精原干细胞微环境研究进展

doi:10.16288/j.yczz.22-136

遗传 ›› 2022, Vol. 44 ›› Issue (12): 1103-1116.doi: 10.16288/j.yczz.22-136

精原干细胞微环境研究进展

余志鑫(), 李鹏宇, 李凯, 缪时英, 王琳芳, 宋伟()

中国医学科学院基础医学研究所，北京协和医学院基础学院，医学分子生物学国家重点实验室，北京 100005

收稿日期:2022-05-05 修回日期:2022-07-30 出版日期:2022-12-20 发布日期:2022-09-01
通讯作者: 宋伟 E-mail:15619830345@163.com;songwei@ibms.pumc.edu.cn
作者简介:余志鑫，在读硕士研究生，专业方向：生物化学与分子生物学。E-mail: 15619830345@163.com
基金资助:
国家重点研发计划项目(2018YFC1003500);国家自然科学基金项目(31970794);国家自然科学基金项目(32000586)

Progress on spermatogonial stem cell microenvironment

Zhixin Yu(), Pengyu Li, Kai Li, Shiying Miao, Linfang Wang, Wei Song()

State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, Beijing 100005, China

Received:2022-05-05 Revised:2022-07-30 Online:2022-12-20 Published:2022-09-01
Contact: Song Wei E-mail:15619830345@163.com;songwei@ibms.pumc.edu.cn
Supported by:
the National Key Research and Development Program(2018YFC1003500);the National Natural Science Foundation of China(31970794);the National Natural Science Foundation of China(32000586)

摘要/Abstract

摘要：

精原干细胞(spermatogonia stem cells, SSCs)是一类在睾丸中具有长期自我更新和分化潜能的生殖细胞(germ cells, GCs)，即位于基底膜上的组织干细胞，其自我更新和分化受到周围微环境的调控。近年来对SSCs的研究取得了一系列重要进展，为临床治疗部分男性不育患者带来了曙光。其中，微环境对SSCs的调节功能的研究尤为重要，微环境负责整合不同类型的细胞成分、细胞外基质、细胞外调节分子及激素等对SSCs的作用，从而调节SSCs命运。关于SSCs微环境的研究已开始逐步成为干细胞研究的主要内容之一。本文主要对小鼠(Mus musculus)SSCs微环境的细胞组成、调控因子以及特点等研究现状进行了综述，为深入研究SSCs微环境的结构和功能提供背景资料，希望在未来能够通过多种研究模式复用，发现更为丰富的细胞表型和微环境因子。

关键词: 精原干细胞, 微环境, 自我更新, 分化, 激素调控

Abstract:

Spermatogonial stem cells (SSCs) are germ cells (GCs) with long-term self-renewal and differentiation potential in testis, namely tissue stem cells located on the basement membrane, whose self-renewal and differentiation are regulated by the surrounding microenvironment. In recent years, the research of SSCs has made a series of important progress, which brings the hope for the clinical treatment of some male infertility patients. Among them, the microenvironment is particularly important in regulating SSCs. The microenvironment is responsible for integrating the effects of different types of cell components, extracellular matrix, extracellular regulatory molecules and hormones on SSCs, thus regulating the fate of SSCs. The research on SSCs microenvironment has gradually become one of the main contents of stem cell research. In this review, we mainly summarize the cell composition, regulatory factors and characteristics of mouse SSCs microenvironment, thereby providing background information for in-depth study on the structure and function of SSCs microenvironment, and opportunity to find more abundant cell phenotypes and microenvironmental factors through multiple research models in the future.

Key words: spermatogonia stem cells, microenvironment, self-renewal, differentiation, hormone regulation

余志鑫, 李鹏宇, 李凯, 缪时英, 王琳芳, 宋伟. 精原干细胞微环境研究进展[J]. 遗传, 2022, 44(12): 1103-1116.

Zhixin Yu, Pengyu Li, Kai Li, Shiying Miao, Linfang Wang, Wei Song. Progress on spermatogonial stem cell microenvironment[J]. Hereditas(Beijing), 2022, 44(12): 1103-1116.

