Nuclear translocation of MTL5 from cytoplasm requires its direct interaction with LIN9 and is essential for male meiosis and fertility
Meiosis is essential for the generation of gametes and sexual reproduction, yet the factors and underlying mechanisms regulating meiotic progression remain largely unknown. Here, we showed that MTL5 translocates into nuclei of spermatocytes during zygotene-pachytene transition and ensures meiosis ad...
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| creator | Zhang, Xingxia Li, Ming Jiang, Xiaohua Ma, Hui Fan, Suixing Li, Yang Yu, Changping Xu, Jianze Khan, Ranjha Jiang, Hanwei Shi, Qinghua |
| description | Meiosis is essential for the generation of gametes and sexual reproduction, yet the factors and underlying mechanisms regulating meiotic progression remain largely unknown. Here, we showed that MTL5 translocates into nuclei of spermatocytes during zygotene-pachytene transition and ensures meiosis advances beyond pachytene stage. MTL5 shows strong interactions with MuvB core complex components, a well-known transcriptional complex regulating mitotic progression, and the zygotene-pachytene transition of MTL5 is mediated by its direct interaction with the component LIN9, through MTL5 C-terminal 443-475 residues. Male Mtl5c-mu/c-mu mice expressing the truncated MTL5 (p.Ser445Arg fs*3) that lacks the interaction with LIN9 and is detained in cytoplasm showed male infertility and spermatogenic arrest at pachytene stage, same as that of Mtl5 knockout mice, indicating that the interaction with LIN9 is essential for the nuclear translocation and function of MTL5 during meiosis. Our data demonstrated MTL5 translocates into nuclei during the zygotene-pachytene transition to initiate its function along with the MuvB core complex in pachytene spermatocytes, highlighting a new mechanism regulating the progression of male meiosis. |
| doi_str_mv | 10.1371/journal.pgen.1009753 |
| format | Article |
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Here, we showed that MTL5 translocates into nuclei of spermatocytes during zygotene-pachytene transition and ensures meiosis advances beyond pachytene stage. MTL5 shows strong interactions with MuvB core complex components, a well-known transcriptional complex regulating mitotic progression, and the zygotene-pachytene transition of MTL5 is mediated by its direct interaction with the component LIN9, through MTL5 C-terminal 443-475 residues. Male Mtl5c-mu/c-mu mice expressing the truncated MTL5 (p.Ser445Arg fs*3) that lacks the interaction with LIN9 and is detained in cytoplasm showed male infertility and spermatogenic arrest at pachytene stage, same as that of Mtl5 knockout mice, indicating that the interaction with LIN9 is essential for the nuclear translocation and function of MTL5 during meiosis. Our data demonstrated MTL5 translocates into nuclei during the zygotene-pachytene transition to initiate its function along with the MuvB core complex in pachytene spermatocytes, highlighting a new mechanism regulating the progression of male meiosis.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009753</identifier><identifier>PMID: 34388164</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Active Transport, Cell Nucleus - physiology ; Animals ; Biology and Life Sciences ; Cell cycle ; Cell Cycle Proteins - metabolism ; Chromosome Pairing - genetics ; Cytoplasm ; DNA-Binding Proteins ; Engineering and Technology ; Fertility ; Fertility - genetics ; Fertility - physiology ; Gametes ; Genetic aspects ; Genetic research ; Infertility ; Infertility, Male - genetics ; Infertility, Male - metabolism ; Localization ; Male ; Medicine and Health Sciences ; Meiosis ; Meiosis - physiology ; Meiotic Prophase I - physiology ; Metallothionein - genetics ; Metallothionein - metabolism ; Mice ; Mice, Inbred C57BL ; Nuclear transport ; Pachytene ; Pachytene Stage - genetics ; Physiological aspects ; Proteins ; Reproductive technologies ; Research and Analysis Methods ; Sexual reproduction ; Spermatocytes ; Spermatocytes - physiology ; Spermatogenesis ; Spermatogenesis - physiology ; Testes ; Testis ; Transcription ; Translocation (Genetics) ; Tumor Suppressor Proteins - metabolism ; Tumor Suppressor Proteins - physiology ; Zygotene</subject><ispartof>PLoS genetics, 2021-08, Vol.17 (8), p.e1009753-e1009753</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Xingxia</au><au>Li, Ming</au><au>Jiang, Xiaohua</au><au>Ma, Hui</au><au>Fan, Suixing</au><au>Li, Yang</au><au>Yu, Changping</au><au>Xu, Jianze</au><au>Khan, Ranjha</au><au>Jiang, Hanwei</au><au>Shi, Qinghua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nuclear translocation of MTL5 from cytoplasm requires its direct interaction with LIN9 and is essential for male meiosis and fertility</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2021-08-13</date><risdate>2021</risdate><volume>17</volume><issue>8</issue><spage>e1009753</spage><epage>e1009753</epage><pages>e1009753-e1009753</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Meiosis is essential for the generation of gametes and sexual reproduction, yet the factors and underlying mechanisms regulating meiotic progression remain largely unknown. Here, we showed that MTL5 translocates into nuclei of spermatocytes during zygotene-pachytene transition and ensures meiosis advances beyond pachytene stage. MTL5 shows strong interactions with MuvB core complex components, a well-known transcriptional complex regulating mitotic progression, and the zygotene-pachytene transition of MTL5 is mediated by its direct interaction with the component LIN9, through MTL5 C-terminal 443-475 residues. Male Mtl5c-mu/c-mu mice expressing the truncated MTL5 (p.Ser445Arg fs*3) that lacks the interaction with LIN9 and is detained in cytoplasm showed male infertility and spermatogenic arrest at pachytene stage, same as that of Mtl5 knockout mice, indicating that the interaction with LIN9 is essential for the nuclear translocation and function of MTL5 during meiosis. Our data demonstrated MTL5 translocates into nuclei during the zygotene-pachytene transition to initiate its function along with the MuvB core complex in pachytene spermatocytes, highlighting a new mechanism regulating the progression of male meiosis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34388164</pmid><doi>10.1371/journal.pgen.1009753</doi><orcidid>https://orcid.org/0000-0002-1010-4407</orcidid><orcidid>https://orcid.org/0000-0002-5682-6827</orcidid><orcidid>https://orcid.org/0000-0002-0995-2345</orcidid><orcidid>https://orcid.org/0000-0002-6133-9759</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1553-7404 |
| ispartof | PLoS genetics, 2021-08, Vol.17 (8), p.e1009753-e1009753 |
| issn | 1553-7404 1553-7390 1553-7404 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
| subjects | Active Transport, Cell Nucleus - physiology Animals Biology and Life Sciences Cell cycle Cell Cycle Proteins - metabolism Chromosome Pairing - genetics Cytoplasm DNA-Binding Proteins Engineering and Technology Fertility Fertility - genetics Fertility - physiology Gametes Genetic aspects Genetic research Infertility Infertility, Male - genetics Infertility, Male - metabolism Localization Male Medicine and Health Sciences Meiosis Meiosis - physiology Meiotic Prophase I - physiology Metallothionein - genetics Metallothionein - metabolism Mice Mice, Inbred C57BL Nuclear transport Pachytene Pachytene Stage - genetics Physiological aspects Proteins Reproductive technologies Research and Analysis Methods Sexual reproduction Spermatocytes Spermatocytes - physiology Spermatogenesis Spermatogenesis - physiology Testes Testis Transcription Translocation (Genetics) Tumor Suppressor Proteins - metabolism Tumor Suppressor Proteins - physiology Zygotene |
| title | Nuclear translocation of MTL5 from cytoplasm requires its direct interaction with LIN9 and is essential for male meiosis and fertility |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-12T21%3A19%3A27IST&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=Nuclear%20translocation%20of%20MTL5%20from%20cytoplasm%20requires%20its%20direct%20interaction%20with%20LIN9%20and%20is%20essential%20for%20male%20meiosis%20and%20fertility&rft.jtitle=PLoS%20genetics&rft.au=Zhang,%20Xingxia&rft.date=2021-08-13&rft.volume=17&rft.issue=8&rft.spage=e1009753&rft.epage=e1009753&rft.pages=e1009753-e1009753&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1009753&rft_dat=%3Cgale_plos_%3EA673927447%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=2573455624&rft_id=info:pmid/34388164&rft_galeid=A673927447&rft_doaj_id=oai_doaj_org_article_22465a6b721242288bb3e3dee9e687bc&rfr_iscdi=true |