{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T21:04:26Z","timestamp":1792098266965,"version":"4.4.0"},"reference-count":155,"publisher":"Impact Journals, LLC","issue":"39","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Oncotarget"],"published-print":{"date-parts":[[2017,9,12]]},"DOI":"10.18632\/oncotarget.19640","type":"journal-article","created":{"date-parts":[[2017,7,28]],"date-time":"2017-07-28T03:09:03Z","timestamp":1501211343000},"page":"66709-66727","source":"Crossref","is-referenced-by-count":69,"title":["Progress and future prospect of <i>in vitro<\/i> spermatogenesis"],"prefix":"10.18632","volume":"8","author":[{"given":"Fahar","family":"Ibtisham","sequence":"first","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiang","family":"Wu","sequence":"additional","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mei","family":"Xiao","sequence":"additional","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lilong","family":"An","sequence":"additional","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zachary","family":"Banker","sequence":"additional","affiliation":[{"name":"Foreign Language College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aamir","family":"Nawab","sequence":"additional","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Zhao","sequence":"additional","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guanghui","family":"Li","sequence":"additional","affiliation":[{"name":"Agricultural College, Guangdong Ocean University, Zhanjiang, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"7892","published-online":{"date-parts":[[2017,7,27]]},"reference":[{"key":"1","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1093\/ilar\/ilv004","article-title":"Beyond the Mouse Monopoly: Studying the Male Germ Line in Domestic Animal Models","volume":"56","author":"Dobrinski","year":"2015","journal-title":"ILAR J"},{"key":"2","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1159\/000355599","article-title":"Male Germ Cell Development in Humans","volume":"81","author":"S\u00f6der","year":"2014","journal-title":"Horm Res Paediatr"},{"key":"3","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1098\/rstb.2010.0026","article-title":"Spermatogonial stem cell regulation and spermatogenesis","volume":"365","author":"Orwig","year":"2010","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"4","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/j.stem.2016.05.001","article-title":"Gametogenesis from Pluripotent Stem Cells","volume":"18","author":"Miyauchi","year":"2016","journal-title":"Cell Stem Cell"},{"key":"5","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1002\/jemt.20699","article-title":"The spermatogonial stem cell niche","volume":"72","author":"de Rooij","year":"2009","journal-title":"Microsc Res Tech"},{"key":"6","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/S0925-4773(99)00271-3","article-title":"The onset of germ cell migration in the mouse embryo","volume":"91","author":"Wylie","year":"2000","journal-title":"Mech Dev"},{"key":"7","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1530\/jrf.0.0930233","article-title":"Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice","volume":"93","author":"de Rooij","year":"1991","journal-title":"J Reprod Fertil"},{"key":"8","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1002\/(SICI)1097-0185(20000201)258:2<210::AID-AR10>3.0.CO;2-X","article-title":"Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis","volume":"258","author":"Hayashi","year":"2000","journal-title":"Anat Rec"},{"key":"9","doi-asserted-by":"crossref","first-page":"2538","DOI":"10.4161\/cc.25627","article-title":"NOTCH signaling in Sertoli cells regulates gonocyte fate","volume":"12","author":"Hofmann","year":"2013","journal-title":"Cell Cycle"},{"key":"10","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1038\/aja.2011.112","article-title":"Differentiation of murine male germ cells to spermatozoa in a soft agar culture system","volume":"14","author":"Huleihel","year":"2012","journal-title":"Asian J Androl"},{"key":"11","doi-asserted-by":"crossref","first-page":"R159","DOI":"10.1530\/REP-14-0481","article-title":"Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by Sertoli cell signaling","volume":"149","author":"Liu","year":"2015","journal-title":"Reproduction"},{"key":"12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/aja.1001800102","article-title":"A study of intercellular bridges during spermatogenesis in the rat","volume":"180","author":"Russell","year":"1987","journal-title":"Am J Anat"},{"key":"13","first-page":"a005850","article-title":"Germ cell intercellular bridges","volume":"3","author":"Matzuk","year":"2011","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"14","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1530\/rep.1.00220","article-title":"anddifferentiation of male germ cells in the mouse","volume":"128","author":"Lacham-Kaplan","year":"2004","journal-title":"Reproduction"},{"key":"15","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/0027-5107(93)90159-D","article-title":"A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H\/101 F1 hybrid mouse","volume":"290","author":"de