{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T04:22:11Z","timestamp":1790050931389,"version":"4.0.1"},"reference-count":167,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T00:00:00Z","timestamp":1761955200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>The growing interest in improving the fertility-rate of livestock species, considering their high economic value, has prompted the development of new methodological approaches using male germline stem cells. Spermatogonial stem cells\u2019 (SSCs) potential to self-renew and differentiate into mature spermatozoa holds promise for their transplantation into testicular tissue and use in new biotechnological methodologies. Moreover, SSCs\u2019 ability to convey genetic information to the next generation is a property that could be exploited for gene targeting. The review provides an update on the main aspects of SSC biology, focusing on the genetic regulators of self-renewal and differentiation processes and different isolation methods. In addition, recent advancement in the cryopreservation of SSCs from domestic animals and their transplantation into recipients\u2019 testes are also discussed. Finally, a section focused on canine SSCs (cSSCs), their biological aspects, and their potential clinical application in the field of reproduction is included. This represents an effective animal model for human reproduction, development, and disease, given that the reproductive anatomy and physiology of canine species and human are similar. We then report on the potential clinical transplantation of SSCs into recipient testicular tissue and suggest future topics to explore for significant advances in fertility preservation.<\/jats:p>","DOI":"10.3390\/vetsci12111047","type":"journal-article","created":{"date-parts":[[2025,11,3]],"date-time":"2025-11-03T13:15:14Z","timestamp":1762175714000},"page":"1047","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Spermatogonial Stem Cells in Domestic Animals: Current Insights and Future Directions with a Focus on Dogs"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0482-7681","authenticated-orcid":false,"given":"Caterina","family":"Squillacioti","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicola","family":"Mirabella","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Iasevoli","sequence":"additional","affiliation":[{"name":"Clinica Veterinaria \u201cGenimal\u201d, Via Principe di Piemonte, 186, Pomigliano d\u2019Arco, 80038 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2154-4205","authenticated-orcid":false,"given":"Simona","family":"Tafuri","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-8683-4711","authenticated-orcid":false,"given":"Valeria","family":"Iervolino","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1133-4300","authenticated-orcid":false,"given":"Alessandra","family":"Pelagalli","sequence":"additional","affiliation":[{"name":"Department of Advanced Biomedical Sciences, University of Naples Federico II, Via Pansini 5, 80131 Naples, Italy"},{"name":"Institute of Biostructures and Bioimages, National Research Council, Via De Amicis 95, 80131 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1722","DOI":"10.1126\/science.1144885","article-title":"A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis","volume":"317","author":"Yoshida","year":"2007","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1038\/nrm2319","article-title":"No place like home: Anatomy and function of the stem cell niche","volume":"9","author":"Jones","year":"2008","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"4071","DOI":"10.1007\/s00018-019-03201-6","article-title":"Mechanisms regulating mammalian spermatogenesis and fertility recovery following germ cell depletion","volume":"76","author":"La","year":"2019","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Ghasemi, N., Azizi, H., Qorbanee, A., and Skutella, T. (2025). From unipotency to pluripotency: Deciphering protein networks and signaling pathways in the generation of embryonic stem-like cells from murine spermatogonial stem cells. BMC Genom., 26.","DOI":"10.1186\/s12864-025-11612-y"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1007\/s00335-007-9037-1","article-title":"Understanding hereditary diseases using the dog and human as companion model systems","volume":"18","author":"Tsai","year":"2007","journal-title":"Mamm. Genome"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s42826-022-00128-1","article-title":"Role of animal models in biomedical research: A review","volume":"38","author":"Mukherjee","year":"2022","journal-title":"Lab. Anim. Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1038\/nature04338","article-title":"Genome sequence, comparative analysis and haplotype structure of the domestic dog","volume":"438","author":"Wade","year":"2005","journal-title":"Nature"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/s13353-022-00721-z","article-title":"Dog-human translational genomics: State of the art and genomic resources","volume":"63","author":"Pallotti","year":"2022","journal-title":"J. Appl. Genet."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.semcdb.2017.08.024","article-title":"The companion dog as a unique translational model for aging","volume":"70","author":"Mazzatenta","year":"2017","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Schiffman, J.D., and Breen, M. (2015). Comparative oncology: What dogs and other species can teach us about humans with cancer. Philos. Trans. R. Soc. Lond. B Biol. Sci., 370.","DOI":"10.1098\/rstb.2014.0231"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Wright, S.J. (2017). Spotlight on Reproduction in Domestic Dogs as a Model for Human Reproduction. Animal Models and Human Reproduction, John Wiley & Sons, Inc.","DOI":"10.1002\/9781118881286.ch11"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"R265","DOI":"10.1530\/REP-20-0042","article-title":"The dog as a sentinel species for environmental effects on human fertility","volume":"159","author":"Sumner","year":"2020","journal-title":"Reproduction"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1007\/s00441-020-03212-x","article-title":"The study and manipulation of spermatogonial stem cells using animal models","volume":"380","author":"Ibtisham","year":"2020","journal-title":"Cell Tissue Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"R151","DOI":"10.1530\/REP-16-0588","article-title":"Role of the testis interstitial compartment in spermatogonial stem cell function","volume":"153","author":"Potter","year":"2017","journal-title":"Reproduction"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1152\/physrev.00025.2011","article-title":"The germline stem cell niche unit in mammalian testes","volume":"92","author":"Oatley","year":"2012","journal-title":"Physiol. