{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T18:54:24Z","timestamp":1780080864451,"version":"3.54.0"},"reference-count":38,"publisher":"Springer Science and Business Media LLC","issue":"12","license":[{"start":{"date-parts":[[2022,3,23]],"date-time":"2022-03-23T00:00:00Z","timestamp":1647993600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2022,3,23]],"date-time":"2022-03-23T00:00:00Z","timestamp":1647993600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"funder":[{"DOI":"10.13039\/501100005851","name":"Shahid Beheshti University of Medical Sciences","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100005851","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Reprod. Sci."],"published-print":{"date-parts":[[2022,12]]},"DOI":"10.1007\/s43032-022-00884-4","type":"journal-article","created":{"date-parts":[[2022,3,23]],"date-time":"2022-03-23T16:03:59Z","timestamp":1648051439000},"page":"3394-3403","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["miR-106b-5p Intensifies the Proliferative Potential of Spermatogonial Stem Cells as a Prerequisite for Male Infertility Treatment"],"prefix":"10.1007","volume":"29","author":[{"given":"Amir Hossein","family":"Hasani Fard","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mahmoud","family":"Valizadeh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zohreh","family":"Mazaheri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seyed Jalil","family":"Hosseini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,3,23]]},"reference":[{"issue":"Suppl 10","key":"884_CR1","first-page":"68","volume":"90","author":"G Guerri","year":"2020","unstructured":"Guerri G, Maniscalchi T, Barati S, Gerli S, Di Renzo GC, Della Morte C, et al. Non-syndromic monogenic female infertility. Acta Bio Medica: Atenei Parmensis. 2020;90(Suppl 10):68.","journal-title":"Acta Bio Medica: Atenei Parmensis"},{"issue":"3","key":"884_CR2","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.rbmo.2017.12.005","volume":"36","author":"A Bracke","year":"2018","unstructured":"Bracke A, Peeters K, Punjabi U, Hoogewijs D, Dewilde S. A search for molecular mechanisms underlying male idiopathic infertility. Reprod Biomed Online. 2018;36(3):327\u201339.","journal-title":"Reprod Biomed Online"},{"issue":"2","key":"884_CR3","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/j.mcna.2017.10.008","volume":"102","author":"MM Pan","year":"2017","unstructured":"Pan MM, Hockenberry MS, Kirby EW, Lipshultz LI. Male infertility diagnosis and treatment in the era of in vitro fertilization and intracytoplasmic sperm injection. Med Clin North Am. 2017;102(2):337\u201347.","journal-title":"Med Clin North Am"},{"key":"884_CR4","doi-asserted-by":"publisher","first-page":"1155","DOI":"10.3389\/fphys.2019.01155","volume":"10","author":"L Dong","year":"2019","unstructured":"Dong L, Kristensen SG, Hildorf S, Gul M, Clasen-Linde E, Fedder J, et al. Propagation of spermatogonial stem cell-like cells from infant boys. Front Physiol. 2019;10:1155.","journal-title":"Front Physiol"},{"issue":"6","key":"884_CR5","doi-asserted-by":"publisher","first-page":"1374","DOI":"10.1002\/jcb.24479","volume":"114","author":"Y Mei","year":"2013","unstructured":"Mei Y, Bian C, Li J, Du Z, Zhou H, Yang Z, et al. miR-21 modulates the ERK\u2013MAPK signaling pathway by regulating SPRY2 expression during human mesenchymal stem cell differentiation. J Cell Biochem. 2013;114(6):1374\u201384.","journal-title":"J Cell Biochem"},{"key":"884_CR6","doi-asserted-by":"crossref","unstructured":"Vlajkovi\u0107 S, \u010cukuranovi\u0107 R, Dakovi\u0107 Bjelakovi\u0107 M, Stefanovi\u0107 V. Possible therapeutic use of spermatogonial stem cells in the treatment of male infertility: a brief overview. The Scientific World Journal. 2012;2012.","DOI":"10.1100\/2012\/374151"},{"issue":"3","key":"884_CR7","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1093\/humupd\/dmaa003","volume":"26","author":"M Gul","year":"2020","unstructured":"Gul M, Hildorf S, Dong L, Thorup J, Hoffmann ER, Jensen CFS, et al. Review of injection techniques for spermatogonial stem cell transplantation. Hum Reprod Update. 