Tricyclic antidepressant amitriptyline indirectly increases the proliferation of adult dentate gyrus-derived neural precursors: an involvement of astrocytes
Antidepressants increase the proliferation of neural precursors in adult dentate gyrus (DG), which is considered to be involved in the therapeutic action of antidepressants. However, the mechanism underlying it remains unclear. By using cultured adult rat DG-derived neural precursors (ADP), we have...
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| creator | Boku, Shuken Hisaoka-Nakashima, Kazue Nakagawa, Shin Kato, Akiko Kajitani, Naoto Inoue, Takeshi Kusumi, Ichiro Takebayashi, Minoru |
| description | Antidepressants increase the proliferation of neural precursors in adult dentate gyrus (DG), which is considered to be involved in the therapeutic action of antidepressants. However, the mechanism underlying it remains unclear. By using cultured adult rat DG-derived neural precursors (ADP), we have already shown that antidepressants have no direct effects on ADP. Therefore, antidepressants may increase the proliferation of neural precursors in adult DG via unknown indirect mechanism. We have also shown that amitriptyline (AMI), a tricyclic antidepressant, induces the expressions of GDNF, BDNF, FGF2 and VEGF, common neurogenic factors, in primary cultured astrocytes (PCA). These suggest that AMI-induced factors in astrocytes may increase the proliferation of neural precursors in adult DG. To test this hypothesis, we examined the effects of AMI-induced factors and conditioned medium (CM) from PCA treated with AMI on ADP proliferation. The effects of CM and factors on ADP proliferation were examined with BrdU immunocytochemistry. AMI had no effect on ADP proliferation, but AMI-treated CM increased it. The receptors of GDNF, BDNF and FGF2, but not VEGF, were expressed in ADP. FGF2 significantly increased ADP proliferation, but not BDNF and GDNF. In addition, both of a specific inhibitor of FGF receptors and anti-FGF2 antibody significantly counteracted the increasing effect of CM on ADP proliferation. In addition, FGF2 in brain is mainly derived from astrocytes that are key components of the neurogenic niches in adult DG. These suggest that AMI may increase ADP proliferation indirectly via PCA and that FGF2 may a potential candidate to mediate such an indirect effect of AMI on ADP proliferation via astrocytes. |
| doi_str_mv | 10.1371/journal.pone.0079371 |
| format | Article |
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However, the mechanism underlying it remains unclear. By using cultured adult rat DG-derived neural precursors (ADP), we have already shown that antidepressants have no direct effects on ADP. Therefore, antidepressants may increase the proliferation of neural precursors in adult DG via unknown indirect mechanism. We have also shown that amitriptyline (AMI), a tricyclic antidepressant, induces the expressions of GDNF, BDNF, FGF2 and VEGF, common neurogenic factors, in primary cultured astrocytes (PCA). These suggest that AMI-induced factors in astrocytes may increase the proliferation of neural precursors in adult DG. To test this hypothesis, we examined the effects of AMI-induced factors and conditioned medium (CM) from PCA treated with AMI on ADP proliferation. The effects of CM and factors on ADP proliferation were examined with BrdU immunocytochemistry. AMI had no effect on ADP proliferation, but AMI-treated CM increased it. The receptors of GDNF, BDNF and FGF2, but not VEGF, were expressed in ADP. FGF2 significantly increased ADP proliferation, but not BDNF and GDNF. In addition, both of a specific inhibitor of FGF receptors and anti-FGF2 antibody significantly counteracted the increasing effect of CM on ADP proliferation. In addition, FGF2 in brain is mainly derived from astrocytes that are key components of the neurogenic niches in adult DG. These suggest that AMI may increase ADP proliferation indirectly via PCA and that FGF2 may a potential candidate to mediate such an indirect effect of AMI on ADP proliferation via astrocytes.