{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,30]],"date-time":"2026-01-30T06:35:28Z","timestamp":1769754928704,"version":"3.49.0"},"reference-count":46,"publisher":"Elsevier BV","issue":"7","license":[{"start":{"date-parts":[[2021,7,1]],"date-time":"2021-07-01T00:00:00Z","timestamp":1625097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,7,1]],"date-time":"2021-07-01T00:00:00Z","timestamp":1625097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T00:00:00Z","timestamp":1621296000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["17933225"],"award-info":[{"award-number":["17933225"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["JP19gm1110008"],"award-info":[{"award-number":["JP19gm1110008"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["18H02935"],"award-info":[{"award-number":["18H02935"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["18H04882"],"award-info":[{"award-number":["18H04882"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["18H05281"],"award-info":[{"award-number":["18H05281"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["19H04906"],"award-info":[{"award-number":["19H04906"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["19H05750"],"award-info":[{"award-number":["19H05750"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["19K22512"],"award-info":[{"award-number":["19K22512"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["20K06445"],"award-info":[{"award-number":["20K06445"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Stem Cell Reports"],"published-print":{"date-parts":[[2021,7]]},"DOI":"10.1016\/j.stemcr.2021.05.013","type":"journal-article","created":{"date-parts":[[2021,6,17]],"date-time":"2021-06-17T10:38:21Z","timestamp":1623926301000},"page":"1832-1844","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":21,"title":["Spermatogonial stem cell transplantation into nonablated mouse recipient testes"],"prefix":"10.1016","volume":"16","author":[{"given":"Hiroko","family":"Morimoto","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Narumi","family":"Ogonuki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mito","family":"Kanatsu-Shinohara","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shogo","family":"Matoba","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Atsuo","family":"Ogura","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takashi","family":"Shinohara","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.stemcr.2021.05.013_bib1","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1124\/dmd.106.012880","article-title":"Induction of glutathione synthesis explains pharmacodynamics of high-dose busulfan in mice and highlights putative mechanism of drug interaction","volume":"35","author":"Bouligand","year":"2007","journal-title":"Drug Metab. Dispos."},{"key":"10.1016\/j.stemcr.2021.05.013_bib2","doi-asserted-by":"crossref","first-page":"5085","DOI":"10.1073\/pnas.79.16.5085","article-title":"Special proliferative sites are not needed for seeding and proliferation of transfused bone marrow cells in normal syngeneic mice","volume":"79","author":"Brecher","year":"1982","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"10.1016\/j.stemcr.2021.05.013_bib3","doi-asserted-by":"crossref","first-page":"11303","DOI":"10.1073\/pnas.91.24.11303","article-title":"Germline transmission of donor haplotype following spermatogonial transplantation","volume":"91","author":"Brinster","year":"1994","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"10.1016\/j.stemcr.2021.05.013_bib4","doi-asserted-by":"crossref","first-page":"11298","DOI":"10.1073\/pnas.91.24.11298","article-title":"Spermatogenesis following male germ-cell transplantation","volume":"91","author":"Brinster","year":"1994","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"10.1016\/j.stemcr.2021.05.013_bib5","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1095\/biolreprod.105.043810","article-title":"GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes","volume":"73","author":"Buageaw","year":"2005","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib6","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/0027-5107(87)90057-1","article-title":"Effects of busulfan on murine spermatogenesis: cytotoxicity, sterility, sperm abnormalities, and dominant lethal mutations","volume":"176","author":"Bucci","year":"1987","journal-title":"Mutat. Res."