{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T08:39:47Z","timestamp":1792226387452,"version":"4.4.0"},"reference-count":35,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2020,1,9]],"date-time":"2020-01-09T00:00:00Z","timestamp":1578528000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP15J04519"],"award-info":[{"award-number":["JP15J04519"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP15H05573"],"award-info":[{"award-number":["JP15H05573"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP15K14367"],"award-info":[{"award-number":["JP15K14367"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP18K14715"],"award-info":[{"award-number":["JP18K14715"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP17H01394"],"award-info":[{"award-number":["JP17H01394"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["JP18gm5010001"],"award-info":[{"award-number":["JP18gm5010001"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["P01HD087157"],"award-info":[{"award-number":["P01HD087157"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["R01HD088412"],"award-info":[{"award-number":["R01HD088412"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000865","name":"Bill & Melinda Gates Foundation","doi-asserted-by":"publisher","award":["OPP1160866"],"award-info":[{"award-number":["OPP1160866"]}],"id":[{"id":"10.13039\/100000865","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japanese Society for the Promotion of Science","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,4,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>In mammals, more than 2000 genes are specifically or abundantly expressed in testis, but gene knockout studies revealed several are not individually essential for male fertility. Tesmin (Metallothionein-like 5; Mtl5) was originally reported as a testis-specific transcript that encodes a member of the cysteine-rich motif containing metallothionein family. Later studies showed that Tesmin has two splicing variants and both are specifically expressed in male and female germ cells. Herein, we clarified that the long (Tesmin-L) and short (Tesmin-S) transcript forms start expressing from spermatogonia and the spermatocyte stage, respectively, in testis. Furthermore, while Tesmin-deficient female mice are fertile, male mice are infertile due to arrested spermatogenesis at the pachytene stage. We were able to rescue the infertility with a Tesmin-L transgene, where we concluded that TESMIN-L is critical for meiotic completion in spermatogenesis and indispensable for male fertility.<\/jats:p>","DOI":"10.1093\/biolre\/ioaa002","type":"journal-article","created":{"date-parts":[[2020,1,9]],"date-time":"2020-01-09T07:08:06Z","timestamp":1578553686000},"page":"975-983","source":"Crossref","is-referenced-by-count":28,"title":["Tesmin, Metallothionein-Like 5, is Required for Spermatogenesis in Mice\u2020"],"prefix":"10.1093","volume":"102","author":[{"given":"Asami","family":"Oji","sequence":"first","affiliation":[{"name":"Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan"},{"name":"Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ayako","family":"Isotani","sequence":"first","affiliation":[{"name":"Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan"},{"name":"Immunology Frontier Research Center, Osaka University, Suita, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshitaka","family":"Fujihara","sequence":"first","affiliation":[{"name":"Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julio M","family":"Castaneda","sequence":"first","affiliation":[{"name":"Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seiya","family":"Oura","sequence":"first","affiliation":[{"name":"Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan"},{"name":"Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masahito","family":"Ikawa","sequence":"first","affiliation":[{"name":"Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan"},{"name":"Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan"},{"name":"Immunology Frontier Research Center, Osaka University, Suita, Osaka, Japan"},{"name":"The Institute of Medical Science, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,1,9]]},"reference":[{"key":"2020040320552410500_ref1","doi-asserted-by":"crossref","first-page":"12201","DOI":"10.1073\/pnas.1635054100","article-title":"A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets","volume":"100","author":"Schultz","year":"2003","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020040320552410500_ref2","doi-asserted-by":"crossref","first-page":"7704","DOI":"10.1073\/pnas.1608458113","article-title":"Genome engineering uncovers 54 evolutionarily conserved and testis-enriched genes that are not required for male fertility in mice","volume":"113","author":"Miyata","year":"2016","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020040320552410500_ref3","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1038\/3855","article-title":"Cyclin A1 is required for meiosis in the male mouse","volume":"20","author":"Liu","year":"1998","journal-title":"Nat