{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T22:46:03Z","timestamp":1792622763429,"version":"4.5.0"},"reference-count":53,"publisher":"Japanese Society of Animal Reproduction","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Reprod. Dev.","Journal of Reproduction and Development"],"published-print":{"date-parts":[[2019]]},"DOI":"10.1262\/jrd.2019-042","type":"journal-article","created":{"date-parts":[[2019,8,25]],"date-time":"2019-08-25T22:03:03Z","timestamp":1566770583000},"page":"467-473","source":"Crossref","is-referenced-by-count":17,"title":["Early production of offspring by &lt;i&gt;in vitro&lt;\/i&gt; fertilization using first-wave spermatozoa from prepubertal male mice"],"prefix":"10.1262","volume":"65","author":[{"given":"Keiji","family":"MOCHIDA","sequence":"first","affiliation":[{"name":"RIKEN BioResource Center, Tsukuba, Ibaraki 305-0074, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ayumi","family":"HASEGAWA","sequence":"additional","affiliation":[{"name":"RIKEN BioResource Center, Tsukuba, Ibaraki 305-0074, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Narumi","family":"OGONUKI","sequence":"additional","affiliation":[{"name":"RIKEN BioResource Center, Tsukuba, Ibaraki 305-0074, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kimiko","family":"INOUE","sequence":"additional","affiliation":[{"name":"RIKEN BioResource Center, Tsukuba, Ibaraki 305-0074, Japan"},{"name":"Graduate School of Life and Environmental Science, University of Tsukuba, Ibaraki 305-8572, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Atsuo","family":"OGURA","sequence":"additional","affiliation":[{"name":"RIKEN BioResource Center, Tsukuba, Ibaraki 305-0074, Japan"},{"name":"Graduate School of Life and Environmental Science, University of Tsukuba, Ibaraki 305-8572, Japan"},{"name":"RIKEN Cluster for Pioneering Research, Saitama 351-0198, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"349","reference":[{"key":"1","doi-asserted-by":"crossref","unstructured":"1.  Oakberg EF. A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. <i>Am J Anat<\/i> 1956; 99: 391\u2013413.","DOI":"10.1002\/aja.1000990303"},{"key":"2","unstructured":"2.  Russell LD, Ettlin RA, Hikim APS, Clegg ED. Histological and histopathological evaluation of the testis. Cache River Press, Clearwater FL. 1990."},{"key":"3","doi-asserted-by":"crossref","unstructured":"3.  Itman C, Mendis S, Barakat B, Loveland KL. All in the family: TGF-\u03b2 family action in testis development. <i>Reproduction<\/i> 2006; 132: 233\u2013246.","DOI":"10.1530\/rep.1.01075"},{"key":"4","doi-asserted-by":"crossref","unstructured":"4.  de Kretser DM, Loveland KL, Meehan T, O\u2019Bryan MK, Phillips DJ, Wreford NG. Inhibins, activins and follistatin: actions on the testis. <i>Mol Cell Endocrinol<\/i> 2001; 180: 87\u201392.","DOI":"10.1016\/S0303-7207(01)00502-0"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5.  Barakat B, O\u2019Connor AE, Gold E, de Kretser DM, Loveland KL. Inhibin, activin, follistatin and FSH serum levels and testicular production are highly modulated during the first spermatogenic wave in mice. <i>Reproduction<\/i> 2008; 136: 345\u2013359.","DOI":"10.1530\/REP-08-0140"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6.  Pavlok A. Development of the penetration activity of mouse epididymal spermatozoa in vivo and in vitro. <i>J Reprod Fertil<\/i> 1974; 36: 203\u2013205.","DOI":"10.1530\/jrf.0.0360203"},{"key":"7","unstructured":"7.  