Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level
The regulation of inflammatory responses is an important intervention in biological function and macrophages play an essential role during inflammation. Skeletal muscle is the largest organ in the human body and releases various factors which mediate anti-inflammatory/immune modulatory effects. Rece...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2023-12-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/89512 |
| _version_ | 1797402904687017984 |
|---|---|
| author | Atomu Yamaguchi Noriaki Maeshige Hikari Noguchi Jiawei Yan Xiaoqi Ma Mikiko Uemura Dongming Su Hiroyo Kondo Kristopher Sarosiek Hidemi Fujino |
| author_facet | Atomu Yamaguchi Noriaki Maeshige Hikari Noguchi Jiawei Yan Xiaoqi Ma Mikiko Uemura Dongming Su Hiroyo Kondo Kristopher Sarosiek Hidemi Fujino |
| author_sort | Atomu Yamaguchi |
| collection | DOAJ |
| description | The regulation of inflammatory responses is an important intervention in biological function and macrophages play an essential role during inflammation. Skeletal muscle is the largest organ in the human body and releases various factors which mediate anti-inflammatory/immune modulatory effects. Recently, the roles of extracellular vesicles (EVs) from a large variety of cells are reported. In particular, EVs released from skeletal muscle are attracting attention due to their therapeutic effects on dysfunctional organs and tissues. Also, ultrasound (US) promotes release of EVs from skeletal muscle. In this study, we investigated the output parameters and mechanisms of US-induced EV release enhancement and the potential of US-treated skeletal muscle-derived EVs in the regulation of inflammatory responses in macrophages. High-intensity US (3.0 W/cm2) irradiation increased EV secretion from C2C12 murine muscle cells via elevating intracellular Ca2+ level without negative effects. Moreover, US-induced EVs suppressed expression levels of pro-inflammatory factors in macrophages. miRNA sequencing analysis revealed that miR-206-3p and miR-378a-3p were especially abundant in skeletal myotube-derived EVs. In this study we demonstrated that high-intensity US promotes the release of anti-inflammatory EVs from skeletal myotubes and exert anti-inflammatory effects on macrophages. |
| first_indexed | 2024-03-09T02:30:53Z |
| format | Article |
| id | doaj.art-bca3f47080eb42c49f01e2c27f4fda4a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-09T02:30:53Z |
| publishDate | 2023-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-bca3f47080eb42c49f01e2c27f4fda4a2023-12-06T13:01:35ZengeLife Sciences Publications LtdeLife2050-084X2023-12-011210.7554/eLife.89512Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium levelAtomu Yamaguchi0Noriaki Maeshige1https://orcid.org/0000-0002-3573-347XHikari Noguchi2Jiawei Yan3Xiaoqi Ma4Mikiko Uemura5Dongming Su6Hiroyo Kondo7Kristopher Sarosiek8Hidemi Fujino9Department of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Kobe, JapanDepartment of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Kobe, JapanDepartment of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Kobe, JapanSchool of Life Sciences and Technology, ShanghaiTech University, Shanghai, ChinaDepartment of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Kobe, JapanDepartment of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Kobe, JapanDepartment of Pathology, Nanjing Medical University, Nanjing, ChinaDepartment of Health and Nutrition , Shubun University, Ichinomiya, JapanJohn B. Little Center for Radiation Sciences, Harvard University T.H. Chan School of Public Health, Boston, United StatesDepartment of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Kobe, JapanThe regulation of inflammatory responses is an important intervention in biological function and macrophages play an essential role during inflammation. Skeletal muscle is the largest organ in the human body and releases various factors which mediate anti-inflammatory/immune modulatory effects. Recently, the roles of extracellular vesicles (EVs) from a large variety of cells are reported. In particular, EVs released from skeletal muscle are attracting attention due to their therapeutic effects on dysfunctional organs and tissues. Also, ultrasound (US) promotes release of EVs from skeletal muscle. In this study, we investigated the output parameters and mechanisms of US-induced EV release enhancement and the potential of US-treated skeletal muscle-derived EVs in the regulation of inflammatory responses in macrophages. High-intensity US (3.0 W/cm2) irradiation increased EV secretion from C2C12 murine muscle cells via elevating intracellular Ca2+ level without negative effects. Moreover, US-induced EVs suppressed expression levels of pro-inflammatory factors in macrophages. miRNA sequencing analysis revealed that miR-206-3p and miR-378a-3p were especially abundant in skeletal myotube-derived EVs. In this study we demonstrated that high-intensity US promotes the release of anti-inflammatory EVs from skeletal myotubes and exert anti-inflammatory effects on macrophages.https://elifesciences.org/articles/89512extracellular vesiclesskeletal musclesultrasoundmacrophagesinflammation |
| spellingShingle | Atomu Yamaguchi Noriaki Maeshige Hikari Noguchi Jiawei Yan Xiaoqi Ma Mikiko Uemura Dongming Su Hiroyo Kondo Kristopher Sarosiek Hidemi Fujino Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level eLife extracellular vesicles skeletal muscles ultrasound macrophages inflammation |
| title | Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level |
| title_full | Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level |
| title_fullStr | Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level |
| title_full_unstemmed | Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level |
| title_short | Pulsed ultrasound promotes secretion of anti-inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level |
| title_sort | pulsed ultrasound promotes secretion of anti inflammatory extracellular vesicles from skeletal myotubes via elevation of intracellular calcium level |
| topic | extracellular vesicles skeletal muscles ultrasound macrophages inflammation |
| url | https://elifesciences.org/articles/89512 |
| work_keys_str_mv | AT atomuyamaguchi pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT noriakimaeshige pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT hikarinoguchi pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT jiaweiyan pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT xiaoqima pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT mikikouemura pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT dongmingsu pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT hiroyokondo pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT kristophersarosiek pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel AT hidemifujino pulsedultrasoundpromotessecretionofantiinflammatoryextracellularvesiclesfromskeletalmyotubesviaelevationofintracellularcalciumlevel |