Rooij","year":"1993","journal-title":"Mutat Res"},{"key":"16","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1126\/science.134.3482.832","article-title":"Calendar of gametogenic development in the prepuberal male mouse","volume":"134","author":"Hacket","year":"1961","journal-title":"Science"},{"key":"17","doi-asserted-by":"crossref","first-page":"2085","DOI":"10.1095\/biolreprod.103.017020","article-title":"Characterization of spermatogonial stem cell maturation and differentiation in neonatal mice","volume":"69","author":"Griswold","year":"2003","journal-title":"Biol Reprod"},{"key":"18","doi-asserted-by":"crossref","first-page":"4155","DOI":"10.1242\/dev.02004","article-title":"Genetic and epigenetic properties of mouse male germline stem cells during long-term culture","volume":"132","author":"Shinohara","year":"2005","journal-title":"Development"},{"key":"19","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.anireprosci.2007.11.029","article-title":"Role of Sertoli cell number and function on regulation of spermatogenesis","volume":"105","author":"Varner","year":"2008","journal-title":"Anim Reprod Sci"},{"key":"20","first-page":"77","article-title":"Establishment and differentiation of human embryonic stem cell derived germ cells","volume":"63","author":"Clark","year":"2007","journal-title":"Soc Reprod Fertil Suppl"},{"key":"21","doi-asserted-by":"crossref","unstructured":"Felici M De. Oogenesis 2013:19-38.","DOI":"10.1016\/j.melaen.2013.02.004"},{"key":"22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1365-2605.1987.tb00160.x","article-title":"Morphology of normal and malignant germ cells","volume":"10","author":"Hartmann","year":"1987","journal-title":"Int J Androl"},{"key":"23","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0925-4773(99)00307-X","article-title":"SRY, SOX9, and DAX1 expression patterns during human sex determination and gonadal development","volume":"91","author":"Wilson","year":"2000","journal-title":"Mech Dev"},{"key":"24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/bdrc.20142","article-title":"Gonocytes, the forgotten cells of the germ cell lineage","volume":"87","author":"Culty","year":"2009","journal-title":"Birth Defects Res C Embryo Today"},{"key":"25","doi-asserted-by":"crossref","first-page":"R139","DOI":"10.1530\/REP-14-0431","article-title":"Mammalian gonocyte and spermatogonia differentiation: recent advances and remaining challenges","volume":"149","author":"Culty","year":"2015","journal-title":"Reproduction"},{"key":"26","first-page":"7","article-title":"Histological and morphometric studies on the kinetics of germ cells and immature Sertoli cells during human prespermatogenesis","volume":"24","author":"Engemann","year":"1992","journal-title":"Andrologia"},{"key":"27","first-page":"169","article-title":"Differentiation markers of Sertoli cells and germ cells in fetal and early postnatal human testis","volume":"209","author":"Steger","year":"2004","journal-title":"Anat Embryol (Berl)"},{"key":"28","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1002\/aja.1001260106","article-title":"Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops)","volume":"126","author":"Clermont","year":"1969","journal-title":"Am J Anat"},{"key":"29","first-page":"535","article-title":"Morphological and histometric study of human spermatogonia from birth to the onset of puberty","volume":"139","author":"Nistal","year":"1984","journal-title":"J Anat"},{"key":"30","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1095\/biolreprod.109.078550","article-title":"Isolation, characterization, and culture of human spermatogonia","volume":"82","author":"Dym","year":"2010","journal-title":"Biol Reprod"},{"key":"31","doi-asserted-by":"crossref","first-page":"469","DOI":"10.2164\/jandrol.107.004655","article-title":"The cycle of the seminiferous epithelium in humans: a need to revisit?","volume":"29","author":"Amann","year":"2008","journal-title":"J Androl"},{"key":"32","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1038\/embor.2009.211","article-title":"Molecular aspects of male fertility. International Workshop on Molecular Andrology","volume":"10","author":"Hedger","year":"2009","journal-title":"EMBO Rep"},{"key":"33","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1242\/dev.032243","article-title":"Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal","volume":"136","author":"Brinster","year":"2009","journal-title":"Development"},{"key":"34","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1046\/j.1365-2265.1999.00846.x","article-title":"Role of FSH in the regulation of spermatogenesis: clinical aspects","volume":"51","author":"Weinbauer","year":"1999","journal-title":"Clin Endocrinol (Oxf)"},{"key":"35","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1002\/mrd.1088","article-title":"Primordial germ cell-somatic cell partnership: a balancing cell signaling act","volume":"60","author":"Tres","year":"2001","journal-title":"Mol Reprod Dev"},{"key":"36","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1006\/dbio.2001.0173","article-title":"Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse","volume":"232","author":"Zhao","year":"2001","journal-title":"Dev