Domeniconi RF, Souza AC, Xu B, Washington AM, Hinton BT. Is the epididymis a series of organs placed side by side? <i>Biol Reprod<\/i> 2016; 95: 10."},{"key":"8","doi-asserted-by":"crossref","unstructured":"8.  Lin YW, Hsu TH, Yen PH. Mouse sperm acquire a new structure on the apical hook during epididymal maturation. <i>Asian J Androl<\/i> 2013; 15: 523\u2013528.","DOI":"10.1038\/aja.2013.46"},{"key":"9","unstructured":"9.  Yanagimachi R. Mammalian fertilization. In: Knobil E, Neill JD, (eds.), The Physiology of Reproduction, 2nd ed. New York: Raven Press; 1994: 189\u2013317."},{"key":"10","doi-asserted-by":"crossref","unstructured":"10.  Dacheux JL, Dacheux F. New insights into epididymal function in relation to sperm maturation. <i>Reproduction<\/i> 2013; 147: R27\u2013R42.","DOI":"10.1530\/REP-13-0420"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11.  Dacheux JL, Dacheux F, Paquignon M. Changes in sperm surface membrane and luminal protein fluid content during epididymal transit in the boar. <i>Biol Reprod<\/i> 1989; 40: 635\u2013651.","DOI":"10.1095\/biolreprod40.3.635"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12.  Jervis KM, Robaire B. Dynamic changes in gene expression along the rat epididymis. <i>Biol Reprod<\/i> 2001; 65: 696\u2013703.","DOI":"10.1095\/biolreprod65.3.696"},{"key":"13","doi-asserted-by":"crossref","unstructured":"13.  Cornwall GA. New insights into epididymal biology and function. <i>Hum Reprod Update<\/i> 2009; 15: 213\u2013227.","DOI":"10.1093\/humupd\/dmn055"},{"key":"14","doi-asserted-by":"crossref","unstructured":"14.  Skerget S, Rosenow MA, Petritis K, Karr TL. Sperm proteome maturation in the mouse epididymis. <i>PLoS One<\/i> 2015; 10: e0140650.","DOI":"10.1371\/journal.pone.0140650"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15.  Young SA, Miyata H, Satouh Y, Muto M, Larsen MR, Aitken RJ, Baker MA, Ikawa M. CRISPR\/Cas9-mediated mutation revealed cytoplasmic tail is dispensable for IZUMO1 function and male fertility. <i>Reproduction<\/i> 2016; 152: 665\u2013672.","DOI":"10.1530\/REP-16-0150"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16.  Nixon B, De Iuliis GN, Hart HM, Zhou W, Mathe A, Bernstein IR, Anderson AL, Stanger SJ, Skerrett-Byrne DA, Jamaluddin MFB, Almazi JG, Bromfield EG, Larsen MR, Dun MD. Proteomic profiling of mouse epididymosomes reveals their contributions to post-testicular sperm maturation. <i>Mol Cell Proteomics<\/i> 2019; 18(Suppl 1): S91\u2013S108.","DOI":"10.1074\/mcp.RA118.000946"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17.  Dias GM, Retamal CA, Tobella L, Arnholdt ACV, L\u00f3pez ML. Nuclear status of immature and mature stallion spermatozoa. <i>Theriogenology<\/i> 2006; 66: 354\u2013365.","DOI":"10.1016\/j.theriogenology.2005.10.024"},{"key":"18","doi-asserted-by":"crossref","unstructured":"18.  Aleem M, Padwal V, Choudhari J, Balasinor N, Gill-Sharma MK. Sperm protamine levels as indicators of fertilising potential in sexually mature male rats. <i>Andrologia<\/i> 2008; 40: 29\u201337.","DOI":"10.1111\/j.1439-0272.2008.00805.x"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19.  Yanagimachi R, Kamiguchi Y, Mikamo K, Suzuki F, Yanagimachi H. Maturation of spermatozoa in the epididymis of the Chinese hamster. <i>Am J Anat<\/i> 1985; 172: 317\u2013330.","DOI":"10.1002\/aja.1001720406"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20.  Fujihara Y, Tokuhiro K, Muro Y, Kondoh G, Araki Y, Ikawa M, Okabe M. Expression of TEX101, regulated by ACE, is essential for the production of fertile mouse spermatozoa. <i>Proc Natl Acad Sci USA<\/i> 2013; 110: 8111\u20138116.","DOI":"10.1073\/pnas.1222166110"},{"key":"21","doi-asserted-by":"crossref","unstructured":"21.  