},{"key":"10.1016\/j.stemcr.2021.05.013_bib7","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1530\/REP-19-0254","article-title":"A subpopulation of human Adark spermatogonia behaves as the reserve stem cell","volume":"159","author":"Caldeira-Brant","year":"2020","journal-title":"Reproduction"},{"key":"10.1016\/j.stemcr.2021.05.013_bib8","doi-asserted-by":"crossref","first-page":"1829","DOI":"10.1073\/pnas.1517994113","article-title":"Targeting the Gdnf gene in peritubular myoid cells disrupts undifferentiated spermatogonial cell development","volume":"113","author":"Chen","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"10.1016\/j.stemcr.2021.05.013_bib9","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1152\/physrev.1972.52.1.198","article-title":"Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal","volume":"52","author":"Clermont","year":"1972","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.stemcr.2021.05.013_bib10","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1095\/biolreprod66.6.1579","article-title":"Transplantation of germ cells from glial cell line-derived neurotrophic factor-overexpressing mice to host testes depleted of endogenous spermatogenesis by fractionated irradiation","volume":"66","author":"Creemers","year":"2002","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib11","doi-asserted-by":"crossref","first-page":"e59431","DOI":"10.1371\/journal.pone.0059431","article-title":"The niche-derived glial cell line-derived neurotrophic factor (GDNF) induces migration of mouse spermatogonial stem\/progenitor cells","volume":"8","author":"Dovere","year":"2013","journal-title":"PLoS One"},{"key":"10.1016\/j.stemcr.2021.05.013_bib12","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1002\/mrd.20324","article-title":"Expression patterns of cell-surface molecules on male germ line stem cells during postnatal mouse development","volume":"72","author":"Ebata","year":"2005","journal-title":"Mol. Reprod. Dev."},{"key":"10.1016\/j.stemcr.2021.05.013_bib13","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1089\/scd.2016.0318","article-title":"The NOTCH ligand JAG1 regulates GDNF expression in Sertoli cells","volume":"26","author":"Garcia","year":"2017","journal-title":"Stem Cells Dev."},{"key":"10.1016\/j.stemcr.2021.05.013_bib14","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1016\/S0092-8674(00)81553-6","article-title":"CNS myelin and Sertoli cell tight junction strands are absent in Osp\/claudin-11 null mice","volume":"99","author":"Gow","year":"1999","journal-title":"Cell"},{"key":"10.1016\/j.stemcr.2021.05.013_bib15","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/j.stem.2012.07.017","article-title":"Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm","volume":"11","author":"Hermann","year":"2012","journal-title":"Cell Stem Cell"},{"key":"10.1016\/j.stemcr.2021.05.013_bib16","doi-asserted-by":"crossref","first-page":"1184","DOI":"10.1038\/1941184b0","article-title":"Effect of \u201cbusulfan\u201d (\u201cMyleran\u201d) on the spermatogenic cell population of the rat testis","volume":"194","author":"Jackson","year":"1962","journal-title":"Nature"},{"key":"10.1016\/j.stemcr.2021.05.013_bib17","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1095\/biolreprod.110.087676","article-title":"Stage-specific changes in GDNF expression by rat Sertoli cells: a possible regulator of the replication and differentiation of stem spermatogonia","volume":"85","author":"Johnston","year":"2011","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib18","doi-asserted-by":"crossref","first-page":"1801","DOI":"10.1095\/biolreprod.102.012575","article-title":"Functional assessment of self-renewal activity of male germline stem cells following cytotoxic damages and serial transplantation","volume":"68","author":"Kanatsu-Shinohara","year":"2003","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib19","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1095\/biolreprod.103.017012","article-title":"Long-term proliferation in culture and germline transmission of mouse male germline stem cells","volume":"69","author":"Kanatsu-Shinohara","year":"2003","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib20","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1262\/jrd.09-153N","article-title":"Genetic influences in mouse spermatogonial stem cell self-renewal","volume":"56","author":"Kanatsu-Shinohara","year":"2010","journal-title":"J.\u00a0Reprod. Dev."