Endoplasmic reticulum mediates mitochondrial transfer within the osteocyte dendritic network
Mitochondrial transfer plays a crucial role in the regulation of tissue homeostasis and resistance to cancer chemotherapy. Osteocytes have interconnecting dendritic networks and are a model to investigate its mechanism. We have demonstrated, in primary murine osteocytes with photoactivatable mitocho...
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| Veröffentlicht in: | Science advances 2019-11, Vol.5 (11), p.eaaw7215-eaaw7215 |
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| creator | Gao, Junjie Qin, An Liu, Delin Ruan, Rui Wang, Qiyang Yuan, Jun Cheng, Tak Sum Filipovska, Aleksandra Papadimitriou, J M Dai, Kerong Jiang, Qing Gao, Xiang Feng, Jian Q Takayanagi, Hiroshi Zhang, Changqing Zheng, Ming H |
| description | Mitochondrial transfer plays a crucial role in the regulation of tissue homeostasis and resistance to cancer chemotherapy. Osteocytes have interconnecting dendritic networks and are a model to investigate its mechanism. We have demonstrated, in primary murine osteocytes with photoactivatable mitochondria (PhAM)
and in MLO-Y4 cells, mitochondrial transfer in the dendritic networks visualized by high-resolution confocal imaging. Normal osteocytes transferred mitochondria to adjacent metabolically stressed osteocytes and restored their metabolic function. The coordinated movement and transfer of mitochondria within the dendritic network rely on contact between the endoplasmic reticulum (ER) and mitochondria. Mitofusin 2 (Mfn2), a GTPase that tethers ER to mitochondria, predominantly mediates the transfer. A decline in Mfn2 expression with age occurs concomitantly with both impaired mitochondrial distribution and transfer in the osteocyte dendritic network. These data show a previously unknown function of ER-mitochondrial contact in mediating mitochondrial transfer and provide a mechanism to explain the homeostasis of osteocytes. |
| doi_str_mv | 10.1126/sciadv.aaw7215 |
| format | Article |
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and in MLO-Y4 cells, mitochondrial transfer in the dendritic networks visualized by high-resolution confocal imaging. Normal osteocytes transferred mitochondria to adjacent metabolically stressed osteocytes and restored their metabolic function. The coordinated movement and transfer of mitochondria within the dendritic network rely on contact between the endoplasmic reticulum (ER) and mitochondria. Mitofusin 2 (Mfn2), a GTPase that tethers ER to mitochondria, predominantly mediates the transfer. A decline in Mfn2 expression with age occurs concomitantly with both impaired mitochondrial distribution and transfer in the osteocyte dendritic network. These data show a previously unknown function of ER-mitochondrial contact in mediating mitochondrial transfer and provide a mechanism to explain the homeostasis of osteocytes.</description><identifier>ISSN: 2375-2548</identifier><identifier>EISSN: 2375-2548</identifier><identifier>DOI: 10.1126/sciadv.aaw7215</identifier><identifier>PMID: 31799389</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Animals ; Cell Biology ; Cell Line ; Endoplasmic Reticulum - metabolism ; GTP Phosphohydrolases - metabolism ; Homeostasis - physiology ; Mice ; Mice, Knockout ; Microscopy, Confocal ; Mitochondria - metabolism ; Osteocytes - metabolism ; SciAdv r-articles</subject><ispartof>Science advances, 2019-11, Vol.5 (11), p.eaaw7215-eaaw7215</ispartof><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).</rights><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). 2019 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c456t-3a23ee3f8a3123081af6c2e8e69e1620663513e3abf1fd4badb30e551a969823</citedby><cites>FETCH-LOGICAL-c456t-3a23ee3f8a3123081af6c2e8e69e1620663513e3abf1fd4badb30e551a969823</cites><orcidid>0000-0002-3054-4207 ; 0000-0003-4820-8524 ; 0000-0002-3424-5909 ; 0000-0003-4947-3071 ; 0000-0002-7408-4126 ; 0000-0002-2552-9686 ; 0000-0001-6542-4654 ; 0000-0002-6998-8403 ; 0000-0002-1462-4127 ; 0000-0002-7326-2277 ; 