Yuan S, Zheng H, Zheng Z, Yan W. Proteomic analyses reveal a role of cytoplasmic droplets as an energy source during epididymal sperm maturation. <i>PLoS One<\/i> 2013; 8: e77466.","DOI":"10.1371\/journal.pone.0077466"},{"key":"22","doi-asserted-by":"crossref","unstructured":"22.  Soler C, Yeung CH, Cooper TG. Development of sperm motility patterns in the murine epididymis. <i>Int J Androl<\/i> 1994; 17: 271\u2013278.","DOI":"10.1111\/j.1365-2605.1994.tb01253.x"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23.  Vadnais ML, Aghajanian HK, Lin A, Gerton GL. Signaling in sperm: toward a molecular understanding of the acquisition of sperm motility in the mouse epididymis. <i>Biol Reprod<\/i> 2013; 89: 127.","DOI":"10.1095\/biolreprod.113.110163"},{"key":"24","doi-asserted-by":"crossref","unstructured":"24.  Lakoski KA, Carron CP, Cabot CL, Saling PM. Epididymal maturation and the acrosome reaction in mouse sperm: response to zona pellucida develops coincident with modification of M42 antigen. <i>Biol Reprod<\/i> 1988; 38: 221\u2013233.","DOI":"10.1095\/biolreprod38.1.221"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25.  Lin M, Lee YH, Xu W, Baker MA, Aitken RJ. Ontogeny of tyrosine phosphorylation-signaling pathways during spermatogenesis and epididymal maturation in the mouse. <i>Biol Reprod<\/i> 2006; 75: 588\u2013597.","DOI":"10.1095\/biolreprod.106.052712"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26.  Yamauchi Y, Ajduk A, Riel JM, Ward MA. Ejaculated and epididymal mouse spermatozoa are different in their susceptibility to nuclease-dependent DNA damage and in their nuclease activity. <i>Biol Reprod<\/i> 2007; 77: 636\u2013647.","DOI":"10.1095\/biolreprod.107.062406"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27.  Sato H, Taketomi Y, Isogai Y, Miki Y, Yamamoto K, Masuda S, Hosono T, Arata S, Ishikawa Y, Ishii T, Kobayashi T, Nakanishi H, Ikeda K, Taguchi R, Hara S, Kudo I, Murakami M. Group III secreted phospholipase A2 regulates epididymal sperm maturation and fertility in mice. <i>J Clin Invest<\/i> 2010; 120: 1400\u20131414.","DOI":"10.1172\/JCI40493"},{"key":"28","doi-asserted-by":"crossref","unstructured":"28.  Simerly C, Castro C, Hartnett C, Lin CC, Sukhwani M, Orwig K, Schatten G. Post-testicular sperm maturation: centriole pairs, found in upper epididymis, are destroyed prior to sperm\u2019s release at ejaculation. <i>Sci Rep<\/i> 2016; 6: 31816.","DOI":"10.1038\/srep31816"},{"key":"29","doi-asserted-by":"crossref","unstructured":"29.  Thornton CE, Brown SDM, Glenister PH. Large numbers of mice established by in vitro fertilization with cryopreserved spermatozoa: implications and applications for genetic resource banks, mutagenesis screens, and mouse backcrosses. <i>Mamm Genome<\/i> 1999; 10: 987\u2013992.","DOI":"10.1007\/s003359901145"},{"key":"30","doi-asserted-by":"crossref","unstructured":"30.  Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). <i>Theriogenology<\/i> 2006; 65: 1716\u20131726.","DOI":"10.1016\/j.theriogenology.2005.09.016"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31.  Takeo T, Nakagata N. Combination medium of cryoprotective agents containing L-glutamine and methyl-\u03b2-cyclodextrin in a preincubation medium yields a high fertilization rate for cryopreserved C57BL\/6J mouse sperm. <i>Lab Anim<\/i> 2010; 44: 132\u2013137.","DOI":"10.1258\/la.2009.009074"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32.  