Genet"},{"key":"2020040320552410500_ref4","doi-asserted-by":"crossref","first-page":"4595","DOI":"10.1242\/dev.124.22.4595","article-title":"HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes","volume":"124","author":"Dix","year":"1997","journal-title":"Development"},{"key":"2020040320552410500_ref5","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1007\/s00018-002-8454-2","article-title":"Molecular life sciences metallothionein: the multipurpose protein","volume":"59","author":"Coyle","year":"2002","journal-title":"Cell Mol Life Sci"},{"key":"2020040320552410500_ref6","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1021\/cr020620d","article-title":"Zinc, cadmium, mercury, and copper thiolates and selenolates mimicking protein active site features\u2014structural aspects and biological implications","volume":"104","author":"Henkel","year":"2004","journal-title":"Chem Rev"},{"key":"2020040320552410500_ref7","doi-asserted-by":"crossref","first-page":"6044","DOI":"10.3390\/ijms14036044","article-title":"The role of metallothionein in oxidative stress","volume":"14","author":"Ruttkay-Nedecky","year":"2013","journal-title":"Int J Mol Sci"},{"key":"2020040320552410500_ref8","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1006\/geno.1999.5756","article-title":"A novel testis-specific metallothionein-like protein, tesmin, is an early marker of male germ cell differentiation","volume":"57","author":"Sugihara","year":"1999","journal-title":"Genomics"},{"key":"2020040320552410500_ref9","doi-asserted-by":"crossref","first-page":"1861","DOI":"10.1095\/biolreprod.102.005603","article-title":"Native tesmin is a 60-kilodalton protein that undergoes dynamic changes in its localization during spermatogenesis in mice","volume":"68","author":"Sutou","year":"2003","journal-title":"Biol Reprod"},{"key":"2020040320552410500_ref10","doi-asserted-by":"crossref","first-page":"2219","DOI":"10.1242\/dev.127.10.2219","article-title":"TSO1 is a novel protein that modulates cytokinesis and cell expansion in arabidopsis","volume":"127","author":"Hauser","year":"2000","journal-title":"Development"},{"key":"2020040320552410500_ref11","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/S0162-0134(01)00377-4","article-title":"Germ cell-specific nucleocytoplasmic shuttling protein, tesmin, responsive to heavy metal stress in mouse testes","volume":"88","author":"Matsuura","year":"2002","journal-title":"J Inorg Biochem"},{"key":"2020040320552410500_ref12","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1002\/mrd.20007","article-title":"Tesmin transcription is regulated differently during male and female meiosis","volume":"67","author":"Olesen","year":"2004","journal-title":"Mol Reprod Dev"},{"key":"2020040320552410500_ref13","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/0378-1119(91)90434-D","article-title":"Efficient selection for high-expression transfectants with a novel eukaryotic vector","volume":"108","author":"Hitoshi","year":"1991","journal-title":"Gene"},{"key":"2020040320552410500_ref14","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/S0014-5793(97)00313-X","article-title":"Green mice\u2019 as a source of ubiquitous green cells","volume":"407","author":"Okabe","year":"1997","journal-title":"FEBS Lett"},{"key":"2020040320552410500_ref15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep03355","article-title":"Generation of mutant mice by pronuclear injection of circular plasmid expressing Cas9 and single guided RNA","volume":"3","author":"Mashiko","year":"2013","journal-title":"Sci Rep"},{"key":"2020040320552410500_ref16","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/B978-0-12-801185-0.00015-5","article-title":"CRISPR\/Cas9-based genome editing in mice by single plasmid injection","volume":"546","author":"Fujihara","year":"2014","journal-title":"Methods Enzymol"},{"key":"2020040320552410500_ref17","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1006\/dbio.2000.9989","article-title":"Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling","volume":"229","author":"Chuma","year":"2001","journal-title":"Dev Biol"},{"key":"2020040320552410500_ref18","doi-asserted-by":"crossref","first-page":"e198","DOI":"10.1371\/journal.pgen.0030198","article-title":"Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein","volume":"3","author":"De La Fuente","year":"2007","journal-title":"PLoS Genet"},{"key":"2020040320552410500_ref19","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1038\/85830","article-title":"Recombinational DNA double-strand breaks in mice precede synapsis","volume":"27","author":"Mahadevaiah","year":"2001","journal-title":"Nat Genet"},{"key":"2020040320552410500_ref20","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1002\/cyto.a.22463","article-title":"Optimized flow cytometry isolation of murine spermatocytes","volume":"85","author":"Gaysinskaya","year":"2014","journal-title":"Cytom Part A"},{"key":"2020040320552410500_ref21","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1186\/s12864-015-2095-y","article-title":"The epigenetic processes of