Biol"},{"key":"37","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nature03813","article-title":"Blimp1 is a critical determinant of the germ cell lineage in mice","volume":"436","author":"Surani","year":"2005","journal-title":"Nature"},{"key":"38","doi-asserted-by":"crossref","first-page":"1295","DOI":"10.1242\/dev.030619","article-title":"Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration","volume":"136","author":"Wylie","year":"2009","journal-title":"Development"},{"key":"39","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S0925-4773(00)00283-5","article-title":"Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development","volume":"93","author":"Noce","year":"2000","journal-title":"Mech Dev"},{"key":"40","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/S0925-4773(01)00499-3","article-title":"Two mouse piwi-related genes: miwi and mili","volume":"108","author":"Nakano","year":"2001","journal-title":"Mech Dev"},{"key":"41","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1111\/j.1365-2605.1981.tb00732.x","article-title":"A comparison between the morphology and cell kinetics of gonocytes and adult type undifferentiated spermatogonia in the mouse","volume":"4","author":"de Rooij","year":"1981","journal-title":"Int J Androl"},{"key":"42","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1083\/jcb.74.1.68","article-title":"Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization","volume":"74","author":"Dym","year":"1977","journal-title":"J Cell Biol"},{"key":"43","first-page":"10","article-title":"The Role of Retinoic Acid (RA) in Spermatogonial Differentiation","volume":"94","author":"Geyer","year":"2016","journal-title":"Biol Reprod"},{"key":"44","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.reprotox.2012.12.005","article-title":"Daily sperm production: application in studies of prenatal exposure to nanoparticles in mice","volume":"36","author":"Hougaard","year":"2013","journal-title":"Reprod Toxicol"},{"key":"45","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1038\/ng1366","article-title":"Plzf is required in adult male germ cells for stem cell self-renewal","volume":"36","author":"Braun","year":"2004","journal-title":"Nat Genet"},{"key":"46","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1126\/science.1172645","article-title":"The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells","volume":"325","author":"Saga","year":"2009","journal-title":"Science"},{"key":"47","first-page":"139","article-title":"Differential Expression of Genes Involved in Early Events of Spermatogenesis in Mice","volume":"4","author":"Reddy","year":"2013","journal-title":"J Cell Sci Ther"},{"key":"48","doi-asserted-by":"crossref","first-page":"2084","DOI":"10.1016\/j.jpedsurg.2015.08.031","article-title":"Oct4-GFP expression during transformation of gonocytes into spermatogonial stem cells in the perinatal mouse testis","volume":"50","author":"Hutson","year":"2015","journal-title":"J Pediatr Surg"},{"key":"49","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1007\/s10815-016-0708-2","article-title":"Alteration of spermatogenesis following spermatogonial stem cells transplantation in testicular torsion-detorsion mice","volume":"33","author":"Koruji","year":"2016","journal-title":"J Assist Reprod Genet"},{"key":"50","first-page":"143","article-title":"The Future of Azoospermic Patients: In vitro Spermatogenesis","volume":"4","author":"Mi","year":"2015","journal-title":"Andrology (Los Angel)"},{"key":"51","doi-asserted-by":"crossref","first-page":"5894","DOI":"10.1210\/endo.140.12.7172","article-title":"Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia","volume":"140","author":"van Pelt","year":"1999","journal-title":"Endocrinology"},{"key":"52","doi-asserted-by":"crossref","first-page":"1893","DOI":"10.1095\/biolreprod63.6.1893","article-title":"Involvement of the D-type cyclins in germ cell proliferation and differentiation in the mouse","volume":"63","author":"de Rooij","year":"2000","journal-title":"Biol Reprod"},{"key":"53","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.ydbio.2011.10.027","article-title":"SOHLH1 and SOHLH2 coordinate spermatogonial differentiation","volume":"361","author":"Rajkovic","year":"2012","journal-title":"Dev Biol"},{"key":"54","first-page":"36","article-title":"Germ Cell Differentiation from Embryonic Stem Cells of Mice: Induction Control by BMP4 Signaling","author":"Forouzandeh-Moghadam","year":"2016","journal-title":"Biosci Rep"},{"key":"55","doi-asserted-by":"crossref","first-page":"14976","DOI":"10.1073\/pnas.0807297105","article-title":"Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice","volume":"105","author":"Page","year":"2008","journal-title":"Proc Natl Acad Sci USA"},{"key":"56","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1083\/jcb.200603063","article-title":"Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis","volume":"173","author":"Wang","year":"2006","journal-title":"J Cell Biol"},{"key":"57","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S1097-2765(00)80404-9","article-title":"The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility","volume":"5","author":"Hoog","year":"2000","journal-title":"Mol