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1038\/s41422-018-0099-2","article-title":"The adult human testis transcriptional cell atlas","volume":"28","author":"Guo","year":"2018","journal-title":"Cell Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4379","DOI":"10.1038\/s41467-018-06881-z","article-title":"Testicular endothelial cells are a critical population in the germline stem cell niche","volume":"9","author":"Bhang","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2012","DOI":"10.1095\/biolreprod.104.028381","article-title":"Immunohistochemical Profiling of Germ Cells Within the Human Fetal Testis: Identification of Three Subpopulations","volume":"71","author":"Gaskell","year":"2004","journal-title":"Biol. Reprod."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1111\/andr.12810","article-title":"Developmental underpinnings of spermatogonial stem cell establishment","volume":"8","author":"Law","year":"2020","journal-title":"Andrology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"194571","DOI":"10.1242\/dev.194571","article-title":"Proper timing of a quiescence period in precursor prospermatogonia is required for stem cell pool establishment in the male germline","volume":"148","author":"Du","year":"2021","journal-title":"Development"},{"key":"ref_21","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. USA"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1126\/science.1182868","article-title":"Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment","volume":"328","author":"Nakagawa","year":"2010","journal-title":"Science"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"658","DOI":"10.1016\/j.stem.2014.01.019","article-title":"Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states","volume":"14","author":"Hara","year":"2014","journal-title":"Cell Stem Cell"},{"key":"ref_24","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":"ref_25","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.ydbio.2004.12.006","article-title":"Isolation of male germ-line stem cells; influence of GDNF","volume":"279","author":"Hofmann","year":"2005","journal-title":"Dev. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"16489","DOI":"10.1073\/pnas.0407063101","article-title":"Growth factors essential for selfrenewal and expansion of mouse spermatogonial stem cells","volume":"101","author":"Kubota","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.stemcr.2014.06.007","article-title":"Enhanced fitness of adult spermatogonial stem cells bearing a paternal age-associated FGFR2 mutation","volume":"3","author":"Assif","year":"2014","journal-title":"Stem Cell Rep."},{"key":"ref_28","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":"Chen","year":"2015","journal-title":"Reproduction"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1107","DOI":"10.1016\/j.celrep.2015.07.015","article-title":"Macrophages contribute to the spermatogonial niche in the adult testis","volume":"12","author":"Potter","year":"2015","journal-title":"Cell Rep."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Sawaied, A., Arazi, E., AbuElhija, A., Lunenfeld, E., and Huleihel, M. (2021). The presence of colony-stimulating factor-1 and its receptor in different cells of the testis; it involved in the development of spermatogenesis in vitro. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22052325"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1186\/s13287-024-03893-z","article-title":"Microenvironment of spermatogonial stem cells: A key factor in the regulation of spermatogenesis","volume":"15","author":"Liu","year":"2024","journal-title":"Stem Cell Res. Ther."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1782","DOI":"10.1016\/j.stemcr.2018.03.016","article-title":"FGF2 has distinct molecular functions from GDNF in the mouse germline niche","volume":"10","author":"Masaki","year":"2018","journal-title":"Stem Cell Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2615","DOI":"10.1007\/s10815-020-01912-5","article-title":"EGF, GDNF, and IGF-1 influence the proliferation and stemness of ovine spermatogonial stem cells in vitro","volume":"37","author":"Binsila","year":"2020","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1574","DOI":"10.1111\/rda.13566","article-title":"The effects of growth factors on proliferation of spermatogonial stem cells from Guangxi Bama mini-pig","volume":"54","author":"Zhao","year":"2019","journal-title":"Reprod. Dom. Anim."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"25842","DOI":"10.1074\/jbc.M703474200","article-title":"Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling","volume":"282","author":"Oatley","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.stemcr.2021.01.015","article-title":"Spermatogonial stem cell numbers are reduced by transient inhibition of GDNF signaling but restored by self-renewing replication when signaling resumes","volume":"16","author":"Parker","year":"2021","journal-title":"Stem Cell Rep."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"eabq3173","DOI":"10.1126\/sciadv.abq3173","article-title":"Decoding the spermatogonial stem cell niche under physiological and recovery conditions in adult mice and humans","volume":"9","author":"Jin","year":"2023","journal-title":"Sci. Adv."