2020;26(3):368\u201391.","journal-title":"Hum Reprod Update"},{"key":"884_CR8","doi-asserted-by":"crossref","unstructured":"Lian J, Tian H, Liu L, Zhang X, Li W, Deng Y, et al. Downregulation of microRNA-383 is associated with male infertility and promotes testicular embryonal carcinoma cell proliferation by targeting IRF1. Cell death & disease. 2010;1(11):e94-e.","DOI":"10.1038\/cddis.2010.70"},{"issue":"4","key":"884_CR9","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1093\/molehr\/gaaa016","volume":"26","author":"A Vashisht","year":"2020","unstructured":"Vashisht A, Gahlay G. Using miRNAs as diagnostic biomarkers for male infertility: Opportunities and challenges. Mol Hum Reprod. 2020;26(4):199\u2013214.","journal-title":"Mol Hum Reprod"},{"issue":"1","key":"884_CR10","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1111\/andr.12714","volume":"8","author":"A Salas-Huetos","year":"2020","unstructured":"Salas-Huetos A, James E, Aston K, Carrell D, Jenkins T, Yeste M. The role of miRNAs in male human reproduction: A systematic review. Andrology. 2020;8(1):7\u201326.","journal-title":"Andrology"},{"issue":"8","key":"884_CR11","doi-asserted-by":"publisher","first-page":"670","DOI":"10.1002\/bies.201200019","volume":"34","author":"MA Li","year":"2012","unstructured":"Li MA, He L. microRNAs as novel regulators of stem cell pluripotency and somatic cell reprogramming. BioEssays. 2012;34(8):670\u201380.","journal-title":"BioEssays"},{"issue":"1","key":"884_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12958-021-00758-5","volume":"19","author":"M Khanehzad","year":"2021","unstructured":"Khanehzad M, Nourashrafeddin SM, Abolhassani F, Kazemzadeh S, Madadi S, Shiri E, et al. MicroRNA-30a-5p promotes differentiation in neonatal mouse spermatogonial stem cells (SSCs). Reprod Biol Endocrinol. 2021;19(1):1\u201314.","journal-title":"Reprod Biol Endocrinol"},{"key":"884_CR13","doi-asserted-by":"crossref","unstructured":"Tong M-H, Mitchell DA, McGowan SD, Evanoff R, Griswold MD. Two miRNA Clusters, Mir-17\u201392 (Mirc1) and Mir-106b-25 (Mirc3), Are Involved in the Regulation of Spermatogonial Differentiation in Mice1. Biology of Reproduction. 2012;86(3).","DOI":"10.1095\/biolreprod.111.096313"},{"issue":"1","key":"884_CR14","first-page":"111","volume":"41","author":"T Ogawa","year":"2003","unstructured":"Ogawa T, Arechaga J, Avarbock M, Brinster R. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol. 2003;41(1):111\u201322.","journal-title":"Int J Dev Biol"},{"issue":"1","key":"884_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13578-015-0034-x","volume":"5","author":"W Zhou","year":"2015","unstructured":"Zhou W, Shao H, Zhang D, Dong J, Cheng W, Wang L, et al. PTEN signaling is required for the maintenance of spermatogonial stem cells in mouse, by regulating the expressions of PLZF and UTF1. Cell Biosci. 2015;5(1):1\u201310.","journal-title":"Cell Biosci"},{"issue":"1","key":"884_CR16","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep25438","volume":"6","author":"V Olariu","year":"2016","unstructured":"Olariu V, L\u00f6vkvist C, Sneppen K. Nanog, Oct4 and Tet1 interplay in establishing pluripotency. Sci Rep. 2016;6(1):1\u201311.","journal-title":"Sci Rep"},{"issue":"6","key":"884_CR17","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1093\/molehr\/gaaa027","volume":"26","author":"A Hurtado","year":"2020","unstructured":"Hurtado A, Palomino R, Georg I, Lao M, Real FM, Carmona FD, et al. Deficiency of the onco-miRNA cluster, miR-106b\u223c 25, causes oligozoospermia and the cooperative action of miR-106b\u223c 25 and miR-17\u223c 92 is required to maintain male fertility. Mol Hum Reprod. 2020;26(6):389\u2013401.","journal-title":"Mol Hum Reprod"},{"key":"884_CR18","doi-asserted-by":"crossref","unstructured":"Khuu C, Utheim TP, Sehic A. The three paralogous microRNA clusters in development and disease, miR-17\u201392, miR-106a-363, and miR-106b-25. Scientifica. 2016;2016.","DOI":"10.1155\/2016\/1379643"},{"issue":"10","key":"884_CR19","doi-asserted-by":"publisher","first-page":"2205","DOI":"10.1002\/stem.1474","volume":"31","author":"Z He","year":"2013","unstructured":"He Z, Jiang J, Kokkinaki M, Tang L, Zeng W, Gallicano I, et al. MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem cells. 