图/表 2

参考文献 129

[1]	Li LH, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol, 2005, 21: 605-631. pmid: 16212509
[2]	Cai YH, Wang JJ, Zou K. The progresses of spermatogonial stem cells sorting using fluorescence-activated cell sorting. Stem Cell Rev Rep, 2020, 16(1): 94-102. doi: 10.1007/s12015-019-09929-9 pmid: 31792769
[3]	Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc Natl Acad Sci USA, 2001, 98(11): 6186-6191. doi: 10.1073/pnas.111158198
[4]	Fayomi AP, Orwig KE. Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Res, 2018, 29: 207-214. doi: S1873-5061(18)30110-7 pmid: 29730571
[5]	Oatley JM, Brinster RL. The germline stem cell niche unit in mammalian testes. Physiol Rev, 2012, 92(2): 577-595. doi: 10.1152/physrev.00025.2011 pmid: 22535892
[6]	Chen LY, Willis WD, Eddy EM. Targeting the gdnf gene in peritubular myoid cells disrupts undifferentiated spermatogonial cell development. Proc Natl Acad Sci USA, 2016, 113(7): 1829-1834. doi: 10.1073/pnas.1517994113
[7]	Lord T, Oatley JM. A revised A(single) model to explain stem cell dynamics in the mouse male germline. Reproduction, 2017, 154(2): R55-R64. doi: 10.1530/REP-17-0034
[8]	de Rooij DG. The nature and dynamics of spermatogonial stem cells. Development, 2017, 144(17): 3022-3030. doi: 10.1242/dev.146571 pmid: 28851723
[9]	Ehmcke J, Schlatt S. A revised model for spermatogonial expansion in man: lessons from non-human primates. Reproduction, 2006, 132(5): 673-680. pmid: 17071768
[10]	Wu ZR, Luby-Phelps K, Bugde A, Molyneux LA, Denard B, Li WH, Süel GM, Garbers DL. Capacity for stochastic self-renewal and differentiation in mammalian spermatogonial stem cells. J Cell Biol, 2009, 187(4): 513-524. doi: 10.1083/jcb.200907047 pmid: 19948499
[11]	Hara K, Nakagawa T, Enomoto H, Suzuki M, Yamamoto M, Simons BD, Yoshida S. Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell, 2014, 14(5): 658-672. doi: 10.1016/j.stem.2014.01.019 pmid: 24792118
[12]	Nakagawa T, Nabeshima YI, Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell, 2007, 12(2): 195-206. pmid: 17276338
[13]	Wong MD, Jin ZG, Xie T. Molecular mechanisms of germline stem cell regulation. Annu Rev Genet, 2005, 39: 173-195. pmid: 16285857
[14]	Schofield R. The relationship between the spleen colony- forming cell and the haemopoietic stem cell. Blood Cells, 1978, 4(1-2): 7-25. pmid: 747780
[15]	Guo JT, Grow EJ, Mlcochova H, Maher GJ, Lindskog C, Nie XC, Guo YX, Takei Y, Yun JN, Cai L, Kim R, Carrell DT, Goriely A, Hotaling JM, Cairns BR. The adult human testis transcriptional cell atlas. Cell Res, 2018, 28(12): 1141-1157. doi: 10.1038/s41422-018-0099-2 pmid: 30315278
[16]	Mäkelä JA, Hobbs RM. Molecular regulation of spermatogonial stem cell renewal and differentiation. Reproduction, 2019, 158(5): R169-R187. doi: 10.1530/REP-18-0476
[17]	Yoshida S. Mouse spermatogenesis reflects the unity and diversity of tissue stem cell niche systems. Cold Spring Harb Perspect Biol, 2020, 12(12): a036186. doi: 10.1101/cshperspect.a036186
[18]	Oakberg EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat, 1956, 99(3): 507-516. doi: 10.1002/aja.1000990307
[19]	Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci, 1952, 55(4): 548-573. doi: 10.1111/j.1749-6632.1952.tb26576.x