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1530\/REP-07-0419","article-title":"Propagation of bovine spermatogonial stem cells in vitro","volume":"136","author":"Aponte","year":"2008","journal-title":"Reproduction"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1071\/RD12330","article-title":"Effects of glial cell line-derived neurotrophic factor, fibroblast growth factor 2 and epidermal growth factor on proliferation and the expression of some genes in buffalo (Bubalus bubalis) spermatogonial cells","volume":"25","author":"Kadam","year":"2013","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_40","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":"Ogonuki","year":"2003","journal-title":"Biol. Reprod."},{"key":"ref_41","first-page":"1009","article-title":"CXCL12-CXCR4 signaling is required for the maintenance of mouse spermatogonial stem cells","volume":"126","author":"Yang","year":"2013","journal-title":"J. Cell Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3878","DOI":"10.4161\/cc.7.24.7262","article-title":"ATRA and KL promote differentiation toward the meiotic program of male germ cells","volume":"7","author":"Pellegrini","year":"2008","journal-title":"Cell Cycle"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1095\/biolreprod.110.085456","article-title":"BMP4-induced differentiation of a rat spermatogonial stem cell line causes changes in its cell adhesion properties","volume":"83","author":"Carlomagno","year":"2010","journal-title":"Biol. Reprod."},{"key":"ref_44","first-page":"1455","article-title":"SOHLH1 and SOHLH2 control kit expression during postnatal male germ cell development","volume":"125","author":"Barrios","year":"2012","journal-title":"J. Cell. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1242\/dev.087403","article-title":"MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells","volume":"140","author":"Yang","year":"2013","journal-title":"Development"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.stem.2012.02.004","article-title":"Functional antagonism between Sall4 and Plzf defines germline progenitors","volume":"10","author":"Hobbs","year":"2012","journal-title":"Cell Stem Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3456","DOI":"10.1172\/JCI57984","article-title":"Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis","volume":"121","author":"Goertz","year":"2011","journal-title":"J. Clin. Investig."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e1829","DOI":"10.31661\/gmj.v9i0.1829","article-title":"Determination of the excitatory effects of MicroRNA-30 in the self-renewal and differentiation process of neonatal mouse spermatogonial stem cells","volume":"9","author":"Khanehzad","year":"2020","journal-title":"Galen Med. J."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1002\/jcb.24655","article-title":"miR-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2","volume":"115","author":"Yu","year":"2014","journal-title":"J. Cell. Biochem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"199799","DOI":"10.1242\/dev.199799","article-title":"The microRNA miR-202 prevents precocious spermatogonial differentiation and meiotic initiation during mouse spermatogenesis","volume":"148","author":"Chen","year":"2021","journal-title":"Development"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Tong, M.H., Mitchell, D.A., McGowan, S.D., Evanoff, R., and Griswold, M.D. (2012). Two miRNA clusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of spermatogonial differentiation in mice. Biol. Reprod., 86.","DOI":"10.1095\/biolreprod.111.096313"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e2713","DOI":"10.1097\/MD.0000000000002713","article-title":"Targeted disruption of miR-17-92 impairs mouse spermatogenesis by activating mTOR signaling pathway","volume":"95","author":"Xie","year":"2016","journal-title":"Medicine"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"3950","DOI":"10.1111\/jcmm.16347","article-title":"Sertoli cell-derived exosomal microRNA-486-5p regulates differentiation of spermatogonial stem cell through PTEN in mice","volume":"25","author":"Li","year":"2021","journal-title":"J. Cell. Mol. Med."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1089\/rej.2015.1719","article-title":"miR-204 regulates the proliferation of dairy goat spermatogonial stem cells via targeting to Sirt1","volume":"19","author":"Niu","year":"2016","journal-title":"Rejuvenation Res."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Gao, Y., Wu, F., Ren, Y., Zhou, Z., Chen, N., Huang, Y., Lei, C., Chen, H., and Dang, R. (2020). MiRNAs expression profiling of bovine (Bos taurus) testes and effect of bta-miR-146b on proliferation and apoptosis in bovine male germline stem cells. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21113846"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1095\/biolreprod.103.020867","article-title":"CD9 is a surface marker on mouse and rat male germline stem cells","volume":"70","author":"Toyokuni","year":"2004","journal-title":"Biol. Reprod."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"6487","DOI":"10.1073\/pnas.0631767100","article-title":"Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells","volume":"100","author":"Kubota","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5504","DOI":"10.1073\/pnas.96.10.5504","article-title":"beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells","volume":"96","author":"Shinohara","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_59","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":"Zi","year":"2010","journal-title":"Biol. Reprod."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"21672","DOI":"10.1073\/pnas.0912432106","article-title":"Prepubertal human spermatogonia and mouse gonocytes share conserved gene expressionof germline stem cell regulatory molecules","volume":"106","author":"Wu","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1002\/bdrc.20141","article-title":"Spermatogonial stem cells: Mouse and human comparisons","volume":"87","author":"Dym","year":"2009","journal-title":"Birth Defects Res. Part C Embryo Today Rev."