0000-0003-1185-4768</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6867880/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6867880/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31799389$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gao, Junjie</creatorcontrib><creatorcontrib>Qin, An</creatorcontrib><creatorcontrib>Liu, Delin</creatorcontrib><creatorcontrib>Ruan, Rui</creatorcontrib><creatorcontrib>Wang, Qiyang</creatorcontrib><creatorcontrib>Yuan, Jun</creatorcontrib><creatorcontrib>Cheng, Tak Sum</creatorcontrib><creatorcontrib>Filipovska, Aleksandra</creatorcontrib><creatorcontrib>Papadimitriou, J M</creatorcontrib><creatorcontrib>Dai, Kerong</creatorcontrib><creatorcontrib>Jiang, Qing</creatorcontrib><creatorcontrib>Gao, Xiang</creatorcontrib><creatorcontrib>Feng, Jian Q</creatorcontrib><creatorcontrib>Takayanagi, Hiroshi</creatorcontrib><creatorcontrib>Zhang, Changqing</creatorcontrib><creatorcontrib>Zheng, Ming H</creatorcontrib><title>Endoplasmic reticulum mediates mitochondrial transfer within the osteocyte dendritic network</title><title>Science advances</title><addtitle>Sci Adv</addtitle><description>Mitochondrial transfer plays a crucial role in the regulation of tissue homeostasis and resistance to cancer chemotherapy. Osteocytes have interconnecting dendritic networks and are a model to investigate its mechanism. We have demonstrated, in primary murine osteocytes with photoactivatable mitochondria (PhAM)
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These data show a previously unknown function of ER-mitochondrial contact in mediating mitochondrial transfer and provide a mechanism to explain the homeostasis of osteocytes.</description><subject>Animals</subject><subject>Cell Biology</subject><subject>Cell Line</subject><subject>Endoplasmic Reticulum - metabolism</subject><subject>GTP Phosphohydrolases - metabolism</subject><subject>Homeostasis - physiology</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Microscopy, Confocal</subject><subject>Mitochondria - metabolism</subject><subject>Osteocytes - metabolism</subject><subject>SciAdv r-articles</subject><issn>2375-2548</issn><issn>2375-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkc1LAzEQxYMottRePUqOXlrz0U2zF0GKXyB46VEIs9lZG93d1CRr6X_vllappxmYN795zCPkkrMp50LdROug_J4CbOaCZydkKOQ8m4hspk-P-gEZx_jBGOMzpTKen5OB5PM8lzofkrf7tvTrGmLjLA2YnO3qrqENlg4SRtq45O3Kt2VwUNMUoI0VBrpxaeVamlZIfUzo7TYhLXEn6xG0xbTx4fOCnFVQRxwf6ogsH-6Xi6fJy-vj8-LuZWJnmUoTCUIiykqD5EIyzaFSVqBGlSNXgiklMy5RQlHxqpwVUBaSYZZxyFWuhRyR2z123RW9cYtt77M26-AaCFvjwZn_k9atzLv_NkqrudasB1wfAMF_dRiTaVy0WNfQou-iEVLw_nVC5710upfa4GMMWP2d4czsQjH7UMwhlH7h6tjcn_w3AvkDlSWNvA</recordid><startdate>20191101</startdate><enddate>20191101</enddate><creator>Gao, Junjie</creator><creator>Qin, An</creator><creator>Liu, Delin</creator><creator>Ruan, Rui</creator><creator>Wang, Qiyang</creator><creator>Yuan, Jun</creator><creator>Cheng, Tak Sum</creator><creator>Filipovska, Aleksandra</creator><creator>Papadimitriou, J M</creator><creator>Dai, Kerong</creator><creator>Jiang, Qing</creator><creator>Gao, Xiang</creator><creator>Feng, Jian Q</creator><creator>Takayanagi, Hiroshi</creator><creator>Zhang, Changqing</creator><creator>Zheng, Ming H</creator><general>American Association for the Advancement of Science</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><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3054-4207</orcidid><orcidid>https://orcid.org/0000-0003-4820-8524</orcidid><orcidid>https://orcid.org/0000-0002-3424-5909</orcidid><orcidid>https://orcid.org/0000-0003-4947-3071</orcidid><orcidid>https://orcid.org/0000-0002-7408-4126</orcidid><orcidid>https://orcid.org/0000-0002-2552-9686</orcidid><orcidid>https://orcid.org/0000-0001-6542-4654</orcidid><orcidid>https://orcid.org/0000-0002-6998-8403</orcidid><orcidid>https://orcid.org/0000-0002-1462-4127</orcidid><orcidid>https://orcid.org/0000-0002-7326-2277</orcidid><orcidid>https://orcid.org/0000-0003-1185-4768</orcidid></search><sort><creationdate>20191101</creationdate><title>Endoplasmic reticulum mediates mitochondrial transfer within the osteocyte dendritic network</title><author>Gao, Junjie ; Qin, An ; Liu, Delin ; Ruan, Rui ; Wang, Qiyang ; Yuan, Jun ; Cheng, Tak Sum ; Filipovska, Aleksandra ; Papadimitriou, J M ; Dai, Kerong ; Jiang, Qing ; Gao, Xiang ; Feng, Jian Q ; Takayanagi, Hiroshi ; Zhang, Changqing ; Zheng, Ming H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c456t-3a23ee3f8a3123081af6c2e8e69e1620663513e3abf1fd4badb30e551a969823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Cell