2013;31(10):2205\u201317.","journal-title":"Stem cells"},{"issue":"8","key":"884_CR20","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1002\/mrd.22843","volume":"84","author":"YL Huang","year":"2017","unstructured":"Huang YL, Huang GY, Lv J, Pan LN, Luo X, Shen J. miR-100 promotes the proliferation of spermatogonial stem cells via regulating Stat3. Mol Reprod Dev. 2017;84(8):693\u2013701.","journal-title":"Mol Reprod Dev"},{"issue":"2","key":"884_CR21","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1530\/rep.1.01075","volume":"132","author":"C Itman","year":"2006","unstructured":"Itman C, Mendis S, Barakat B, Loveland KL. All in the family: TGF-\u03b2 family action in testis development. Reproduction. 2006;132(2):233\u201346.","journal-title":"Reproduction"},{"issue":"2","key":"884_CR22","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1093\/molehr\/gax065","volume":"24","author":"C Rombaut","year":"2017","unstructured":"Rombaut C, Mertes H, Heindryckx B, Goossens E. Human in vitro spermatogenesis from pluripotent stem cells: in need of a stepwise differentiation protocol? Mol Hum Reprod. 2017;24(2):47\u201354.","journal-title":"Mol Hum Reprod"},{"key":"884_CR23","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1016\/j.scr.2017.07.016","volume":"24","author":"C Spiller","year":"2017","unstructured":"Spiller C, Burnet G, Bowles J. Regulation of fetal male germ cell development by members of the TGF\u03b2 superfamily. Stem cell research. 2017;24:174\u201380.","journal-title":"Stem cell research"},{"issue":"8","key":"884_CR24","doi-asserted-by":"publisher","first-page":"13342","DOI":"10.1002\/jcp.28011","volume":"234","author":"M Deng","year":"2019","unstructured":"Deng M, Hou SY, Tong BD, Yin JY, Xiong W. The Smad2\/3\/4 complex binds miR-139 promoter to modulate TGF\u03b2-induced proliferation and activation of human Tenon\u2019s capsule fibroblasts through the Wnt pathway. J Cell Physiol. 2019;234(8):13342\u201352.","journal-title":"J Cell Physiol"},{"key":"884_CR25","doi-asserted-by":"crossref","unstructured":"Hata A, Chen Y-G. TGF-\u03b2 signaling from receptors to Smads. Cold Spring Harbor perspectives in biology. 2016;8(9):a022061.","DOI":"10.1101\/cshperspect.a022061"},{"key":"884_CR26","doi-asserted-by":"crossref","unstructured":"Miyazawa K, Miyazono K. Regulation of TGF-\u03b2 family signaling by inhibitory Smads. Cold Spring Harbor Perspectives in Biology. 2017;9(3):a022095.","DOI":"10.1101\/cshperspect.a022095"},{"key":"884_CR27","doi-asserted-by":"publisher","first-page":"653","DOI":"10.3389\/fcell.2020.00653","volume":"8","author":"J Yang","year":"2020","unstructured":"Yang J, Jiang W. The role of SMAD2\/3 in human embryonic stem cells. Frontiers in Cell and Developmental Biology. 2020;8:653.","journal-title":"Frontiers in Cell and Developmental Biology"},{"issue":"50","key":"884_CR28","doi-asserted-by":"publisher","first-page":"5162","DOI":"10.1038\/onc.2012.11","volume":"31","author":"AL Smith","year":"2012","unstructured":"Smith AL, Iwanaga R, Drasin DJ, Micalizzi DS, Vartuli RL, Tan A-C, et al. The miR-106b-25 cluster targets Smad7, activates TGF-\u03b2 signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene. 2012;31(50):5162\u201371.","journal-title":"Oncogene"},{"issue":"4","key":"884_CR29","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1242\/dev.146928","volume":"144","author":"AR Helsel","year":"2017","unstructured":"Helsel AR, Yang Q-E, Oatley MJ, Lord T, Sablitzky F, Oatley JM. ID4 levels dictate the stem cell state in mouse spermatogonia. Development. 2017;144(4):624\u201334.","journal-title":"Development"},{"issue":"4","key":"884_CR30","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1111\/j.2047-2927.2014.00226.x","volume":"2","author":"C Sachs","year":"2014","unstructured":"Sachs C, Robinson BD, Andres Martin L, Webster T, Gilbert M, Lo HY, et al. Evaluation of candidate spermatogonial markers ID 4 and GPR 125 in testes of adult human cadaveric organ donors. Andrology. 