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"9524","DOI":"10.1073\/pnas.0603332103","article-title":"Identifying genes important for spermatogonial stem cell selfrenewal and survival","volume":"103","author":"Oatley","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1146\/annurev.cellbio.24.110707.175355","article-title":"Regulation of spermatogonial stem cell self-renewal in mammals","volume":"24","author":"Oatley","year":"2008","journal-title":"Ann. Rev. Cell. Dev. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1262\/jrd.2020-019","article-title":"CD2 is a surface marker for mouse and rat spermatogonial stem cells","volume":"66","author":"Chen","year":"2020","journal-title":"J. Reprod. Develop."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"RP85380","DOI":"10.7554\/eLife.85380.3","article-title":"FOXC2 marks and maintains the primitive spermatogonial stem cells subpopulation in the adult testis","volume":"12","author":"Wang","year":"2023","journal-title":"eLife"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1712","DOI":"10.1002\/jcb.24835","article-title":"CD49f-positive testicular cells in Saanen dairy goat were identified as spermatogonia-like cells by miRNA profiling analysis","volume":"115","author":"Wu","year":"2014","journal-title":"J. Cell. Biochem."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Lu, X., Yin, P., Li, H., Gao, W., Jia, H., and Ma, W. (2024). Transcriptome analysis of key genes involved in the initiation of spermatogonial stem cell differentiation. Genes, 15.","DOI":"10.3390\/genes15020141"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.theriogenology.2023.07.008","article-title":"The role of miR-199a-3p in inhibiting the proliferation of spermatogonial stem cells under heat stress","volume":"211","author":"Zhuo","year":"2023","journal-title":"Theriogenology"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"104583","DOI":"10.1016\/j.psj.2024.104583","article-title":"miR-1458 is inhibited by low concentrations of Vitamin B6 and targets TBX6 to promote the formation of spermatogonial stem cells in Rugao Yellow Chicken","volume":"104","author":"Geng","year":"2025","journal-title":"Poult. Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1095\/biolreprod.107.063057","article-title":"Establishment of a short-term in vitro assay for mouse spermatogonial stem cells","volume":"77","author":"Yeh","year":"2007","journal-title":"Biol. Reprod."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/humrep\/deac245","article-title":"Human spermatogonial stem cells and their niche in male (in)fertility: Novel concepts from single-cell RNA-sequencing","volume":"38","author":"Neuhaus","year":"2023","journal-title":"Hum. Reprod."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1530\/rep.0.1240085","article-title":"Isolation and purification of type A spermatogonia from the bovine testis","volume":"124","author":"Izadyar","year":"2002","journal-title":"Reproduction"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1093\/biolre\/ioae109","article-title":"Spermatogonial stem cell technologies: Applications from human medicine to wildlife conservation","volume":"111","author":"Damyanova","year":"2024","journal-title":"Biol. Reprod."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"5","DOI":"10.4103\/aja.aja_41_21","article-title":"Recent advances in isolation, identification, and culture of mammalian spermatogonial stem cells","volume":"24","author":"Xi","year":"2022","journal-title":"Asian J. Androl."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.anireprosci.2018.04.070","article-title":"Isolation and enrichment of putative spermatogonial stem cells from ram (Ovis aries) testis","volume":"196","author":"Binsila","year":"2018","journal-title":"Anim. Reprod. Sci."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Nabulindo, N.W., Nguhiu-Mwangi, J., Kipyegon, A.N., Ogugo, M., Muteti, C., Tiambo, C., Oatley, M.J., Oatley, J.M., and Kemp, S. (2022). Culture of kenyan goat (Capra hircus) undifferentiated spermatogonia in feeder-free conditions. Front. Vet. Sci., 9.","DOI":"10.3389\/fvets.2022.894075"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1530\/REP-13-0086","article-title":"Isolation, genetic manipulation, and transplantation of canine spermatogonial stem cells: Progress toward transgenesis through the male germline","volume":"146","author":"Harkey","year":"2013","journal-title":"Reproduction"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1111\/rda.14278","article-title":"Propagation of porcine spermatogonial stem cells in serum-free culture conditions using knockout serum replacement","volume":"58","author":"Lalmalsawma","year":"2023","journal-title":"Reprod. Dom. Anim."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2039","DOI":"10.1071\/RD15003","article-title":"Factors supporting long-term culture of bovine male germ cells","volume":"28","author":"Sahare","year":"2015","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1111\/rda.12819","article-title":"Molecular markers of putative spermatogonial stem cells in the domestic cat","volume":"52","author":"Kim","year":"2017","journal-title":"Reprod. Dom. Anim."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"273","DOI":"10.4103\/2305-0500.390302","article-title":"Cryopreserved ovine spermatogonial stem cells maintain stemness and colony forming ability in vitro","volume":"12","author":"Pramod","year":"2023","journal-title":"Asian Pac. J. Reprod."},{"key":"ref_82","first-page":"R95","article-title":"Regulation of GDNF expression in Sertoli cells","volume":"157","author":"Parekh","year":"2019","journal-title":"Reproduction"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1407","DOI":"10.5713\/ajas.15.0592","article-title":"Isolation and identification of prepubertal buffalo (Bubalus bubalis) spermatogonial stem cells","volume":"29","author":"Feng","year":"2016","journal-title":"Asian Australas. J. Anim. Sci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"e14661","DOI":"10.1111\/rda.14661","article-title":"Optimal isolation, culture, and in vitro propagation of spermatogonial stem cells in Huaixiang chicken","volume":"59","author":"Ibtisham","year":"2024","journal-title":"Reprod. Dom. Anim."