Cell"},{"key":"58","doi-asserted-by":"crossref","first-page":"2755","DOI":"10.1242\/jcs.02402","article-title":"Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis","volume":"118","author":"Cooke","year":"2005","journal-title":"J Cell Sci"},{"key":"59","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1006\/dbio.2002.0708","article-title":"Meiotic prophase abnormalities and metaphase cell death in MLH1-deficient mouse spermatocytes: insights into regulation of spermatogenic progress","volume":"249","author":"Handel","year":"2002","journal-title":"Dev Biol"},{"key":"60","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1038\/nature02312","article-title":"The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis","volume":"427","author":"Watanabe","year":"2004","journal-title":"Nature"},{"key":"61","first-page":"423","article-title":"Un menage a quatre: the molecular biology of chromosome segregation in meiosis","volume":"112","author":"Nasmyth","year":"2003","journal-title":"Cell"},{"key":"62","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1095\/biolreprod61.5.1256","article-title":"Round spermatid-specific transcription of the mouse SP-10 gene is mediated by a 294-base pair proximal promoter","volume":"61","author":"Herr","year":"1999","journal-title":"Biol Reprod"},{"key":"63","doi-asserted-by":"crossref","first-page":"1838","DOI":"10.1016\/j.bbadis.2012.02.008","article-title":"Molecular control of rodent spermatogenesis","volume":"1822","author":"Vormer","year":"2012","journal-title":"Biochim Biophys Acta"},{"key":"64","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1093\/molehr\/gaq052","article-title":"Human primordial germ cells migrate along nerve fibers and Schwann cells from the dorsal hind gut mesentery to the gonadal ridge","volume":"16","author":"Byskov","year":"2010","journal-title":"Mol Hum Reprod"},{"key":"65","doi-asserted-by":"crossref","first-page":"e296","DOI":"10.1111\/j.1365-2605.2011.01199.x","article-title":"Human spermatogonial stem cells: a possible origin for spermatocytic seminoma","volume":"34","author":"Hofmann","year":"2011","journal-title":"Int J Androl"},{"key":"66","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1159\/000277141","article-title":"Origin, development and regulation of human Leydig cells","volume":"73","author":"Soder","year":"2010","journal-title":"Horm Res Paediatr"},{"key":"67","first-page":"153","article-title":"The sertoli cell\u2014a hormonal target and \u2018super\u2019 nurse for germ cells that determines testicular size","volume":"66","author":"Soder","year":"2006","journal-title":"Horm Res"},{"key":"68","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1159\/000328822","article-title":"Ontogenesis of Ap-2gamma expression in rat testes","volume":"5","author":"Jahnukainen","year":"2011","journal-title":"Sex Dev"},{"key":"69","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1196\/annals.1411.015","article-title":"Testicular morphogenesis: comparison ofandmodels to study male gonadal development","volume":"1120","author":"Schlatt","year":"2007","journal-title":"Ann N Y Acad Sci"},{"key":"70","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1038\/nature09850","article-title":"production of functional sperm in cultured neonatal mouse testes","volume":"471","author":"Ogawa","year":"2011","journal-title":"Nature"},{"key":"71","doi-asserted-by":"crossref","first-page":"32","DOI":"10.4161\/spmg.19383","article-title":"Models of in vitro spermatogenesis","volume":"2","author":"Ivell","year":"2012","journal-title":"Spermatogenesis"},{"key":"72","first-page":"461","article-title":"Quelques r\u00e9sultats de la m\u00e9thode de culture des tissus","volume":"60","author":"Champy","year":"1920","journal-title":"Arch Zool Exp Gen"},{"key":"73","first-page":"232","article-title":"The Developmentof the Mammalian Gonad. Ovary and Ovogenesis. Proc R Soc London Ser B,","volume":"125","author":"Martinovitch","year":"1938","journal-title":"Biol Sci"},{"key":"74","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1210\/endo-74-5-788","article-title":"Initiation of Spermatogenesis","volume":"74","author":"Perloff","year":"1964","journal-title":"Endocrinology"},{"key":"75","first-page":"327","article-title":"Maintenance of adult human testicular tissue in culture","volume":"157","author":"Steinberger","year":"1967","journal-title":"Anat Rec"},{"key":"76","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1508\/cytologia.36.298","article-title":"Autoradiographic evidence of human male germ-cell differentiation in vitro","volume":"36","author":"Sasaki","year":"1971","journal-title":"Cytologia (Tokyo)"},{"key":"77","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1095\/biolreprod28.5.1217","article-title":"Differentiation Mouse Cryptorchid of Type A Spermatogonia from Testes in Serum-Free","volume":"28","author":"Osaka","year":"1983","journal-title":"Biol Reprod"},{"key":"78","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1111\/j.1749-6632.1984.tb38321.x","article-title":"Rat spermatogenesistraced by live cell squashes and monoclonal antibodies","volume":"438","author":"Parvinen","year":"1984","journal-title":"Ann N Y Acad Sci"},{"key":"79","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1002\/j.1939-4640.1985.tb03287.x","article-title":"Flow