},{"key":"10.1016\/j.stemcr.2021.05.013_bib21","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1016\/j.stem.2012.06.011","article-title":"Reconstitution of mouse spermatogonial stem cell niches in culture","volume":"11","author":"Kanatsu-Shinohara","year":"2012","journal-title":"Cell Stem Cell"},{"key":"10.1016\/j.stemcr.2021.05.013_bib22","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1095\/biolreprod.115.137869","article-title":"Fertility of male germline stem cells following spermatogonial transplantation in infertile mouse models","volume":"94","author":"Kanatsu-Shinohara","year":"2016","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib23","doi-asserted-by":"crossref","first-page":"2637","DOI":"10.1101\/gad.287045.116","article-title":"Myc\/Mycn-mediated glycolysis enhances mouse spermatogonial stem cell self-renewal","volume":"30","author":"Kanatsu-Shinohara","year":"2016","journal-title":"Genes Dev."},{"key":"10.1016\/j.stemcr.2021.05.013_bib24","doi-asserted-by":"crossref","first-page":"7837","DOI":"10.1073\/pnas.1914963117","article-title":"Autologous transplantation of spermatogonial stem cells restores fertility in congenitally infertile mice","volume":"117","author":"Kanatsu-Shinohara","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"10.1016\/j.stemcr.2021.05.013_bib25","doi-asserted-by":"crossref","first-page":"5087","DOI":"10.1242\/jcs.01393","article-title":"Compartmentalization established by claudin-11-based tight junctions in stria vascularis is required for hearing through generation of endocochlear potentials","volume":"117","author":"Kitajiri","year":"2004","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.stemcr.2021.05.013_bib26","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1093\/biolre\/ioy077","article-title":"Spermatogonial stem cells","volume":"99","author":"Kubota","year":"2018","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib27","first-page":"3575","article-title":"Cytotoxic effects of chemotherapeutic drugs on mouse testis cells","volume":"39","author":"Lu","year":"1979","journal-title":"Cancer Res."},{"key":"10.1016\/j.stemcr.2021.05.013_bib28","first-page":"137","article-title":"Stage-specific sensitivity of spermatogonia to different chemotherapeutic drugs","volume":"38","author":"Meistrich","year":"1984","journal-title":"Biomed. Pharmacother."},{"key":"10.1016\/j.stemcr.2021.05.013_bib29","doi-asserted-by":"crossref","first-page":"1489","DOI":"10.1126\/science.287.5457.1489","article-title":"Regulation of cell fate decision of undifferentiated spermatogonia by GDNF","volume":"287","author":"Meng","year":"2000","journal-title":"Science"},{"key":"10.1016\/j.stemcr.2021.05.013_bib30","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1080\/17425255.2017.1360277","article-title":"Clarifying busulfan metabolism and drug interactions to support new therapeutic drug monitoring strategies: a comprehensive review","volume":"13","author":"Meyers","year":"2017","journal-title":"Expert Opin. Drug Metab. Toxicol."},{"key":"10.1016\/j.stemcr.2021.05.013_bib31","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1095\/biolreprod60.6.1429","article-title":"Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes","volume":"60","author":"Nagano","year":"1999","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib32","first-page":"111","article-title":"Transplantation of testis germinal cells into mouse seminiferous tubules","volume":"41","author":"Ogawa","year":"1997","journal-title":"Int. J. Dev. Biol."},{"key":"10.1016\/j.stemcr.2021.05.013_bib33","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1054\/tice.1999.0060","article-title":"Recipient preparation is critical for spermatogonial transplantation in the rat","volume":"31","author":"Ogawa","year":"1999","journal-title":"Tissue Cell"},{"key":"10.1016\/j.stemcr.2021.05.013_bib34","doi-asserted-by":"crossref","first-page":"8423","DOI":"10.1096\/fj.201802361R","article-title":"Undifferentiated spermatogonia require Cyp26b1 expression through NOTCH signaling and drive germ cell differentiation","volume":"33","author":"Parekh","year":"2019","journal-title":"FASEB J."