},{"key":"ref_85","first-page":"61","article-title":"Transplantation of goat spermatogonial stem cells into the mouse rete testis","volume":"1","author":"Shirazi","year":"2015","journal-title":"Int. J. Anim. Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/s00441-017-2673-1","article-title":"Horse spermatogonial stem cell cryopreservation: Feasible protocols and potential biotechnological applications","volume":"370","author":"Costa","year":"2017","journal-title":"Cell Tissue Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1111\/rda.14043","article-title":"Isolation and in vitro expansion of porcine spermatogonial stem cells","volume":"57","author":"Zhao","year":"2022","journal-title":"Reprod. Dom. Anim."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"2604","DOI":"10.1096\/fj.10-175802","article-title":"Glial cell line-derived neurotrophic factor and endothelial cells promote self-renewal of rabbit germ cells with spermatogonial stem cell properties","volume":"25","author":"Kubota","year":"2011","journal-title":"FASEB J."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1186\/s13287-024-03701-8","article-title":"Expression profiling of stemness markers in testicular germline stem cells from neonatal and adult Swiss albino mice during their transdifferentiation in vitro","volume":"15","author":"Indu","year":"2024","journal-title":"Stem Cell Res. Ther."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1002\/mrd.22958","article-title":"Long-term culture of undifferentiated spermatogonia isolated from immature and adult bovine testes","volume":"85","author":"Kitamura","year":"2018","journal-title":"Mol. Reprod. Dev."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1111\/rda.13900","article-title":"Transcriptome analysis revealed differences in the microenvironment of spermatogonial stem cells in seminiferous tubules between prepubertal and adult buffaloes","volume":"56","author":"Zhang","year":"2021","journal-title":"Reprod. Dom. Anim."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"e14056","DOI":"10.1111\/and.14056","article-title":"Culture bovine prospermatogonia with 2i medium","volume":"53","author":"Cai","year":"2021","journal-title":"Andrologia"},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Yang, R., Zhang, B., Wang, Y., Zhang, Y., Zhao, Y., Jiang, D., Chen, L., Tang, B., and Zhang, X. (2024). H3K9me3 Levels Affect the Proliferation of Bovine Spermatogonial Stem Cells. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25179215"},{"key":"ref_94","unstructured":"Baarends, W., and Grootegoed, J. (1999). Molecular biology of male gametogenesis. Molecular Biology in Reproductive Medicine, Parthenon Publishing."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1007\/s00580-019-02944-9","article-title":"The beneficial effect of equine chorionic gonadotropin hormone (eCG) on the in vitro co-culture of bovine spermatogonial stem cell with Sertoli cells","volume":"28","author":"Kashfi","year":"2019","journal-title":"Comp. Clin. Pathol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1080\/19396368.2017.1358774","article-title":"In vitro effects of melatonin on colonization of neonate mouse spermatogonial stem cells","volume":"63","author":"Navid","year":"2017","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_97","first-page":"5954635","article-title":"Melatonin protects goat spermatogonial stem cells against oxidative damage during cryopreservation by improving antioxidant capacity and inhibiting mitochondrial apoptosis pathway","volume":"31","author":"Feng","year":"2020","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"e14729","DOI":"10.1111\/rda.14729","article-title":"Low testosterone concentration improves colonisation and viability in the co-cultured goat spermatogonial stem cell with Sertoli cells","volume":"59","author":"Salimi","year":"2024","journal-title":"Reprod. Domest. Anim."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"108","DOI":"10.4314\/sajas.v48i1.13","article-title":"Optimization of in vitro culture and transfection condition of bovine primary spermatogonial stem cells","volume":"48","author":"Jafarnejad","year":"2018","journal-title":"S. Afr. J. Anim. Sci."},{"key":"ref_100","first-page":"29","article-title":"Antioxidant effects of selenium on seminiferous tubules of immature mice testis","volume":"17","author":"Kushki","year":"2015","journal-title":"Zahedan J. Res. Med. Sci."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"106916","DOI":"10.1016\/j.domaniend.2025.106916","article-title":"From spermatogenesis to fertilisation: The role of melatonin on ram spermatozoa","volume":"91","author":"Casao","year":"2025","journal-title":"Domest. Anim. Endocrinol."},{"key":"ref_102","first-page":"e135750","article-title":"In Vitro culture of ovine spermatogonial stem cells: Effects of grape seed extracts and vitamin C","volume":"11","author":"Zolfaghari","year":"2024","journal-title":"Gene Cell Tissue"},{"key":"ref_103","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":"Ogawa","year":"2000","journal-title":"Nat. Med."