[20]	Hess RA. Quantitative and qualitative characteristics of the stages and transitions in the cycle of the rat seminiferous epithelium: light microscopic observations of perfusion-fixed and plastic-embedded testes. Biol Reprod, 1990, 43(3): 525-542. pmid: 2271734
[21]	Kitadate Y, Jörg DJ, Tokue M, Maruyama A, Ichikawa R, Tsuchiya S, Segi-Nishida E, Nakagawa T, Uchida A, Kimura-Yoshida C, Mizuno S, Sugiyama F, Azami T, Ema M, Noda C, Kobayashi S, Matsuo I, Kanai Y, Nagasawa T, Sugimoto Y, Takahashi S, Simons BD, Yoshida S. Competition for mitogens regulates spermatogenic stem cell homeostasis in an open niche. Cell Stem Cell, 2019, 24(1): 79-92.e6. doi: S1934-5909(18)30549-6 pmid: 30581080
[22]	Yoshida S, Sukeno M, Nabeshima YI. A vasculature- associated niche for undifferentiated spermatogonia in the mouse testis. Science, 2007, 317(5845): 1722-1726. pmid: 17823316
[23]	Oatley MJ, Racicot KE, Oatley JM. Sertoli cells dictate spermatogonial stem cell niches in the mouse testis. Biol Reprod, 2011, 84(4): 639-645. doi: 10.1095/biolreprod.110.087320 pmid: 21084712
[24]	Lord T, Nixon B. Metabolic changes accompanying spermatogonial stem cell differentiation. Dev Cell, 2020, 52(4): 399-411. doi: S1534-5807(20)30015-0 pmid: 32097651
[25]	Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell, 2010, 7(2): 150-161. doi: 10.1016/j.stem.2010.07.007 pmid: 20682444
[26]	Cheng CY, Wong EWP, Yan HHN, Mruk DD. Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances. Mol Cell Endocrinol, 2010, 315(1-2): 49-56. doi: 10.1016/j.mce.2009.08.004 pmid: 19682538
[27]	Watanabe S, Kanatsu-Shinohara M, Ogonuki N, Matoba S, Ogura A, Shinohara T. In vivo genetic manipulation of spermatogonial stem cells and their microenvironment by Adeno-associated viruses. Stem Cell Reports, 2018, 10(5): 1551-1564. doi: S2213-6711(18)30132-2 pmid: 29628393
[28]	Garcia TX, Farmaha JK, Kow S, Hofmann MC. RBPJ in mouse sertoli cells is required for proper regulation of the testis stem cell niche. Development, 2014, 141(23): 4468-4478. doi: 10.1242/dev.113969 pmid: 25406395
[29]	Kanatsu-Shinohara M, Ogonuki N, Matoba S, Ogura A, Shinohara T. Autologous transplantation of spermatogonial stem cells restores fertility in congenitally infertile mice. Proc Natl Acad Sci USA, 2020, 117(14): 7837-7844. doi: 10.1073/pnas.1914963117
[30]	Nishimura H, L'Hernault SW. Spermatogenesis. Curr Biol, 2017, 27(18): R988-R994. doi: 10.1016/j.cub.2017.07.067
[31]	Rebourcet D, O'Shaughnessy PJ, Monteiro A, Milne L, Cruickshanks L, Jeffrey N, Guillou F, Freeman TC, Mitchell RT, Smith LB. Sertoli cells maintain leydig cell number and peritubular myoid cell activity in the adult mouse testis. PLoS One, 2014, 9(8): e105687. doi: 10.1371/journal.pone.0105687
[32]	Wang YQ, Batool A, Chen SR, Liu YX. GATA4 is a negative regulator of contractility in mouse testicular peritubular myoid cells. Reproduction, 2018, 156(4): 343-351.
[33]	Chen LY, Brown PR, Willis WB, Eddy EM. Peritubular myoid cells participate in male mouse spermatogonial stem cell maintenance. Endocrinology, 2014, 155(12): 4964-4974. doi: 10.1210/en.2014-1406
[34]	Spinnler K, Köhn FM, Schwarzer U, Mayerhofer A. Glial cell line-derived neurotrophic factor is constituteively produced by human testicular peritubular cells and may contribute to the spermatogonial stem cell niche in man. Hum Reprod, 2010, 25(9): 2181-2187. doi: 10.1093/humrep/deq170