Biology</topic><topic>Cell Line</topic><topic>Endoplasmic Reticulum - metabolism</topic><topic>GTP Phosphohydrolases - metabolism</topic><topic>Homeostasis - physiology</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Microscopy, Confocal</topic><topic>Mitochondria - metabolism</topic><topic>Osteocytes - metabolism</topic><topic>SciAdv r-articles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gao, Junjie</creatorcontrib><creatorcontrib>Qin, An</creatorcontrib><creatorcontrib>Liu, Delin</creatorcontrib><creatorcontrib>Ruan, Rui</creatorcontrib><creatorcontrib>Wang, Qiyang</creatorcontrib><creatorcontrib>Yuan, Jun</creatorcontrib><creatorcontrib>Cheng, Tak Sum</creatorcontrib><creatorcontrib>Filipovska, Aleksandra</creatorcontrib><creatorcontrib>Papadimitriou, J M</creatorcontrib><creatorcontrib>Dai, Kerong</creatorcontrib><creatorcontrib>Jiang, Qing</creatorcontrib><creatorcontrib>Gao, Xiang</creatorcontrib><creatorcontrib>Feng, Jian Q</creatorcontrib><creatorcontrib>Takayanagi, Hiroshi</creatorcontrib><creatorcontrib>Zhang, Changqing</creatorcontrib><creatorcontrib>Zheng, Ming H</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science advances</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gao, Junjie</au><au>Qin, An</au><au>Liu, Delin</au><au>Ruan, Rui</au><au>Wang, Qiyang</au><au>Yuan, Jun</au><au>Cheng, Tak Sum</au><au>Filipovska, Aleksandra</au><au>Papadimitriou, J M</au><au>Dai, Kerong</au><au>Jiang, Qing</au><au>Gao, Xiang</au><au>Feng, Jian Q</au><au>Takayanagi, Hiroshi</au><au>Zhang, Changqing</au><au>Zheng, Ming H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Endoplasmic reticulum mediates mitochondrial transfer within the osteocyte dendritic network</atitle><jtitle>Science advances</jtitle><addtitle>Sci Adv</addtitle><date>2019-11-01</date><risdate>2019</risdate><volume>5</volume><issue>11</issue><spage>eaaw7215</spage><epage>eaaw7215</epage><pages>eaaw7215-eaaw7215</pages><issn>2375-2548</issn><eissn>2375-2548</eissn><abstract>Mitochondrial transfer plays a crucial role in the regulation of tissue homeostasis and resistance to cancer chemotherapy. Osteocytes have interconnecting dendritic networks and are a model to investigate its mechanism. We have demonstrated, in primary murine osteocytes with photoactivatable mitochondria (PhAM)
and in MLO-Y4 cells, mitochondrial transfer in the dendritic networks visualized by high-resolution confocal imaging. Normal osteocytes transferred mitochondria to adjacent metabolically stressed osteocytes and restored their metabolic function. The coordinated movement and transfer of mitochondria within the dendritic network rely on contact between the endoplasmic reticulum (ER) and mitochondria. Mitofusin 2 (Mfn2), a GTPase that tethers ER to mitochondria, predominantly mediates the transfer. A decline in Mfn2 expression with age occurs concomitantly with both impaired mitochondrial distribution and transfer in the osteocyte dendritic network. These data show a previously unknown function of ER-mitochondrial contact in mediating mitochondrial transfer and provide a mechanism to explain the homeostasis of osteocytes.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>31799389</pmid><doi>10.1126/sciadv.aaw7215</doi><orcidid>https://orcid.org/0000-0002-3054-4207</orcidid><orcidid>https://orcid.org/0000-0003-4820-8524</orcidid><orcidid>https://orcid.org/0000-0002-3424-5909</orcidid><orcidid>https://orcid.org/0000-0003-4947-3071</orcidid><orcidid>https://orcid.org/0000-0002-7408-4126</orcidid><orcidid>https://orcid.org/0000-0002-2552-9686</orcidid><orcidid>https://orcid.org/0000-0001-6542-4654</orcidid><orcidid>https://orcid.org/0000-0002-6998-8403</orcidid><orcidid>https://orcid.org/0000-0002-1462-4127</orcidid><orcidid>https://orcid.org/0000-0002-7326-2277</orcidid><orcidid>https://orcid.org/0000-0003-1185-4768</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Cell Biology Cell Line Endoplasmic Reticulum - metabolism GTP Phosphohydrolases - metabolism Homeostasis - physiology Mice Mice, Knockout Microscopy, Confocal Mitochondria - metabolism Osteocytes - metabolism SciAdv r-articles |
| title | Endoplasmic reticulum mediates mitochondrial transfer within the osteocyte dendritic network |
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