meiosis in male mice are broadly affected by the widely used herbicide atrazine","volume":"16","author":"Gely-Pernot","year":"2015","journal-title":"BMC Genomics"},{"key":"2020040320552410500_ref22","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.devcel.2008.05.015","article-title":"A component of nuage, is essential for spermatogenesis and transposon repression in meiosis","volume":"15","author":"Soper","year":"2008","journal-title":"Dev Cell"},{"key":"2020040320552410500_ref23","doi-asserted-by":"crossref","first-page":"4813","DOI":"10.1021\/ja01574a064","article-title":"A cadmium protein from equine kidney cortex","volume":"79","author":"Margoshes","year":"1957","journal-title":"J Am Chem Soc"},{"key":"2020040320552410500_ref24","doi-asserted-by":"crossref","first-page":"1549","DOI":"10.1039\/C8MT00165K","article-title":"Metallothionein diversity and distribution in the tree of life: a multifunctional protein","volume":"10","author":"Ziller","year":"2018","journal-title":"Metallomics"},{"key":"2020040320552410500_ref25","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1242\/dev.00888","article-title":"BRCA2 deficiency in mice leads to meiotic impairment and infertility","volume":"131","author":"Sharan","year":"2003","journal-title":"Development"},{"key":"2020040320552410500_ref26","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1186\/1471-2164-14-493","article-title":"Suppression of genetic recombination in the pseudoautosomal region and at subtelomeres in mice with a hypomorphic Spo11 allele","volume":"14","author":"Smagulova","year":"2013","journal-title":"BMC Genomics"},{"key":"2020040320552410500_ref27","doi-asserted-by":"crossref","first-page":"e130","DOI":"10.1371\/journal.pgen.0030130","article-title":"Mouse pachytene checkpoint 2 (Trip13) is required for completing meiotic recombination but not synapsis","volume":"3","author":"Li","year":"2007","journal-title":"PLoS Genet"},{"key":"2020040320552410500_ref28","doi-asserted-by":"crossref","first-page":"9377","DOI":"10.1074\/jbc.275.13.9377","article-title":"Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1","volume":"275","author":"Smirnova","year":"2000","journal-title":"J Biol Chem"},{"key":"2020040320552410500_ref29","doi-asserted-by":"crossref","first-page":"25487","DOI":"10.1074\/jbc.M009154200","article-title":"Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals","volume":"276","author":"Saydam","year":"2001","journal-title":"J Biol Chem"},{"key":"2020040320552410500_ref30","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1038\/nature01228","article-title":"Role for a drosophila Myb-containing protein complex in site-specific DNA replication","volume":"420","author":"Beall","year":"2002","journal-title":"Nature"},{"key":"2020040320552410500_ref31","doi-asserted-by":"crossref","first-page":"1549","DOI":"10.1242\/dev.000521","article-title":"Tombola, a tesmin\/TSO1-family protein, regulates transcriptional activation in the drosophila male germline and physically interacts with always early","volume":"134","author":"Jiang","year":"2007","journal-title":"Development"},{"key":"2020040320552410500_ref32","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1016\/j.cell.2006.04.038","article-title":"A gene-centered C. elegans protein-DNA interaction network","volume":"125","author":"Deplancke","year":"2006","journal-title":"Cell"},{"key":"2020040320552410500_ref33","doi-asserted-by":"crossref","first-page":"1903","DOI":"10.4161\/cc.6.15.4512","article-title":"LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2\/M genes","volume":"6","author":"Schmit","year":"2007","journal-title":"Cell Cycle"},{"key":"2020040320552410500_ref34","doi-asserted-by":"crossref","first-page":"5703","DOI":"10.1111\/j.1742-4658.2009.07261.x","article-title":"LIN54 is an essential core subunit of the DREAM\/LINC complex that binds to the cdc2 promoter in a sequence-specific manner","volume":"276","author":"Schmit","year":"2009","journal-title":"FEBS J"},{"key":"2020040320552410500_ref35","doi-asserted-by":"crossref","first-page":"3227","DOI":"10.4161\/cc.21569","article-title":"LIN54 harboring a mutation in CHC domain is localized to the cytoplasm and inhibits cell cycle progression","volume":"11","author":"Matsuo","year":"2012","journal-title":"Cell Cycle"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioaa002\/31775528\/ioaa002.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/102\/4\/975\/32994450\/ioaa002.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/102\/4\/975\/32994450\/ioaa002.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,10]],"date-time":"2022-10-10T12:49:54Z","timestamp":1665406194000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/102\/4\/975\/5698627"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,9]]},"references-count":35,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,1,9]]},"published-print":{"date-parts":[[2020,4,15]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioaa002","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,4]]},"published":{"date-parts":[[2020,1,9]]}}}