Cytometric DNA Analysis of Defined Stages of Rat Seminiferous Epithelial Cycle DuringDifferentiation","volume":"6","author":"Parvinen","year":"1985","journal-title":"J Androl"},{"key":"80","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1095\/biolreprod59.2.379","article-title":"Meiotic differentiation of germinal cells in three-week cultures of whole cell population from rat seminiferous tubules","volume":"59","author":"Durand","year":"1998","journal-title":"Biol Reprod"},{"key":"81","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1016\/S0140-6736(98)04784-9","article-title":"Restoration of fertility byspermatogenesis","volume":"353","author":"Mendoza","year":"1999","journal-title":"Lancet"},{"key":"82","doi-asserted-by":"crossref","first-page":"4467","DOI":"10.1210\/jcem.83.12.5304","article-title":"Human spermatogenesis: respective effects of follicle-stimulating hormone and testosterone on meiosis, spermiogenesis, and Sertoli cell apoptosis","volume":"83","author":"Greco","year":"1998","journal-title":"J Clin Endocrinol Metab"},{"key":"83","doi-asserted-by":"crossref","first-page":"2355","DOI":"10.1002\/stem.1238","article-title":"Concise review: Spermatogenesis in an artificial three-dimensional system","volume":"30","author":"Mahmoud","year":"2012","journal-title":"Stem Cells"},{"key":"84","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1007\/978-1-62703-038-0_41","article-title":"spermatogenesis using an organ culture technique","volume":"927","author":"Ogawa","year":"2013","journal-title":"Methods Mol Biol"},{"key":"85","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1038\/ncomms1478","article-title":"production of fertile sperm from murine spermatogonial stem cell lines","volume":"2","author":"Ogawa","year":"2011","journal-title":"Nat Commun"},{"key":"86","doi-asserted-by":"crossref","first-page":"16934","DOI":"10.1073\/pnas.1211845109","article-title":"Testis tissue explantation cures spermatogenic failure in c-Kit ligand mutant mice","volume":"109","author":"Ogawa","year":"2012","journal-title":"Proc Natl Acad Sci USA"},{"key":"87","doi-asserted-by":"crossref","first-page":"e0130171","DOI":"10.1371\/journal.pone.0130171","article-title":"Spermatogenesis in Explanted Adult Mouse Testis Tissues","volume":"10","author":"Ogawa","year":"2015","journal-title":"PLoS One"},{"key":"88","doi-asserted-by":"crossref","first-page":"3377","DOI":"10.1073\/pnas.80.11.3377","article-title":"Viability of rat spermatogenic cellsis facilitated by their coculture with Sertoli cells in serum-free hormone-supplemented medium","volume":"80","author":"Kierszenbaum","year":"1983","journal-title":"Proc Natl Acad Sci USA"},{"key":"89","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1007\/BF02621259","article-title":"Viability of meiotic prophase spermatocytes of rats is facilitated in primary culture of dispersed testicular cells on collagen gel by supplementing epinephrine or norepinephrine: evidence that meiotic prophase spermatocytes complete meiotic divisions in","volume":"25","author":"Nagao","year":"1989","journal-title":"Cell Dev Biol"},{"key":"90","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1016\/0092-8674(93)90543-Y","article-title":"Transmeiotic differentiation of male germ cells in culture","volume":"75","author":"Cuzin","year":"1993","journal-title":"Cell"},{"key":"91","doi-asserted-by":"crossref","first-page":"5533","DOI":"10.1073\/pnas.91.12.5533","article-title":"Immortalized germ cells undergo meiosis","volume":"91","author":"Millan","year":"1994","journal-title":"Proc Natl Acad Sci USA"},{"key":"92","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1126\/science.1073162","article-title":"Generation anddifferentiation of a spermatogonial cell line","volume":"297","author":"Dym","year":"2002","journal-title":"Science"},{"key":"93","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1111\/j.1439-0272.2004.00617.x","article-title":"maturation of fresh and frozen-thawed mouse round spermatids","volume":"36","author":"Kazemnejad","year":"2004","journal-title":"Andrologia"},{"key":"94","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1111\/j.1439-0531.2008.01281.x","article-title":"Culture and Differentiation of Buffalo (Bubalus bubalis) Spermatogonia","volume":"45","author":"Jiang","year":"2010","journal-title":"Reprod Domest Anim"},{"key":"95","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1677\/jme.1.01493","article-title":"The effects of FSH and of testosterone on the completion of meiosis and the very early steps of spermiogenesis of the rat: anstudy","volume":"33","author":"Durand","year":"2004","journal-title":"J Mol Endocrinol"},{"key":"96","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1093\/humrep\/14.5.1287","article-title":"maturation of round spermatids using co-culture on Vero cells","volume":"14","author":"Sousa","year":"1999","journal-title":"Hum Reprod"},{"key":"97","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/S0015-0282(02)04833-1","article-title":"Completion of meiosis in human primary spermatocytes throughcoculture with Vero cells","volume":"79","author":"Kusunoki","year":"2003","journal-title":"Fertil