},{"key":"10.1016\/j.stemcr.2021.05.013_bib35","doi-asserted-by":"crossref","first-page":"1505","DOI":"10.1634\/stemcells.2005-0580","article-title":"Effects of aging and niche microenvironment on spermatogonial stem cell self-renewal","volume":"24","author":"Ryu","year":"2006","journal-title":"Stem Cells"},{"key":"10.1016\/j.stemcr.2021.05.013_bib36","doi-asserted-by":"crossref","first-page":"e28367","DOI":"10.1371\/journal.pone.0028367","article-title":"Cyclical and patch-like GDNF distribution along the basal surface of Sertoli cells in mouse and hamster testes","volume":"6","author":"Sato","year":"2011","journal-title":"PLoS One"},{"key":"10.1016\/j.stemcr.2021.05.013_bib37","doi-asserted-by":"crossref","first-page":"dev151555","DOI":"10.1242\/dev.151555","article-title":"Cyclical expression of GDNF is required for spermatogonial stem cell homeostasis","volume":"145","author":"Sharma","year":"2018","journal-title":"Development"},{"key":"10.1016\/j.stemcr.2021.05.013_bib38","doi-asserted-by":"crossref","first-page":"1428","DOI":"10.1111\/andr.12807","article-title":"Restoration of functional sperm production in irradiated pubertal rhesus monkeys by spermatogonial stem cell transplantation","volume":"8","author":"Shetty","year":"2020","journal-title":"Andrology"},{"key":"10.1016\/j.stemcr.2021.05.013_bib39","doi-asserted-by":"crossref","first-page":"6186","DOI":"10.1073\/pnas.111158198","article-title":"Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility","volume":"98","author":"Shinohara","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"10.1016\/j.stemcr.2021.05.013_bib40","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1095\/biolreprod66.5.1491","article-title":"Germ line stem cell competition in postnatal mouse testes","volume":"66","author":"Shinohara","year":"2002","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib41","doi-asserted-by":"crossref","first-page":"1108","DOI":"10.1093\/humrep\/dex061","article-title":"The production of glial cell line-derived neurotrophic factor by human Sertoli cells is substantially reduced in Sertoli cell-only testes","volume":"32","author":"Singh","year":"2017","journal-title":"Hum. Reprod."},{"key":"10.1016\/j.stemcr.2021.05.013_bib42","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0925-4773(02)00004-7","article-title":"Homeostatic regulation of germinal stem cell proliferation by the GDNF\/FSH pathway","volume":"113","author":"Tadokoro","year":"2002","journal-title":"Mech. Dev."},{"key":"10.1016\/j.stemcr.2021.05.013_bib43","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.stemcr.2015.01.010","article-title":"Functional differences between GDNF-dependent and FGF2-dependent mouse spermatogonial stem cell self-renewal","volume":"4","author":"Takashima","year":"2015","journal-title":"Stem Cell Rep."},{"key":"10.1016\/j.stemcr.2021.05.013_bib44","doi-asserted-by":"crossref","first-page":"213","DOI":"10.2307\/3570892","article-title":"A direct measurement of the radiation sensitivity of normal mouse bone marrow","volume":"14","author":"Till","year":"1961","journal-title":"Radiat. Res."},{"key":"10.1016\/j.stemcr.2021.05.013_bib45","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/j.stemcr.2017.01.006","article-title":"SHISA6 confers resistance to differentiation-promoting Wnt\/beta-catenin signaling in mouse spermatogenic stem cells","volume":"8","author":"Tokue","year":"2017","journal-title":"Stem Cell Rep."},{"key":"10.1016\/j.stemcr.2021.05.013_bib46","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1093\/humrep\/der357","article-title":"The efficiency of male fertility restoration is dependent on the recovery kinetics of spermatogonial stem cells after cytotoxic treatment with busulfan in mice","volume":"27","author":"Zohni","year":"2012","journal-title":"Hum. Reprod."}],"container-title":["Stem Cell Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2213671121002642?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2213671121002642?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T09:46:23Z","timestamp":1761990383000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2213671121002642"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7]]},"references-count":46,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2021,7]]}},"alternative-id":["S2213671121002642"],"URL":"https:\/\/doi.org\/10.1016\/j.stemcr.2021.05.013","relation":{},"ISSN":["2213-6711"],"issn-type":[{"value":"2213-6711","type":"print"}],"subject":[],"published":{"date-parts":[[2021,7]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Spermatogonial stem cell transplantation into nonablated mouse recipient testes","name":"articletitle","label":"Article Title"},{"value":"Stem Cell Reports","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.stemcr.2021.05.013","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 The Author(s).","name":"copyright","label":"Copyright"}]}}