[35]	Zhou R, Wu J, Liu B, Jiang YQ, Chen W, Li J, He QY, He ZP. The roles and mechanisms of leydig cells and myoid cells in regulating spermatogenesis. Cell Mol Life Sci, 2019, 76(14): 2681-2695. doi: 10.1007/s00018-019-03101-9 pmid: 30980107
[36]	Bhang DH, Kim BJ, Kim BG, Schadler K, Baek KH, Kim YH, Hsiao W, Ding BS, Rafii S, Weiss MJ, Chou ST, Kolon TF, Ginsberg JP, Ryu BY, Ryeom S. Testicular endothelial cells are a critical population in the germline stem cell niche. Nat Commun, 2018, 9(1): 4379. doi: 10.1038/s41467-018-06881-z pmid: 30348976
[37]	Del Punta K, Charreau EH, Pignataro OP. Nitric oxide inhibits leydig cell steroidogenesis. Endocrinology, 1996, 137(12): 5337-5343. pmid: 8940355
[38]	Kim YH, Oh MG, Bhang DH, Kim BJ, Jung SE, Kim SM, Dohr G, Kim SU, Ryeom S, Ryu BY. Testicular endothelial cells promote self-renewal of spermatogonial stem cells in rats. Biol Reprod, 2019, 101(2): 360-367. doi: 10.1093/biolre/ioz105
[39]	O'Hara L, Smith LB. Androgen receptor roles in spermatogenesis and infertility. Best Pract Res Clin Endocrinol Metab, 2015, 29(4): 595-605. doi: 10.1016/j.beem.2015.04.006 pmid: 26303086
[40]	Guo JT, Sosa E, Chitiashvili T, Nie XC, Rojas EJ, Oliver E, Donor Connect, Plath K, Hotaling JM, Stukenborg JB, Clark AT, Cairns BR. Single-cell analysis of the developing human testis reveals somatic niche cell specification and fetal germline stem cell establishment. Cell Stem Cell, 2021, 28(4): 764-778.e4. doi: 10.1016/j.stem.2020.12.004 pmid: 33453151
[41]	Tripiciano A, Filippini A, Ballarini F, Palombi F. Contractile response of peritubular myoid cells to prostaglandin F2alpha. Mol Cell Endocrinol, 1998, 138(1-2): 143-150. pmid: 9685223
[42]	Nicholson HD, Hardy MP. Luteinizing hormone differentially regulates the secretion of testicular oxytocin and testosterone by purified adult rat leydig cells in vitro. Endocrinology, 1992, 130(2): 671-677. pmid: 1733715
[43]	Huang YH, Chin CC, Ho HN, Chou CK, Shen CN, Kuo HC, Wu TJ, Wu YC, Hung YC, Chang CC, Ling TY. Pluripotency of mouse spermatogonial stem cells maintained by IGF-1-dependent pathway. FASEB J, 2009, 23(7): 2076-2087.
[44]	Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self- renewal. Development, 2009, 136(7): 1191-1199. doi: 10.1242/dev.032243 pmid: 19270176
[45]	Wang S, Wang XX, Wu YJ, Han CS. IGF-1R signaling is essential for the proliferation of cultured mouse spermatogonial stem cells by promoting the G2/M progression of the cell cycle. Stem Cells Dev, 2015, 24(4): 471-483. doi: 10.1089/scd.2014.0376 pmid: 25356638
[46]	Hume DA, Halpin D, Charlton H, Gordon S. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of endocrine organs. Proc Natl Acad Sci USA, 1984, 81(13): 4174-4177. doi: 10.1073/pnas.81.13.4174
[47]	DeFalco T, Potter SJ, Williams AV, Waller B, Kan MJ, Capel B. Macrophages contribute to the spermatogonial niche in the adult testis. Cell Rep, 2015, 12(7): 1107-1119. doi: 10.1016/j.celrep.2015.07.015 pmid: 26257171
[48]	Fehervari Z. Testicular macrophage origin. Nat Immunol, 2017, 18(10): 1067. doi: 10.1038/ni.3846 pmid: 28926535
[49]	Lokka E, Lintukorpi L, Cisneros-Montalvo S, Mäkelä JA, Tyystjärvi S, Ojasalo V, Gerke H, Toppari J, Rantakari P, Salmi M. Generation, localization and functions of macrophages during the development of testis. Nat Commun, 2020, 11(1): 4375. doi: 10.1038/s41467-020-18206-0 pmid: 32873797