Steril"},{"key":"98","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1016\/j.theriogenology.2005.04.025","article-title":"Characteristics of rat round spermatids differentiated from spermatogonial cells during co-culture with Sertoli cells, assessed by flow cytometry, microinsemination and RT-PCR","volume":"65","author":"Hochi","year":"2006","journal-title":"Theriogenology"},{"key":"99","doi-asserted-by":"crossref","first-page":"2207","DOI":"10.1095\/biolreprod.102.014050","article-title":"Maintenance of mouse male germ line stem cells","volume":"68","author":"Brinster","year":"2003","journal-title":"Biol Reprod"},{"key":"100","doi-asserted-by":"crossref","first-page":"2598","DOI":"10.1093\/humrep\/der248","article-title":"Improvements in human sperm quality by long-termco-culture with isolated porcine Sertoli cells","volume":"26","author":"Foresta","year":"2011","journal-title":"Hum Reprod"},{"key":"101","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1002\/term.297","article-title":"Evaluation ofspermatogenesis using poly(D,L-lactic-co-glycolic acid) (PLGA)-based macroporous biodegradable scaffolds","volume":"5","author":"Min","year":"2011","journal-title":"J Tissue Eng Regen Med"},{"key":"102","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1016\/j.fertnstert.2012.05.039","article-title":"production of haploid cells after coculture of CD49f+ with Sertoli cells from testicular sperm extraction in nonobstructive azoospermic patients","volume":"98","author":"Simon","year":"2012","journal-title":"Fertil Steril"},{"key":"103","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1007\/s10616-013-9584-0","article-title":"Differentiation of spermatogonial stem cell-like cells from murine testicular tissue into haploid male germ cells","volume":"66","author":"Hu","year":"2014","journal-title":"Cytotechnology"},{"key":"104","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1002\/cncr.21185","article-title":"Sperm cryopreservation before cancer chemotherapy helps in the emotional battle against cancer","volume":"104","author":"Kubota","year":"2005","journal-title":"Cancer"},{"key":"105","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0015-0282(97)81465-3","article-title":"Fertility after chemotherapy for testicular germ cell cancer","volume":"68","author":"Albrecht","year":"1997","journal-title":"Fertil Steril"},{"key":"106","first-page":"9","article-title":"Testicular sperm extraction in azoospermic patients with gonadal germ cell tumors prior to chemotherapy\u2014a new therapy option","volume":"4","author":"Miller","year":"2002","journal-title":"Asian J Androl"},{"key":"107","doi-asserted-by":"crossref","first-page":"1556","DOI":"10.1136\/bmj.318.7197.1556","article-title":"Cancer patients should be offered semen cryopreservation","volume":"318","author":"Brinsden","year":"1999","journal-title":"BMJ"},{"key":"108","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1093\/humupd\/dmp054","article-title":"Options for fertility preservation in prepubertal boys","volume":"16","author":"Donnez","year":"2010","journal-title":"Hum Reprod Update"},{"key":"109","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/S0015-0282(00)01721-0","article-title":"Isolation of germ cells from human testicular tissue for low temperature storage and autotransplantation","volume":"75","author":"Gosden","year":"2001","journal-title":"Fertil Steril"},{"key":"110","doi-asserted-by":"crossref","first-page":"2402","DOI":"10.1093\/humrep\/den272","article-title":"Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue","volume":"23","author":"Curaba","year":"2008","journal-title":"Hum Reprod"},{"key":"111","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/S1521-6934(02)00125-6","article-title":"Cryobiology of ovarian and testicular tissue","volume":"17","author":"Hovatta","year":"2003","journal-title":"Best Pract Res Clin Obstet Gynaecol"},{"key":"112","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1093\/humrep\/dei412","article-title":"Spermatogonial survival after grafting human testicular tissue to immunodeficient mice","volume":"21","author":"Tournaye","year":"2006","journal-title":"Hum Reprod"},{"key":"113","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":"Brinster","year":"1999","journal-title":"Tissue Cell"},{"key":"114","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":"Ramsey","year":"2012","journal-title":"Cell Stem Cell"},{"key":"115","first-page":"21","article-title":"Restoration of fertility after treatment for cancer","volume":"59","author":"Radford","year":"2003","journal-title":"Horm Res"},{"key":"116","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1038\/71496","article-title":"Transplantation of male germ line stem cells restores fertility in infertile mice","volume":"6","author":"Brinster","year":"2000","journal-title":"Nat Med"},{"key":"117","doi-asserted-by":"crossref","first-page":"1770","DOI":"10.1007\/s10439-017-1789-5","article-title":"des Rieux A, Wyns C. Restoring Fertility with Cryopreserved Prepubertal Testicular Tissue: Perspectives with Hydrogel Encapsulation, Nanotechnology, and Bioengineered Scaffolds","volume":"45","author":"de Michele","year":"2017","journal-title":"Ann Biomed