Distribution of microglia/immune cells in the brain of adult zebrafish in homeostatic and regenerative conditions: Focus on oxidative stress during brain repair
Microglia are macrophage‐like cells exerting determinant roles in neuroinflammatory and oxidative stress processes during brain regeneration. We used zebrafish as a model of brain plasticity and repair. First, by performing L‐plastin (Lcp1) immunohistochemistry and using transgenic Tg(mpeg1.1:GFP) o...
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| Veröffentlicht in: | Journal of comparative neurology (1911) 2023-02, Vol.531 (2), p.238-255 |
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| container_title | Journal of comparative neurology (1911) |
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| creator | Narra, Sai Sandhya Rondeau, Philippe Fernezelian, Danielle Gence, Laura Ghaddar, Batoul Bourdon, Emmanuel Lefebvre d'Hellencourt, Christian Rastegar, Sepand Diotel, Nicolas |
| description | Microglia are macrophage‐like cells exerting determinant roles in neuroinflammatory and oxidative stress processes during brain regeneration. We used zebrafish as a model of brain plasticity and repair. First, by performing L‐plastin (Lcp1) immunohistochemistry and using transgenic Tg(mpeg1.1:GFP) or Tg(mpeg1.1:mCherry) fish, we analyzed the distribution of microglia/immune cells in the whole brain. Specific regional differences were evidenced in terms of microglia/immune cell density and morphology (elongated, branched, highly branched, and amoeboid). Taking advantage of Tg(fli:GFP) and Tg(GFAP::GFP) enabling the detection of endothelial cells and neural stem cells (NSCs), we highlighted the association of elongated microglia/immune cells with blood vessels and rounded/amoeboid microglia with NSCs. Second, after telencephalic injury, we showed that L‐plastin cells were still abundantly present at 5 days post‐lesion (dpl) and were associated with regenerative neurogenesis. Finally, RNA‐sequencing analysis from injured telencephalon (5 dpl) confirmed the upregulation of microglia/immune cell markers and highlighted a significant increase of genes involved in oxidative stress (nox2, nrf2a, and gsr). The analysis of antioxidant activities at 5 dpl also revealed an upregulation of superoxide dismutase and persistent H2O2 generation in the injured telencephalon. Also, microglia/immune cells were shown to be a source of oxidative stress at 5 dpl. Overall, our data provide a better characterization of microglia/immune cell distribution in the healthy zebrafish brain, highlighting some evolutionarily conserved features with mammals. They also emphasize that 5 days after injury, microglia/immune cells are still activated and are associated to a persistent redox imbalance. Together, these data raise the question of the role of oxidative stress in regenerative neurogenesis in zebrafish. |
| doi_str_mv | 10.1002/cne.25421 |
| format | Article |
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We used zebrafish as a model of brain plasticity and repair. First, by performing L‐plastin (Lcp1) immunohistochemistry and using transgenic Tg(mpeg1.1:GFP) or Tg(mpeg1.1:mCherry) fish, we analyzed the distribution of microglia/immune cells in the whole brain. Specific regional differences were evidenced in terms of microglia/immune cell density and morphology (elongated, branched, highly branched, and amoeboid). Taking advantage of Tg(fli:GFP) and Tg(GFAP::GFP) enabling the detection of endothelial cells and neural stem cells (NSCs), we highlighted the association of elongated microglia/immune cells with blood vessels and rounded/amoeboid microglia with NSCs. Second, after telencephalic injury, we showed that L‐plastin cells were still abundantly present at 5 days post‐lesion (dpl) and were associated with regenerative neurogenesis. Finally, RNA‐sequencing analysis from injured telencephalon (5 dpl) confirmed the upregulation of microglia/immune cell markers and highlighted a significant increase of genes involved in oxidative stress (nox2, nrf2a, and gsr). The analysis of antioxidant activities at 5 dpl also revealed an upregulation of superoxide dismutase and persistent H2O2 generation in the injured telencephalon. Also, microglia/immune cells were shown to be a source of oxidative stress at 5 dpl. Overall, our data provide a better characterization of microglia/immune cell distribution in the healthy zebrafish brain, highlighting some evolutionarily conserved features with mammals. They also emphasize that 5 days after injury, microglia/immune cells are still activated and are associated to a persistent redox imbalance. Together, these data raise the question of the role of oxidative stress in regenerative neurogenesis in zebrafish.