Mochida K, Hasegawa A, Otaka N, Hama D, Furuya T, Yamaguchi M, Ichikawa E, Ijuin M, Taguma K, Hashimoto M, Takashima R, Kadota M, Hiraiwa N, Mekada K, Yoshiki A, Ogura A. Devising assisted reproductive technologies for wild-derived strains of mice: 37 strains from five subspecies of Mus musculus. <i>PLoS One<\/i> 2014; 9: e114305.","DOI":"10.1371\/journal.pone.0114305"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33.  Toyoda Y, Yokoyama M, Hosi T. Studies on fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. <i>Jpn J Anim Reprod<\/i> 1971; 16: 152\u2013157 (in Japanese with English Abstract).","DOI":"10.1262\/jrd1955.16.152"},{"key":"34","doi-asserted-by":"crossref","unstructured":"34.  Suzuki O, Asano T, Yamamoto Y, Takano K, Koura M. Development in vitro of preimplantation embryos from 55 mouse strains. <i>Reprod Fertil Dev<\/i> 1996; 8: 975\u2013980.","DOI":"10.1071\/RD9960975"},{"key":"35","unstructured":"35.  Kito S, Hayao T, Noguchi-Kawasaki Y, Ohta Y, Hideki U, Tateno S. Improved in vitro fertilization and development by use of modified human tubal fluid and applicability of pronucleate embryos for cryopreservation by rapid freezing in inbred mice. <i>Comp Med<\/i> 2004; 54: 564\u2013570."},{"key":"36","doi-asserted-by":"crossref","unstructured":"36.  Miki H, Lee J, Inoue K, Ogonuki N, Noguchi Y, Mochida K, Kohda T, Nagashima H, Ishino F, Ogura A. Microinsemination with first-wave round spermatids from immature male mice. <i>J Reprod Dev<\/i> 2004; 50: 131\u2013137.","DOI":"10.1262\/jrd.50.131"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37.  Ogonuki N, Inoue K, Hirose M, Miura I, Mochida K, Sato T, Mise N, Mekada K, Yoshiki A, Abe K, Kurihara H, Wakana S, Ogura A. A high-speed congenic strategy using first-wave male germ cells. <i>PLoS One<\/i> 2009; 4: e4943.","DOI":"10.1371\/journal.pone.0004943"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38.  Quinn P, Kerin JF, Warnes GM. Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid. <i>Fertil Steril<\/i> 1985; 44: 493\u2013498.","DOI":"10.1016\/S0015-0282(16)48918-1"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39.  Hasegawa A, Mochida K, Matoba S, Yonezawa K, Ohta A, Watanabe G, Taya K, Ogura A. Efficient production of offspring from Japanese wild-derived strains of mice (<i>Mus musculus molossinus<\/i>) by improved assisted reproductive technologies. <i>Biol Reprod<\/i> 2012; 86: 167: 1\u20137.","DOI":"10.1095\/biolreprod.111.098491"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40.  Hasegawa A, Mochida K, Inoue H, Noda Y, Endo T, Watanabe G, Ogura A. High-yield superovulation in adult mice by anti-inhibin serum treatment combined with estrous cycle synchronization. <i>Biol Reprod<\/i> 2016; 94: 21.","DOI":"10.1095\/biolreprod.115.134023"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41.  Bath ML. Inhibition of in vitro fertilizing capacity of cryopreserved mouse sperm by factors released by damaged sperm, and stimulation by glutathione. <i>PLoS One<\/i> 2010; 5: e9387.","DOI":"10.1371\/journal.pone.0009387"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42.  Hasegawa A, Yonezawa K, Ohta A, Mochida K, Ogura A. Optimization of a protocol for cryopreservation of mouse spermatozoa using cryotubes. <i>J Reprod Dev<\/i> 2012; 58: 156\u2013161.","DOI":"10.1262\/jrd.11-097N"},{"key":"43","doi-asserted-by":"crossref","unstructured":"43.  Choi YH, Toyoda Y. Cyclodextrin removes cholesterol from mouse sperm and induces capacitation in a protein-free medium. <i>Biol Reprod<\/i> 1998; 59: 1328\u20131333.","DOI":"10.1095\/biolreprod59.6.1328"},{"key":"44","doi-asserted-by":"crossref","unstructured":"44.  