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"R71","DOI":"10.1530\/REP-14-0249","article-title":"Xenografting of testicular tissue pieces: Twelve years of an in vivo spermatogenesis system","volume":"148","author":"Arregui","year":"2014","journal-title":"Reproduction"},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Vurchio, V., Colombo, M., Pasquariello, R., and Luvoni, G.C. (2025). Cryopreservation and culture strategies for testicular tissue and cells in small and large animals. Front. Vet. Sci., 12.","DOI":"10.3389\/fvets.2025.1638248"},{"key":"ref_106","doi-asserted-by":"crossref","unstructured":"Han, Z., Liu, X., Wang, H., Qazi, I.H., Wang, L., Du, R., Dai, X., and Xu, C. (2025). Testicular tissue cryopreservation and transplantation as a strategy for feline conservation: A review of research advances. Front. Vet. Sci., 12.","DOI":"10.3389\/fvets.2025.1572150"},{"key":"ref_107","doi-asserted-by":"crossref","unstructured":"Tomcy, T.A., Binsila, B., Sadikh, M., Krishnappa, B., Ramachandran, N., Arangasamy, A., Aranganathan, V., and Selvaraju, S. (2025). Fetal bovine serum in cryomedia protects sheep spermatogonial stem cells and preserves stemness characteristics during cryopreservation. Vitr. Cell Dev. Biol. Anim., 21.","DOI":"10.1007\/s11626-025-01100-8"},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Yang, F., Zhao, J., Li, Y., Niu, C., and Zheng, Y. (2025). Cryopreservation of spermatogonial stem cells: An overview of cryoprotectants. Reprod. Biomed. Online, 51.","DOI":"10.1016\/j.rbmo.2025.105023"},{"key":"ref_109","doi-asserted-by":"crossref","unstructured":"Fathi, S., Nazari, H., Arabi, M., Afzali, A., and Ahmadi, E. (2025). The antioxidant capacity and protective ability of astaxanthin in cryopreservation of mouse spermatogonial stem cells. Cryobiology, 120.","DOI":"10.1016\/j.cryobiol.2025.105261"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s44164-025-00085-8","article-title":"A comparative analysis of vitrification and two slow freezing methods for gonocyte-containing neonatal calf testicular tissue and subsequent in vitro culture","volume":"4","author":"Tang","year":"2025","journal-title":"Vitr. Model"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.cryobiol.2023.01.001","article-title":"Germplasm cryopreservation in bulls: Effects of gonadal tissue type, cryoprotectant agent, and freezing-thawing rates on sperm quality parameters","volume":"110","author":"Aponte","year":"2023","journal-title":"Cryobiology"},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Kaya, C., Esin, B., Akar, M., Can, C., and \u00c7evik, M. (2024). Investigation of the efficacy of different cryoprotectants in the freezing of testicular tissue and epididymal sperm: Spermatogonial parameters, tissue viability and PARP-1 gene expression. Cryobiology, 117.","DOI":"10.1016\/j.cryobiol.2024.104982"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"24195","DOI":"10.1073\/pnas.2010102117","article-title":"Donor-derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males","volume":"117","author":"Ciccarelli","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_114","doi-asserted-by":"crossref","unstructured":"Blank, M.H., Kawaoku, A.J.T., Rui, B.R., Carreira, A.C.O., Hamilton, T.R.S., Goissis, M.D., and Pereira, R.J.G. (2024). Successful xenotransplantation of testicular cells following fractionated chemotherapy of recipient birds. Sci. Rep., 14.","DOI":"10.1038\/s41598-023-45019-0"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1002\/mrd.21147","article-title":"Transgenic sperm produced by electrotransfection and allogeneic transplantation of chicken fetal spermatogonial stem cells","volume":"77","author":"Yu","year":"2010","journal-title":"Mol. Reprod. Dev."},{"key":"ref_116","doi-asserted-by":"crossref","unstructured":"Zeng, W., Tang, L., Bondareva, A., Honaramooz, A., Tanco, V., Dores, C., Megee, S., Modelski, M., Rodriguez-Sosa, J.R., and Paczkowski, M. (2013). Viral transduction of male germline stem cells results in transgene transmission after germcell transplantation in pigs. Biol. Reprod., 88.","DOI":"10.1095\/biolreprod.112.104422"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"926","DOI":"10.1002\/j.1939-4640.2004.tb03163.x","article-title":"A game of cat and mouse: Xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host","volume":"25","author":"Snedaker","year":"2004","journal-title":"J. Androl."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/j.theriogenology.2024.09.022","article-title":"Potential of mesenchymal stromal\/stem cells and spermatogonial stem cells for survival and colonization in bull recipient testes after allogenic transplantation","volume":"230","author":"Segunda","year":"2024","journal-title":"Theriogenology"},{"key":"ref_119","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":"ref_120","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":"ref_121","doi-asserted-by":"crossref","first-page":"669","DOI":"10.4252\/wjsc.v7.i4.669","article-title":"Spermatogonial stem cells: Current biotechnological advances in reproduction and regenerative medicine","volume":"7","author":"Aponte","year":"2015","journal-title":"World J. Stem Cells"},{"key":"ref_122","doi-asserted-by":"crossref","unstructured":"Zhao, X., Wan, W., Zhang, X., Wu, Z., and Yang, H. (2021). Spermatogonial Stem Cell Transplantation in Large Animals. Animals, 11.","DOI":"10.3390\/ani11040918"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1016\/j.tibtech.2023.03.020","article-title":"Chimaeras, complementation, and controlling the male germline","volume":"41","author":"Oback","year":"2023","journal-title":"Trends Biotechnol."},{"key":"ref_124","doi-asserted-by":"crossref","unstructured":"Lara, N.M.L., Goldsmith, T., Rodriguez-Villamil, P., Ongaratto, F., Solin, S., Webster, D., Ganbaatar, U., Hodgson, S., Corbi\u00e8re, S.M.A.S., and Bondareva, A. (2023). DAZL Knockout Pigs as Recipients for Spermatogonial Stem Cell Transplantation. Cells, 12.","DOI":"10.3390\/cells12212582"},{"key":"ref_125","doi-asserted-by":"crossref","unstructured":"Du, H., Li, Y., Ni, A., Liu, S., Chen, J., and Sun, Y. (2024). Research Progress in the Establishment of Sterile Hosts and Their Usage in Conservation of Poultry Genetic Resources. Agriculture, 14.","DOI":"10.3390\/agriculture14071111"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/j.theriogenology.2019.10.007","article-title":"Moderate hypoxia modulates ABCG2 to promote the proliferation of mouse spermatogonial stem cells by maintaining mild ROS levels","volume":"145","author":"Wang","year":"2020","journal-title":"Theriogenology"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"e14561","DOI":"10.1111\/rda.14561","article-title":"Expression pattern of germ cell markers in cryptorchid stallion Testes","volume":"59","author":"Shakeel","year":"2024","journal-title":"Reprod. Dom. Anim."