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.25421</identifier><identifier>PMID: 36282721</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Animals ; Blood vessels ; Brain - metabolism ; brain injury ; Cell density ; CYBB protein ; Cytology ; Danio rerio ; Disease Models, Animal ; Endothelial cells ; Endothelial Cells - metabolism ; GA-binding protein ; Glial fibrillary acidic protein ; Hydrogen peroxide ; immune cells ; Immunohistochemistry ; Inflammation ; Life Sciences ; Macrophages ; Mammals ; Microglia ; Microglia - metabolism ; Neural stem cells ; Neurogenesis ; Neuroplasticity ; Oxidative Stress ; Regeneration ; Sequence analysis ; SOD ; Stem cells ; Superoxide dismutase ; Telencephalon ; teleost ; Zebrafish ; Zebrafish - metabolism ; Zebrafish Proteins - genetics ; Zebrafish Proteins - metabolism</subject><ispartof>Journal of comparative neurology (1911), 2023-02, Vol.531 (2), p.238-255</ispartof><rights>2022 Wiley Periodicals LLC.</rights><rights>2023 Wiley Periodicals LLC.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3871-2d7b69d818f275fdcd42b6f43af9e29515b4054ea2976a1d2d476dc0151addcb3</citedby><cites>FETCH-LOGICAL-c3871-2d7b69d818f275fdcd42b6f43af9e29515b4054ea2976a1d2d476dc0151addcb3</cites><orcidid>0000-0003-4411-5646 ; 0000-0003-2032-518X ; 0000-0003-3731-150X ; 0000-0003-2360-2197 ; 0000-0002-4652-1376</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fcne.25421$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcne.25421$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,778,782,883,1414,27911,27912,45561,45562</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36282721$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04470577$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Narra, Sai Sandhya</creatorcontrib><creatorcontrib>Rondeau, Philippe</creatorcontrib><creatorcontrib>Fernezelian, Danielle</creatorcontrib><creatorcontrib>Gence, Laura</creatorcontrib><creatorcontrib>Ghaddar, Batoul</creatorcontrib><creatorcontrib>Bourdon, Emmanuel</creatorcontrib><creatorcontrib>Lefebvre d'Hellencourt, Christian</creatorcontrib><creatorcontrib>Rastegar, Sepand</creatorcontrib><creatorcontrib>Diotel, Nicolas</creatorcontrib><title>Distribution of microglia/immune cells in the brain of adult zebrafish in homeostatic and regenerative conditions: Focus on oxidative stress during brain repair</title><title>Journal of comparative neurology (1911)</title><addtitle>J Comp Neurol</addtitle><description>Microglia are macrophage‐like cells exerting determinant roles in neuroinflammatory and oxidative stress processes during brain regeneration. We used zebrafish as a model of brain plasticity and repair. First, by performing L‐plastin (Lcp1) immunohistochemistry and using transgenic Tg(mpeg1.1:GFP) or Tg(mpeg1.1:mCherry) fish, we analyzed the distribution of microglia/immune cells in the whole brain. Specific regional differences were evidenced in terms of microglia/immune cell density and morphology (elongated, branched, highly branched, and amoeboid). Taking advantage of Tg(fli:GFP) and Tg(GFAP::GFP) enabling the detection of endothelial cells and neural stem cells (NSCs), we highlighted the association of elongated microglia/immune cells with blood vessels and rounded/amoeboid microglia with NSCs. Second, after telencephalic injury, we showed that L‐plastin cells were still abundantly present at 5 days post‐lesion (dpl) and were associated with regenerative neurogenesis. Finally, RNA‐sequencing analysis from injured telencephalon (5 dpl) confirmed the upregulation of microglia/immune cell markers and highlighted a significant increase of genes involved in oxidative stress (nox2, nrf2a, and gsr). The analysis of antioxidant activities at 5 dpl also revealed an upregulation of superoxide dismutase and persistent H2O2 generation in the injured telencephalon. Also, microglia/immune cells were shown to be a source of oxidative stress at 5 dpl. Overall, our data provide a better characterization of microglia/immune cell distribution in the healthy zebrafish brain, highlighting some evolutionarily conserved features with mammals. They also emphasize that 5 days after injury, microglia/immune cells are still activated and are associated to a persistent redox imbalance. Together, these data raise the question of the role of oxidative stress in regenerative neurogenesis in zebrafish.