Eng"},{"key":"118","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":"Zimmermann","year":"1994","journal-title":"Proc Natl Acad Sci USA"},{"key":"119","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1095\/biolreprod66.1.21","article-title":"Germ cell transplantation in pigs","volume":"66","author":"Dobrinski","year":"2002","journal-title":"Biol Reprod"},{"key":"120","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1530\/rep.0.1260765","article-title":"Autologous and homologous transplantation of bovine spermatogonial stem cells","volume":"126","author":"De Rooij","year":"2003","journal-title":"Reproduction"},{"key":"121","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/S0303-7207(01)00706-7","article-title":"Spermatogonial stem cell preservation and transplantation","volume":"187","author":"Schlatt","year":"2002","journal-title":"Mol Cell Endocrinol"},{"key":"122","first-page":"21","article-title":"Cryopreservation of testis tissues andspermatogenesis. Reprod Med","volume":"15","author":"Ogawa","year":"2016","journal-title":"Biol"},{"key":"123","doi-asserted-by":"crossref","first-page":"2331","DOI":"10.1095\/biolreprod.102.014894","article-title":"Progeny from sperm obtained after ectopic grafting of neonatal mouse testes","volume":"68","author":"Dobrinski","year":"2003","journal-title":"Biol Reprod"},{"key":"124","doi-asserted-by":"crossref","first-page":"1855","DOI":"10.1172\/JCI24189","article-title":"Transplantation of spermatogonial stem cells isolated from leukemic mice restores fertility without inducing leukemia","volume":"115","author":"Okuyama","year":"2005","journal-title":"J Clin Invest"},{"key":"125","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1095\/biolreprod.110.083899","article-title":"murine spermatogenesis in an organ culture system","volume":"83","author":"Ogawa","year":"2010","journal-title":"Biol Reprod"},{"key":"126","doi-asserted-by":"crossref","first-page":"238","DOI":"10.4161\/spmg.22069","article-title":"spermatogenesis: A long journey to get tails","volume":"2","author":"Wilkinson","year":"2012","journal-title":"Spermatogenesis"},{"key":"127","doi-asserted-by":"crossref","first-page":"4320","DOI":"10.1038\/ncomms5320","article-title":"Offspring production with sperm grownfrom cryopreserved testis tissues","volume":"5","author":"Ogawa","year":"2014","journal-title":"Nat Commun"},{"key":"128","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1016\/j.fertnstert.2012.11.037","article-title":"Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach","volume":"99","author":"Buck Louis","year":"2013","journal-title":"Fertil Steril"},{"key":"129","doi-asserted-by":"crossref","first-page":"14629","DOI":"10.1073\/pnas.1517466112","article-title":"Fourteen babies born after round spermatid injection into human oocytes","volume":"112","author":"Yanagimachi","year":"2015","journal-title":"Proc Natl Acad Sci USA"},{"key":"130","doi-asserted-by":"crossref","first-page":"e11062","DOI":"10.1371\/journal.pone.0011062","article-title":"The effect on intracytoplasmic sperm injection outcome of genotype, male germ cell stage and freeze-thawing in mice","volume":"5","author":"Ogura","year":"2010","journal-title":"PLoS One"},{"key":"131","doi-asserted-by":"crossref","first-page":"1407","DOI":"10.1095\/biolreprod58.6.1407","article-title":"Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material","volume":"58","author":"Yanagimachi","year":"1998","journal-title":"Biol Reprod"},{"key":"132","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1097\/01.XHA.0000397686.82729.09","article-title":"Unexplained male infertility: potential causes and management","volume":"1","author":"Agarwal","year":"2011","journal-title":"Hum Androlog"},{"key":"133","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1590\/S1677-55382012000500002","article-title":"Unexplained Male infertility: diagnosis and Management","volume":"38","author":"Agarwal","year":"2012","journal-title":"Int Braz J Urol"},{"key":"134","first-page":"182","article-title":"[Assessment of azoospermia and histological evaluation of spermatogenesis]. [Article in French]","volume":"30","author":"Mitchell","year":"2010","journal-title":"Ann Pathol"},{"key":"135","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1093\/humrep\/del279","article-title":"Histological evaluation of the human testis\u2014approaches to optimizing the clinical value of the assessment: mini review","volume":"22","author":"Skakkebaek","year":"2007","journal-title":"Hum Reprod"},{"key":"136","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.1186\/s40064-016-3512-7","article-title":"Relationship between AZFc deletions and testicular histology in infertile South Chinese men with azoospermia and severe oligospermia","volume":"5","author":"Shen","year":"2016","journal-title":"Springerplus"},{"key":"137","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1016\/j.fertnstert.2003.12.018","article-title":"Overcoming maturation arrest byspermatogenesis: search for the optimal culture system","volume":"81","author":"Tesarik","year":"2004","journal-title":"Fertil Steril"},{"key":"138","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1095\/biolreprod53.4.855","article-title":"Development