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1186\/s13287-019-1335-5","article-title":"High temperature suppressed SSC self-renewal through S phase cell cycle arrest but not apoptosis","volume":"10","author":"Wang","year":"2019","journal-title":"Stem Cell Res. Ther."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.metabol.2018.03.022","article-title":"Endocrine disruptors and testicular function","volume":"86","author":"Lymperi","year":"2018","journal-title":"Metabolism"},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1016\/0140-6736(93)90953-E","article-title":"Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract?","volume":"341","author":"Sharpe","year":"1993","journal-title":"Lancet"},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.reprotox.2021.12.007","article-title":"In vitro impact of genistein and mono(2-ethylhexyl) phthalate (MEHP) on the eicosanoid pathway in spermatogonial stem cells","volume":"107","author":"TranGuzman","year":"2022","journal-title":"Reprod. Toxicol."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"154","DOI":"10.5534\/wjmh.230166","article-title":"Bisphenol analogs downregulate the self-renewal potential of spermatogonial stem cells","volume":"43","author":"Kim","year":"2025","journal-title":"World J. Mens. Health"},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"2397","DOI":"10.1007\/s00204-025-04025-z","article-title":"Mechanisms of bisphenol A and its analogs as endocrine disruptors via nuclear receptors and related signaling pathways","volume":"99","year":"2025","journal-title":"Arch. Toxicol."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1080\/19768354.2022.2061592","article-title":"Transcriptome alterations in spermatogonial stem cells exposed to bisphenol A","volume":"26","author":"Ahn","year":"2022","journal-title":"Anim. Cells Syst."},{"key":"ref_135","doi-asserted-by":"crossref","unstructured":"Cao, Y., Wang, J., Li, X., Liu, B., Li, C., Sun, Y., and Zou, K. (2023). Gastrodin protects porcine Sertoli cells from zearalenone-induced abnormal secretion of glial cell line-derived neurotrophic factor through the NOTCH signaling pathway. Reprod. Biol., 23.","DOI":"10.1016\/j.repbio.2023.100781"},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"101308","DOI":"10.1016\/j.mam.2024.101308","article-title":"Impacts of cancer therapy on male fertility: Past and present","volume":"100","author":"Duffin","year":"2024","journal-title":"Mol. Asp. Med."},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.toxrep.2020.12.023","article-title":"Chemotherapy induced damage to spermatogonial stem cells in prepubertal mouse in vitro impairs long-term spermatogenesis","volume":"8","author":"Lopes","year":"2021","journal-title":"Toxicol. Rep."},{"key":"ref_138","doi-asserted-by":"crossref","unstructured":"Tharmalingam, M.D., Matilionyte, G., Wallace, W.H.B., Stukenborg, J.B., Jahnukainen, K., Oliver, E., Goriely, A., Lane, S., Guo, J., and Cairns, B. (2020). Cisplatin and carboplatin result in similar gonadotoxicity in immature human testis with implications for fertility preservation in childhood cancer. BMC Med., 18.","DOI":"10.1186\/s12916-020-01844-y"},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1111\/j.1469-7580.2009.01122.x","article-title":"The seminiferous epithelium cycle and its duration in different breeds of dog (Canis familiaris)","volume":"215","author":"Soares","year":"2009","journal-title":"J. Anat."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.scr.2018.04.009","article-title":"Spermatogonial stem cells and spermatogenesis in mice, monkeys and men","volume":"29","author":"Fayomi","year":"2018","journal-title":"Stem Cell Res."},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1111\/rda.12848","article-title":"Immunolocalization of proteins in the spermatogenesis process of canine","volume":"52","author":"Pieri","year":"2016","journal-title":"Reprod. Domest. Anim."},{"key":"ref_142","doi-asserted-by":"crossref","unstructured":"Lee, K.H., Lee, R., Lee, W.Y., Kim, D.H., Chung, H.J., Kim, J.H., Kim, N.H., Choi, S.H., Kim, J.H., and Song, H. (2014). Identification and in vitro derivation of spermatogonia in beagle testis. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0109963"},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.anireprosci.2017.08.017","article-title":"Analysis of putative biomarkers of undifferentiated spermatogonia in dog testis","volume":"185","author":"Lee","year":"2017","journal-title":"Anim. Reprod. Sci."},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1186\/s13287-019-1250-9","article-title":"Xenotransplantation of canine spermatogonial stem cells (cSSCs) regulated by FSH promotes spermatogenesis in infertile mice","volume":"10","author":"Pieri","year":"2019","journal-title":"Stem Cell Res. Ther."},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"2437","DOI":"10.1016\/j.febslet.2011.06.013","article-title":"FSH acts on the proliferation of type a spermatogonia via Nur77 that increases GDNF expression in the Sertoli cells","volume":"15","author":"Ding","year":"2011","journal-title":"FEBS Lett."},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1677\/joe.1.06634","article-title":"FSH regulates the formation of adherens junctions and ectoplasmic specialisations between rat Sertoli cells in vitro and in vivo","volume":"189","author":"Sluka","year":"2006","journal-title":"J. Endocrinol."