles of these lncRNAs in MAC infection and macrophage polarization. |
| first_indexed | 2024-04-24T07:04:30Z |
| format | Article |
| id | doaj.art-9cccf859784c4b5e801c6070707c53dc |
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| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-24T07:04:30Z |
| publishDate | 2024-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-9cccf859784c4b5e801c6070707c53dc2024-04-22T04:51:30ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-04-011510.3389/fimmu.2024.13744371374437Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophagesMitsunori Yoshida0Andrew Taejun Kwon1Xian-Yang Qin2Hajime Nishimura3Shiori Maeda4Yuji Miyamoto5Yasuhiro Yoshida6Yoshihiko Hoshino7Harukazu Suzuki8Department of Mycobacteriology, National Institute of Infectious Diseases, Higashi-Murayama, Tokyo, JapanLaboratory for Cellular Function Conversion Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, JapanLaboratory for Cellular Function Conversion Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, JapanLaboratory for Cellular Function Conversion Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, JapanLaboratory for Cellular Function Conversion Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, JapanDepartment of Mycobacteriology, National Institute of Infectious Diseases, Higashi-Murayama, Tokyo, JapanDepartment of Immunology and Parasitology, University of Occupational and Environmental Health, Kita-Kyushu, JapanDepartment of Mycobacteriology, National Institute of Infectious Diseases, Higashi-Murayama, Tokyo, JapanLaboratory for Cellular Function Conversion Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, JapanMycobacterium avium complex (MAC) is a non-tuberculous mycobacterium widely distributed in the environment. Even though MAC infection is increasing in older women and immunocompromised patients, to our knowledge there has been no comprehensive analysis of the MAC-infected host-cell transcriptome—and particularly of long non-coding RNAs (lncRNAs). By using in vitro-cultured primary mouse bone-marrow-derived macrophages (BMDMs) and Cap analysis of gene expression, we analyzed the transcriptional and kinetic landscape of macrophage genes, with a focus on lncRNAs, during MAC infection. MAC infection of macrophages induced the expression of immune/inflammatory response genes and other genes similar to those involved in M1 macrophage activation, consistent with previous reports, although Nos2 (M1 activation) and Arg1 (M2 activation) had distinct expression profiles. We identified 31 upregulated and 30 downregulated lncRNA promoters corresponding respectively to 18 and 26 lncRNAs. Upregulated lncRNAs were clustered into two groups—early and late upregulated—predicted to be associated with immune activation and the immune response to infection, respectively. Furthermore, an Ingenuity Pathway Analysis revealed canonical pathways and upstream transcription regulators associated with differentially expressed lncRNAs. Several differentially expressed lncRNAs reported elsewhere underwent expressional changes upon M1 or M2 preactivation and subsequent MAC infection. Finally, we showed that expressional change of lncRNAs in MAC-infected BMDMs was mediated by toll-like receptor 2, although there may be other mechanisms that sense MAC infection. We identified differentially expressed lncRNAs in MAC-infected BMDMs, revealing diverse features that imply the distinct roles of these lncRNAs in MAC infection and macrophage polarization.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1374437/fullnon-tuberculous mycobacterium (NTM)bone-marrow-derived macrophage (BMDM)cap analysis of gene expression (CAGE)long non-coding RNA (lncRNA)M1 or M2 macrophageIngenuity Pathway Analysis (IPA) |
| spellingShingle | Mitsunori Yoshida Andrew Taejun Kwon Xian-Yang Qin Hajime Nishimura Shiori Maeda Yuji Miyamoto Yasuhiro Yoshida Yoshihiko Hoshino Harukazu Suzuki Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages Frontiers in Immunology non-tuberculous mycobacterium (NTM) bone-marrow-derived macrophage (BMDM) cap analysis of gene expression (CAGE) long non-coding RNA (lncRNA) M1 or M2 macrophage Ingenuity Pathway Analysis (IPA) |
| title | Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages |
| title_full | Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages |
| title_fullStr | Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages |
| title_full_unstemmed | Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages |
| title_short | Transcriptome analysis of long non-coding RNAs in Mycobacterium avium complex–infected macrophages |
| title_sort | transcriptome analysis of long non coding rnas in mycobacterium avium complex infected macrophages |
| topic | non-tuberculous mycobacterium (NTM) bone-marrow-derived macrophage (BMDM) cap analysis of gene expression (CAGE) long non-coding RNA (lncRNA) M1 or M2 macrophage Ingenuity Pathway Analysis (IPA) |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1374437/full |
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