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0079371</identifier><identifier>PMID: 24260208</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amitriptyline ; Amitriptyline - pharmacology ; Animals ; Antidepressants ; Antidepressive Agents, Tricyclic - pharmacology ; Astrocytes ; Astrocytes - drug effects ; Astrocytes - metabolism ; Brain ; Brain-derived neurotrophic factor ; Brain-Derived Neurotrophic Factor - genetics ; Brain-Derived Neurotrophic Factor - metabolism ; Cell growth ; Cell Proliferation - drug effects ; Cells, Cultured ; Conditioning ; Dentate gyrus ; Dentate Gyrus - cytology ; Fibroblast growth factor 2 ; Fibroblast Growth Factor 2 - genetics ; Fibroblast Growth Factor 2 - metabolism ; Fibroblast growth factors ; Fibroblasts ; Gene expression ; Glial cell line-derived neurotrophic factor ; Glial Cell Line-Derived Neurotrophic Factor - genetics ; Glial Cell Line-Derived Neurotrophic Factor - metabolism ; Growth factors ; Health aspects ; Immunocytochemistry ; Immunohistochemistry ; Kinases ; Male ; Medicine ; Mental depression ; Neural stem cells ; Neurogenesis ; Neurons ; Precursors ; Proteins ; Psychiatry ; Rats ; Rats, Sprague-Dawley ; Rats, Wistar ; Receptors ; Reverse Transcriptase Polymerase Chain Reaction ; Rodents ; Stem cells ; University graduates ; Vascular endothelial growth factor ; Vascular Endothelial Growth Factor A - genetics ; Vascular Endothelial Growth Factor A - metabolism</subject><ispartof>PloS one, 2013-11, Vol.8 (11), p.e79371-e79371</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Boku et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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However, the mechanism underlying it remains unclear. By using cultured adult rat DG-derived neural precursors (ADP), we have already shown that antidepressants have no direct effects on ADP. Therefore, antidepressants may increase the proliferation of neural precursors in adult DG via unknown indirect mechanism. We have also shown that amitriptyline (AMI), a tricyclic antidepressant, induces the expressions of GDNF, BDNF, FGF2 and VEGF, common neurogenic factors, in primary cultured astrocytes (PCA). These suggest that AMI-induced factors in astrocytes may increase the proliferation of neural precursors in adult DG. To test this hypothesis, we examined the effects of AMI-induced factors and conditioned medium (CM) from PCA treated with AMI on ADP proliferation. The effects of CM and factors on ADP proliferation were examined with BrdU immunocytochemistry. AMI had no effect on ADP proliferation, but AMI-treated CM increased it. The receptors of GDNF, BDNF and FGF2, but not VEGF, were expressed in ADP. FGF2 significantly increased ADP proliferation, but not BDNF and GDNF. In addition, both of a specific inhibitor of FGF receptors and anti-FGF2 antibody significantly counteracted the increasing effect of CM on ADP proliferation. In addition, FGF2 in brain is mainly derived from astrocytes that are key components of the neurogenic niches in adult DG. These suggest that AMI may increase ADP proliferation indirectly via PCA and that FGF2 may a potential candidate to mediate such an indirect effect of AMI on ADP proliferation via astrocytes.</description><subject>Amitriptyline</subject><subject>Amitriptyline - pharmacology</subject><subject>Animals</subject><subject>Antidepressants</subject><subject>Antidepressive Agents, Tricyclic - pharmacology</subject><subject>Astrocytes</subject><subject>Astrocytes - drug effects</subject><subject>Astrocytes - metabolism</subject><subject>Brain</subject><subject>Brain-derived neurotrophic factor</subject><subject>Brain-Derived Neurotrophic Factor - genetics</subject><subject>Brain-Derived Neurotrophic Factor - metabolism</subject><subject>Cell growth</subject><subject>Cell Proliferation - drug effects</subject><subject>Cells, Cultured</subject><subject>Conditioning</subject><subject>Dentate gyrus</subject><subject>Dentate Gyrus - cytology</subject><subject>Fibroblast growth factor 2</subject><subject>Fibroblast Growth Factor 2 - genetics</subject><subject>Fibroblast Growth Factor 2 - metabolism</subject><subject>Fibroblast growth factors</subject><subject>Fibroblasts</subject><subject>Gene expression</subject><subject>Glial cell line-derived neurotrophic factor</subject><subject>Glial Cell Line-Derived Neurotrophic Factor - genetics</subject><subject>Glial Cell Line-Derived Neurotrophic Factor - metabolism</subject><subject>Growth factors</subject><subject>Health aspects</subject><subject>Immunocytochemistry</subject><subject>Immunohistochemistry</subject><subject>Kinases</subject><subject>Male</subject><subject>Medicine</subject><subject>Mental depression</subject><subject>Neural stem cells</subject><subject>Neurogenesis</subject><subject>Neurons</subject><subject>Precursors</subject><subject>Proteins</subject><subject>Psychiatry</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Rats, Wistar</subject><subject>Receptors</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Rodents</subject><subject>Stem cells</subject><subject>University graduates</subject><subject>Vascular endothelial growth factor</subject><subject>Vascular Endothelial Growth Factor A - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Boku, Shuken</au><au>Hisaoka-Nakashima, Kazue</au><au>Nakagawa, Shin</au><au>Kato, Akiko</au><au>Kajitani, Naoto</au><au>Inoue, Takeshi</au><au>Kusumi, Ichiro</au><au>Takebayashi, Minoru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tricyclic antidepressant amitriptyline indirectly increases the proliferation of adult dentate gyrus-derived neural precursors: an involvement of astrocytes</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-11-18</date><risdate>2013</risdate><volume>8</volume><issue>11</issue><spage>e79371</spage><epage>e79371</epage><pages>e79371-e79371</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Antidepressants increase the proliferation of neural precursors in adult dentate gyrus (DG), which is considered to be involved in the therapeutic action of antidepressants. However, the mechanism underlying it remains unclear. By using cultured adult rat DG-derived neural precursors (ADP), we have already shown that antidepressants have no direct effects on ADP. Therefore, antidepressants may increase the proliferation of neural precursors in adult DG via unknown indirect mechanism. We have also shown that amitriptyline (AMI), a tricyclic antidepressant, induces the expressions of GDNF, BDNF, FGF2 and VEGF, common neurogenic factors, in primary cultured astrocytes (PCA). These suggest that AMI-induced factors in astrocytes may increase the proliferation of neural precursors in adult DG. To test this hypothesis, we examined the effects of AMI-induced factors and conditioned medium (CM) from PCA treated with AMI on ADP proliferation. The effects of CM and factors on ADP proliferation were examined with BrdU immunocytochemistry. AMI had no effect on ADP proliferation, but AMI-treated CM increased it. The receptors of GDNF, BDNF and FGF2, but not VEGF, were expressed in ADP. FGF2 significantly increased ADP proliferation, but not BDNF and GDNF. In addition, both of a specific inhibitor of FGF receptors and anti-FGF2 antibody significantly counteracted the increasing effect of CM on ADP proliferation. In addition, FGF2 in brain is mainly derived from astrocytes that are key components of the neurogenic niches in adult DG. These suggest that AMI may increase ADP proliferation indirectly via PCA and that FGF2 may a potential candidate to mediate such an indirect effect of AMI on ADP proliferation via astrocytes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24260208</pmid><doi>10.1371/journal.pone.0079371</doi><tpages>e79371</tpages><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1459404233 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Amitriptyline Amitriptyline - pharmacology Animals Antidepressants Antidepressive Agents, Tricyclic - pharmacology Astrocytes Astrocytes - drug effects Astrocytes - metabolism Brain Brain-derived neurotrophic factor Brain-Derived Neurotrophic Factor - genetics Brain-Derived Neurotrophic Factor - metabolism Cell growth Cell Proliferation - drug effects Cells, Cultured Conditioning Dentate gyrus Dentate Gyrus - cytology Fibroblast growth factor 2 Fibroblast Growth Factor 2 - genetics Fibroblast Growth Factor 2 - metabolism Fibroblast growth factors Fibroblasts Gene expression Glial cell line-derived neurotrophic factor Glial Cell Line-Derived Neurotrophic Factor - genetics Glial Cell Line-Derived Neurotrophic Factor - metabolism Growth factors Health aspects Immunocytochemistry Immunohistochemistry Kinases Male Medicine Mental depression Neural stem cells Neurogenesis Neurons Precursors Proteins Psychiatry Rats Rats, Sprague-Dawley Rats, Wistar Receptors Reverse Transcriptase Polymerase Chain Reaction Rodents Stem cells University graduates Vascular endothelial growth factor Vascular Endothelial Growth Factor A - genetics Vascular Endothelial Growth Factor A - metabolism |
| title | Tricyclic antidepressant amitriptyline indirectly increases the proliferation of adult dentate gyrus-derived neural precursors: an involvement of astrocytes |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-05T05%3A57%3A26IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Tricyclic%20antidepressant%20amitriptyline%20indirectly%20increases%20the%20proliferation%20of%20adult%20dentate%20gyrus-derived%20neural%20precursors:%20an%20involvement%20of%20astrocytes&rft.jtitle=PloS%20one&rft.au=Boku,%20Shuken&rft.date=2013-11-18&rft.volume=8&rft.issue=11&rft.spage=e79371&rft.epage=e79371&rft.pages=e79371-e79371&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0079371&rft_dat=%3Cgale_plos_%3EA478219438%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1459404233&rft_id=info:pmid/24260208&rft_galeid=A478219438&rft_doaj_id=oai_doaj_org_article_5bebdaf5d07548c6bad2a1dfd827a09d&rfr_iscdi=true |