of normal mice from oocytes injected with secondary spermatocyte nuclei","volume":"53","author":"Yanagimachi","year":"1995","journal-title":"Biol Reprod"},{"key":"139","doi-asserted-by":"crossref","first-page":"5611","DOI":"10.1073\/pnas.95.10.5611","article-title":"Development of normal mice from metaphase I oocytes fertilized with primary spermatocytes","volume":"95","author":"Matsuda","year":"1998","journal-title":"Proc Natl Acad Sci USA"},{"key":"140","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1016\/S0140-6736(05)79121-2","article-title":"Ooplasmic injections of secondary spermatocytes for non-obstructive azoospermia","volume":"351","author":"Miyagawa","year":"1998","journal-title":"Lancet"},{"key":"141","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1186\/s13287-016-0405-1","article-title":"An efficient method for generating a germ cell depleted animal model for studies related to spermatogonial stem cell transplantation","volume":"7","author":"Majumdar","year":"2016","journal-title":"Stem Cell Res Ther"},{"key":"142","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/978-1-60327-214-8_11","article-title":"Spermatogonial stem cell transplantation, testicular function, and restoration of male fertility in mice","volume":"450","author":"McLean","year":"2008","journal-title":"Methods Mol Biol"},{"key":"143","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1111\/j.1439-0531.2008.01176.x","article-title":"Male germ cell transplantation","volume":"43","author":"Dobrinski","year":"2008","journal-title":"Reprod Domest Anim"},{"key":"144","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1126\/science.1137741","article-title":"Male germline stem cells: from mice to men","volume":"316","author":"Brinster","year":"2007","journal-title":"Science"},{"key":"145","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1038\/381418a0","article-title":"Rat spermatogenesis in mouse testis","volume":"381","author":"Brinster","year":"1996","journal-title":"Nature"},{"key":"146","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1095\/biolreprod60.2.515","article-title":"Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes","volume":"60","author":"Brinster","year":"1999","journal-title":"Biol Reprod"},{"key":"147","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1095\/biolreprod61.5.1331","article-title":"Transplantation of germ cells from rabbits and dogs into mouse testes","volume":"61","author":"Brinster","year":"1999","journal-title":"Biol Reprod"},{"key":"148","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1038\/nature00918","article-title":"Sperm from neonatal mammalian testes grafted in mice","volume":"418","author":"Schlatt","year":"2002","journal-title":"Nature"},{"key":"149","doi-asserted-by":"crossref","first-page":"R71","DOI":"10.1530\/REP-14-0249","article-title":"Xenografting of testicular tissue pieces: 12 years of anspermatogenesis system","volume":"148","author":"Dobrinski","year":"2014","journal-title":"Reproduction"},{"key":"150","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1093\/hmg\/ddq520","article-title":"Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells","volume":"20","author":"Reijo Pera","year":"2011","journal-title":"Hum Mol Genet"},{"key":"151","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1002\/stem.13","article-title":"Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells","volume":"27","author":"Clark","year":"2009","journal-title":"Stem Cells"},{"key":"152","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/j.cell.2004.11.011","article-title":"Generation of pluripotent stem cells from neonatal mouse testis","volume":"119","author":"Oshimura","year":"2004","journal-title":"Cell"},{"key":"153","doi-asserted-by":"crossref","first-page":"11457","DOI":"10.1073\/pnas.1932826100","article-title":"Embryonic stem cells can form germ cells","volume":"100","author":"Noce","year":"2003","journal-title":"Proc Natl Acad Sci USA"},{"key":"154","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.devcel.2006.05.010","article-title":"-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice","volume":"11","author":"Haaf","year":"2006","journal-title":"Dev Cell"},{"key":"155","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1038\/nature08562","article-title":"Reijo Pera RA. Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation","volume":"462","author":"Nguyen","year":"2009","journal-title":"Nature"}],"container-title":["Oncotarget"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.oncotarget.com\/lookup\/doi\/10.18632\/oncotarget.19640","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,7,15]],"date-time":"2020-07-15T16:30:24Z","timestamp":1594830624000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.oncotarget.com\/lookup\/doi\/10.18632\/oncotarget.19640"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,7,27]]},"references-count":155,"journal-issue":{"issue":"39","published-print":{"date-parts":[[2017,9,12]]}},"alternative-id":["19640","29029549"],"URL":"https:\/\/doi.org\/10.18632\/oncotarget.19640","relation":{},"ISSN":["1949-2553"],"issn-type":[{"value":"1949-2553","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,7,27]]}}}