Takeo T, Nakagata N. Reduced glutathione enhances fertility of frozen\/thawed C57BL\/6 mouse sperm after exposure to methyl-\u03b2-cyclodextrin. <i>Biol Reprod<\/i> 2011; 85: 1066\u20131072.","DOI":"10.1095\/biolreprod.111.092536"},{"key":"45","doi-asserted-by":"crossref","unstructured":"45.  Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. <i>J Reprod Fertil<\/i> 1989; 86: 679\u2013688.","DOI":"10.1530\/jrf.0.0860679"},{"key":"46","doi-asserted-by":"crossref","unstructured":"46.  Ogura A, Wakayama T, Suzuki O, Shin TY, Matsuda J, Kobayashi Y. Chromosomes of mouse primary spermatocytes undergo meiotic divisions after incorporation into homologous immature oocytes. <i>Zygote<\/i> 1997; 5: 177\u2013182.","DOI":"10.1017\/S096719940000383X"},{"key":"47","doi-asserted-by":"crossref","unstructured":"47.  Venancio JC, Margatho LO, Rorato R, Rosales RRC, Debarba LK, Coletti R, Antunes-Rodrigues J, Elias CF, Elias LLK. Short-term high-fat diet increases leptin activation of CART neurons and advances puberty in female mice. <i>Endocrinology<\/i> 2017; 158: 3929\u20133942.","DOI":"10.1210\/en.2017-00452"},{"key":"48","doi-asserted-by":"crossref","unstructured":"48.  Lacham O, Trounson A. Fertilizing capacity of epididymal and testicular spermatozoa microinjected under the zona pellucida of the mouse oocyte. <i>Mol Reprod Dev<\/i> 1991; 29: 85\u201393.","DOI":"10.1002\/mrd.1080290113"},{"key":"49","doi-asserted-by":"crossref","unstructured":"49.  Bongso A, Trounson A. Evaluation of motility, freezing ability and embryonic development of murine epididymal sperm after coculture with epididymal epithelium. <i>Hum Reprod<\/i> 1996; 11: 1451\u20131456.","DOI":"10.1093\/oxfordjournals.humrep.a019418"},{"key":"50","doi-asserted-by":"crossref","unstructured":"50.  Uehara T, Yanagimachi R. Behavior of nuclei of testicular, caput and cauda epididymal spermatozoa injected into hamster eggs. <i>Biol Reprod<\/i> 1977; 16: 315\u2013321.","DOI":"10.1095\/biolreprod16.3.315"},{"key":"51","doi-asserted-by":"crossref","unstructured":"51.  Conine CC, Sun F, Song L, Rivera-P\u00e9rez JA, Rando OJ. Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice. <i>Dev Cell<\/i> 2018; 46: 470\u2013480.e3.","DOI":"10.1016\/j.devcel.2018.06.024"},{"key":"52","doi-asserted-by":"crossref","unstructured":"52.  Suganuma R, Yanagimachi R, Meistrich ML. Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. <i>Hum Reprod<\/i> 2005; 20: 3101\u20133108.","DOI":"10.1093\/humrep\/dei169"},{"key":"53","doi-asserted-by":"crossref","unstructured":"53.  Zhou D, Suzuki T, Asami M, Perry ACF. Caput epididymidal mouse sperm support full development. <i>Dev Cell<\/i> 2019; 50: 5\u20136.","DOI":"10.1016\/j.devcel.2019.05.012"}],"container-title":["Journal of Reproduction and Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/jrd\/65\/5\/65_2019-042\/_pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,10,26]],"date-time":"2019-10-26T03:38:48Z","timestamp":1572061128000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/jrd\/65\/5\/65_2019-042\/_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019]]},"references-count":53,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2019]]}},"URL":"https:\/\/doi.org\/10.1262\/jrd.2019-042","relation":{},"ISSN":["0916-8818","1348-4400"],"issn-type":[{"value":"0916-8818","type":"print"},{"value":"1348-4400","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019]]}}}