2014;2(4):607\u201314.","journal-title":"Andrology"},{"issue":"2","key":"884_CR31","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41419-018-0335-1","volume":"9","author":"J Zhang","year":"2018","unstructured":"Zhang J, Cao H, Xie J, Fan C, Xie Y, He X, et al. The oncogene Etv5 promotes MET in somatic reprogramming and orchestrates epiblast\/primitive endoderm specification during mESCs differentiation. Cell Death Dis. 2018;9(2):1\u201316.","journal-title":"Cell Death Dis"},{"issue":"11","key":"884_CR32","first-page":"7048","volume":"12","author":"Z Chen","year":"2020","unstructured":"Chen Z, Hong F, Wang Z, Hao D, Yang H. Spermatogonial stem cells are a promising and pluripotent cell source for regenerative medicine. American Journal of Translational Research. 2020;12(11):7048.","journal-title":"American Journal of Translational Research"},{"issue":"8","key":"884_CR33","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1038\/nrurol.2013.145","volume":"10","author":"DJ Katz","year":"2013","unstructured":"Katz DJ, Kolon TF, Feldman DR, Mulhall JP. Fertility preservation strategies for male patients with cancer. Nat Rev Urol. 2013;10(8):463\u201372.","journal-title":"Nat Rev Urol"},{"key":"884_CR34","doi-asserted-by":"crossref","unstructured":"Tang X, Chang C, Hao M, Chen M, Woodley DT, Sch\u00f6nthal AH, et al. Heat shock protein-90alpha (Hsp90\u03b1) stabilizes hypoxia-inducible factor-1\u03b1 (HIF-1\u03b1) in support of spermatogenesis and tumorigenesis. Cancer gene therapy. 2021:1\u201313.","DOI":"10.1038\/s41417-021-00316-6"},{"issue":"16","key":"884_CR35","doi-asserted-by":"publisher","first-page":"3354","DOI":"10.1038\/s41388-020-1222-7","volume":"39","author":"S-Q Luo","year":"2020","unstructured":"Luo S-Q, Xiong D-H, Li J, Li G, Wang Y, Zhang J-M, et al. C1orf35 contributes to tumorigenesis by activating c-MYC transcription in multiple myeloma. Oncogene. 2020;39(16):3354\u201366.","journal-title":"Oncogene"},{"issue":"1","key":"884_CR36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13287-019-1187-z","volume":"10","author":"S Melnik","year":"2019","unstructured":"Melnik S, Werth N, Boeuf S, Hahn E-M, Gotterbarm T, Anton M, et al. Impact of c-MYC expression on proliferation, differentiation, and risk of neoplastic transformation of human mesenchymal stromal cells. Stem Cell Res Ther. 2019;10(1):1\u201318.","journal-title":"Stem Cell Res Ther"},{"issue":"5","key":"884_CR37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41419-021-03739-z","volume":"12","author":"X Yang","year":"2021","unstructured":"Yang X, Shao F, Guo D, Wang W, Wang J, Zhu R, et al. WNT\/\u03b2-catenin-suppressed FTO expression increases m 6 A of c-Myc mRNA to promote tumor cell glycolysis and tumorigenesis. Cell Death Dis. 2021;12(5):1\u201314.","journal-title":"Cell Death Dis"},{"key":"884_CR38","unstructured":"Hasani Fard AH, Kamalipour F, Mazaheri Z, Hosseini SJ. Evaluation Of MiR-106b-5p Expression In The Production Of IPS-Like Cells From Mice SSCs During The Formation Of Teratoma And The Three Embryonic Layers. Cell Journal (Yakhteh). 2022;24(6): In press."}],"container-title":["Reproductive Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s43032-022-00884-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s43032-022-00884-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s43032-022-00884-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,20]],"date-time":"2024-09-20T21:46:56Z","timestamp":1726868816000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s43032-022-00884-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,23]]},"references-count":38,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2022,12]]}},"alternative-id":["884"],"URL":"https:\/\/doi.org\/10.1007\/s43032-022-00884-4","relation":{},"ISSN":["1933-7191","1933-7205"],"issn-type":[{"value":"1933-7191","type":"print"},{"value":"1933-7205","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,23]]},"assertion":[{"value":"1 October 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 February 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 March 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All experiments were approved by the Ethics Committee of Shahid Beheshti University of Medical Sciences and following the Declaration of Helsinki (Approval ID: IR.SBMU.REC1398.073).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"Not applicable.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}}]}}