</description><subject>Animals</subject><subject>Blood vessels</subject><subject>Brain - metabolism</subject><subject>brain injury</subject><subject>Cell density</subject><subject>CYBB protein</subject><subject>Cytology</subject><subject>Danio rerio</subject><subject>Disease Models, Animal</subject><subject>Endothelial cells</subject><subject>Endothelial Cells - metabolism</subject><subject>GA-binding protein</subject><subject>Glial fibrillary acidic protein</subject><subject>Hydrogen peroxide</subject><subject>immune cells</subject><subject>Immunohistochemistry</subject><subject>Inflammation</subject><subject>Life Sciences</subject><subject>Macrophages</subject><subject>Mammals</subject><subject>Microglia</subject><subject>Microglia - metabolism</subject><subject>Neural stem cells</subject><subject>Neurogenesis</subject><subject>Neuroplasticity</subject><subject>Oxidative Stress</subject><subject>Regeneration</subject><subject>Sequence analysis</subject><subject>SOD</subject><subject>Stem cells</subject><subject>Superoxide dismutase</subject><subject>Telencephalon</subject><subject>teleost</subject><subject>Zebrafish</subject><subject>Zebrafish - metabolism</subject><subject>Zebrafish Proteins - genetics</subject><subject>Zebrafish Proteins - metabolism</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kcFu1DAQhi0EokvhwAsgS1zgkK7tOHbMrVpairSCC5wtJ57sukrsxU4K7dP0UXGapUhInCzPfPr_mfkRek3JGSWErVsPZ6zijD5BK0qUKFQt6FO0yj1aKCXkCXqR0jUhRKmyfo5OSsFqJhldofuPLo3RNdPogsehw4NrY9j1zqzdMEwecAt9n7DzeNwDbqJxD5ixUz_iO8iFzqX93N-HAUIazehabLzFEXbgIeb_TVYJ3rrZI33Al6GdEp7tfjm7tPMMkBK2U3R-d3SJcDAuvkTPOtMneHV8T9H3y4tvm6ti-_XT5835tmjLWtKCWdkIZWtad0xWnW0tZ43oeGk6BUxVtGo4qTgYpqQw1DLLpbAtoRU11rZNeYreL7p70-tDdIOJtzoYp6_Ot3quEc4lqaS8oZl9t7CHGH5MkEY9uDTfyXgIU9L5tDUXvJIz-vYf9DpM0edNMlVxrpSi9V_zfPuUInSPE1Ci54h1jlg_RJzZN0fFqRnAPpJ_Ms3AegF-uh5u_6-kN18uFsnfIaSyHA</recordid><startdate>202302</startdate><enddate>202302</enddate><creator>Narra, Sai Sandhya</creator><creator>Rondeau, Philippe</creator><creator>Fernezelian, Danielle</creator><creator>Gence, Laura</creator><creator>Ghaddar, Batoul</creator><creator>Bourdon, Emmanuel</creator><creator>Lefebvre d'Hellencourt, Christian</creator><creator>Rastegar, Sepand</creator><creator>Diotel, Nicolas</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</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>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-4411-5646</orcidid><orcidid>https://orcid.org/0000-0003-2032-518X</orcidid><orcidid>https://orcid.org/0000-0003-3731-150X</orcidid><orcidid>https://orcid.org/0000-0003-2360-2197</orcidid><orcidid>https://orcid.org/0000-0002-4652-1376</orcidid></search><sort><creationdate>202302</creationdate><title>Distribution of microglia/immune cells in the brain of adult zebrafish in homeostatic and regenerative conditions: Focus on oxidative stress during brain repair</title><author>Narra, Sai Sandhya ; 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We used zebrafish as a model of brain plasticity and repair. First, by performing L‐plastin (Lcp1) immunohistochemistry and using transgenic Tg(mpeg1.1:GFP) or Tg(mpeg1.1:mCherry) fish, we analyzed the distribution of microglia/immune cells in the whole brain. Specific regional differences were evidenced in terms of microglia/immune cell density and morphology (elongated, branched, highly branched, and amoeboid). Taking advantage of Tg(fli:GFP) and Tg(GFAP::GFP) enabling the detection of endothelial cells and neural stem cells (NSCs), we highlighted the association of elongated microglia/immune cells with blood vessels and rounded/amoeboid microglia with NSCs. Second, after telencephalic injury, we showed that L‐plastin cells were still abundantly present at 5 days post‐lesion (dpl) and were associated with regenerative neurogenesis. Finally, RNA‐sequencing analysis from injured telencephalon (5 dpl) confirmed the upregulation of microglia/immune cell markers and highlighted a significant increase of genes involved in oxidative stress (nox2, nrf2a, and gsr). The analysis of antioxidant activities at 5 dpl also revealed an upregulation of superoxide dismutase and persistent H2O2 generation in the injured telencephalon. Also, microglia/immune cells were shown to be a source of oxidative stress at 5 dpl. Overall, our data provide a better characterization of microglia/immune cell distribution in the healthy zebrafish brain, highlighting some evolutionarily conserved features with mammals. They also emphasize that 5 days after injury, microglia/immune cells are still activated and are associated to a persistent redox imbalance. 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| ispartof | Journal of comparative neurology (1911), 2023-02, Vol.531 (2), p.238-255 |
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| subjects | Animals Blood vessels Brain - metabolism brain injury Cell density CYBB protein Cytology Danio rerio Disease Models, Animal Endothelial cells Endothelial Cells - metabolism GA-binding protein Glial fibrillary acidic protein Hydrogen peroxide immune cells Immunohistochemistry Inflammation Life Sciences Macrophages Mammals Microglia Microglia - metabolism Neural stem cells Neurogenesis Neuroplasticity Oxidative Stress Regeneration Sequence analysis SOD Stem cells Superoxide dismutase Telencephalon teleost Zebrafish Zebrafish - metabolism Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
| title | Distribution of microglia/immune cells in the brain of adult zebrafish in homeostatic and regenerative conditions: Focus on oxidative stress during brain repair |
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