},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/S0093-691X(97)00415-9","article-title":"Use of in vitro systems to study male germ cell development in neonatal rats","volume":"49","author":"Orth","year":"1998","journal-title":"Theriogenology"},{"key":"ref_148","doi-asserted-by":"crossref","unstructured":"Kasimanickam, V.R., and Kasimanickam, R.K. (2022). Sertoli, Leydig, and spermatogonial cells\u2019 specific gene and protein expressions as dog testes evolve from immature into mature states. Animals, 12.","DOI":"10.3390\/ani12030271"},{"key":"ref_149","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1530\/REP-09-0513","article-title":"THY1 is a conserved marker of undifferentiated spermatogonia in the pre-pubertal bull testis","volume":"139","author":"Reding","year":"2010","journal-title":"Reproduction"},{"key":"ref_150","doi-asserted-by":"crossref","unstructured":"Tarnawa, E.D., Baker, M.D., Aloisio, G.M., Carr, B.R., and Castrillon, D.H. (2013). Gonadal expression of foxo1, but not foxo3, is conserved in diverse mammalian species. Biol. Reprod., 88.","DOI":"10.1095\/biolreprod.112.105791"},{"key":"ref_151","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1136\/vr.152.16.502","article-title":"Incidence of cryptorchidism in dogs and cats","volume":"152","author":"Yates","year":"2003","journal-title":"Vet. Rec."},{"key":"ref_152","doi-asserted-by":"crossref","first-page":"257","DOI":"10.5625\/lar.2016.32.4.257","article-title":"Establishment of a surgically induced cryptorchidism canine recipient model for spermatogonial stem cell transplantation","volume":"32","author":"Lee","year":"2016","journal-title":"Lab. Anim. Res."},{"key":"ref_153","doi-asserted-by":"crossref","unstructured":"Jhun, H., Lee, W.Y., Park, J.K., Hwang, S.G., and Park, H.J. (2022). Transcriptomic analysis of testicular gene expression in a dog model of experimentally induced cryptorchidism. Cells, 11.","DOI":"10.3390\/cells11162476"},{"key":"ref_154","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1007\/s00345-009-0462-5","article-title":"Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress-mediated apoptosis","volume":"28","author":"Shiraishi","year":"2010","journal-title":"World J. Urol."},{"key":"ref_155","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1002\/j.1939-4640.1997.tb01896.x","article-title":"Heat stress causes testicular germ cell apoptosis in adult mice","volume":"18","author":"Yin","year":"1997","journal-title":"J. Androl."},{"key":"ref_156","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1007\/978-1-61779-436-0_11","article-title":"Spermatogenesis in cryptorchidism","volume":"825","author":"Agoulnik","year":"2012","journal-title":"Methods Mol. Biol."},{"key":"ref_157","doi-asserted-by":"crossref","unstructured":"Reifarth, L., K\u00f6rber, H., Packeiser, E.M., and Goericke-Pesch, S. (2023). Detection of spermatogonial stem cells in testicular tissue of dogs with chronic asymptomatic orchitis. Front. Vet. Sci., 10.","DOI":"10.3389\/fvets.2023.1205064"},{"key":"ref_158","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1111\/vec.12087","article-title":"Cryptococcosis as an emerging systemic mycosis in dogs","volume":"23","author":"Vorathavorn","year":"2013","journal-title":"J. Vet. Emerg. Crit. Care"},{"key":"ref_159","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1080\/02681219580000601","article-title":"Cryptococcosis in dogs: A retrospective study of 20 consecutive cases","volume":"33","author":"Malik","year":"1995","journal-title":"J. Med. Vet. Mycol."},{"key":"ref_160","doi-asserted-by":"crossref","first-page":"1716","DOI":"10.2460\/javma.2004.225.1716","article-title":"Clinicopathologic features of an unusual outbreak of cryptococcosis in dogs, cats, ferrets, and a bird: 38 cases (January to July 2003)","volume":"225","author":"Lester","year":"2004","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"ref_161","doi-asserted-by":"crossref","unstructured":"Kuberka, M., Przadka, P., and Dzimira, S. (2025). Concurrent Leydig and Sertoli Cell Tumors Associated with Testicular Mycosis in a Dog: A Case Report and Literature Review. Pathogens, 14.","DOI":"10.3390\/pathogens14080752"},{"key":"ref_162","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1530\/REP-08-0226","article-title":"Production of donor-derived sperm after spermatogonial stem cell transplantation in the dog","volume":"136","author":"Kim","year":"2008","journal-title":"Reproduction"},{"key":"ref_163","doi-asserted-by":"crossref","first-page":"264","DOI":"10.5625\/lar.2017.33.3.264","article-title":"Dose-dependent effects of busulfan on dog testes in preparation for spermatogonial stem cell transplantation","volume":"33","author":"Hur","year":"2017","journal-title":"Lab. Anim. Res."},{"key":"ref_164","doi-asserted-by":"crossref","unstructured":"Lee, K.H., Lee, W.Y., Kim, D.H., Lee, S.H., Do, J.T., Park, C., Kim, J.H., Choi, Y.S., and Song, H. (2016). Vitrified canine testicular cells allow the formation of spermatogonial stem cells and seminiferous tubules following their xenotransplantation into nude mice. Sci. Rep., 6.","DOI":"10.1038\/srep21919"},{"key":"ref_165","doi-asserted-by":"crossref","unstructured":"Machado da Silva, L.D. (2022). Canine and Feline Testicular Preservation. Animals, 12.","DOI":"10.3390\/ani12010124"},{"key":"ref_166","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1016\/j.fertnstert.2025.06.022","article-title":"The use of testicular organoids in advancing future treatments for male factor infertility","volume":"124","author":"Stukenborg","year":"2025","journal-title":"Fertil. Steril."},{"key":"ref_167","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/s13567-020-00891-w","article-title":"Progress and challenges in developing organoids in farm animal species for the study of reproduction and their applications to reproductive biotechnologies","volume":"52","author":"Bourdon","year":"2021","journal-title":"Vet. Res."}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/12\/11\/1047\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,3]],"date-time":"2025-11-03T14:27:27Z","timestamp":1762180047000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/12\/11\/1047"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,1]]},"references-count":167,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["vetsci12111047"],"URL":"https:\/\/doi.org\/10.3390\/vetsci12111047","relation":{},"ISSN":["2306-7381"],"issn-type":[{"value":"2306-7381","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,1]]}}}