[50]	Wang M, Yang YL, Cansever D, Wang YM, Kantores C, Messiaen S, Moison D, Livera G, Chakarov S, Weinberger T, Stremmel C, Fijak M, Klein B, Pleuger C, Lian ZX, Ma WT, Liu QZ, Klee K, Händler K, Ulas T, Schlitzer A, Schultze JL, Becher B, Greter M, Liu ZY, Ginhoux F, Epelman S, Schulz C, Meinhardt A, Bhushan S. Two populations of self-maintaining monocyte- independent macrophages exist in adult epididymis and testis. Proc Natl Acad Sci USA, 2021, 118(1): e2013686117.
[51]	Indumathy S, Pueschl D, Klein B, Fietz D, Bergmann M, Schuppe HC, Da Silva N, Loveland BE, Hickey MJ, Hedger MP, Loveland KL. Testicular immune cell populations and macrophage polarisation in adult male mice and the influence of altered activin A levels. J Reprod Immunol, 2020, 142: 103204. doi: 10.1016/j.jri.2020.103204
[52]	Mossadegh-Keller N, Gentek R, Gimenez G, Bigot S, Mailfert S, Sieweke MH. Developmental origin and maintenance of distinct testicular macrophage populations. J Exp Med, 2017, 214(10): 2829-2841. doi: 10.1084/jem.20170829
[53]	Potter SJ, DeFalco T. Role of the testis interstitial compartment in spermatogonial stem cell function. Reproduction, 2017, 153(4): R151-R162. doi: 10.1530/REP-16-0588
[54]	Wang M, Liu XX, Chang G, Chen YD, An G, Yan LY, Gao S, Xu YW, Cui YL, Dong J, Chen YH, Fan XY, Hu YQ, Song K, Zhu XH, Gao Y, Yao ZK, Bian SH, Hou Y, Lu JH, Wang R, Fan Y, Lian Y, Tang WH, Wang YP, Liu JQ, Zhao LM, Wang LY, Liu ZT, Yuan RP, Shi YJ, Hu BQ, Ren XL, Tang FC, Zhao XY, Qiao J. Single-cell RNA sequencing analysis reveals sequential cell fate transition during human spermatogenesis. Cell Stem Cell, 2018, 23(4): 599-614.e4. doi: S1934-5909(18)30392-8 pmid: 30174296
[55]	Green CD, Ma QY, Manske GL, Shami AN, Zheng XN, Marini S, Moritz L, Sultan C, Gurczynski SJ, Moore BB, Tallquist MD, Li JZ, Hammoud SS. A comprehensive roadmap of murine spermatogenesis defined by single-cell RNA-seq. Dev Cell, 2018, 46(5): 651-667.e10. doi: S1534-5807(18)30636-1 pmid: 30146481
[56]	Zhao JX, Lu P, Wan C, Huang YP, Cui MM, Yang XY, Hu YQ, Zheng Y, Dong J, Wang M, Zhang S, Liu ZT, Bian SH, Wang XM, Wang R, Ren SF, Wang DZ, Yao ZK, Chang G, Tang FC, Zhao XY. Cell-fate transition and determination analysis of mouse male germ cells throughout development. Nat Commun, 2021, 12(1): 6839. doi: 10.1038/s41467-021-27172-0 pmid: 34824237
[57]	Sharma M, Braun RE. Cyclical expression of GDNF is required for spermatogonial stem cell homeostasis. Development, 2018, 145(5): dev151555.
[58]	Tokue M, Ikami K, Mizuno S, Takagi C, Miyagi A, Takada R, Noda C, Kitadate Y, Hara K, Mizuguchi H, Sato T, Taketo MM, Sugiyama F, Ogawa T, Kobayashi S, Ueno N, Takahashi S, Takada S, Yoshida S. SHISA 6 confers resistance to differentiation-promoting Wnt/β-catenin signaling in mouse spermatogenic stem cells. Stem Cell Reports, 2017, 8(3): 561-575. doi: S2213-6711(17)30021-8 pmid: 28196692
[59]	Meng X, Lindahl M, Hyvönen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science, 2000, 287(5457): 1489-1493. pmid: 10688798
[60]	Uchida A, Kishi K, Aiyama Y, Miura K, Takase HM, Suzuki H, Kanai-Azuma M, Iwamori T, Kurohmaru M, Tsunekawa N, Kanai Y. In vivo dynamics of GFRα1- positive spermatogonia stimulated by GDNF signals using a bead transplantation assay. Biochem Biophys Res Commun, 2016, 476(4): 546-552. doi: 10.1016/j.bbrc.2016.05.160
[61]	Masaki K, Sakai M, Kuroki S, Jo JI, Hoshina K, Fujimori Y, Oka K, Amano T, Yamanaka T, Tachibana M, Tabata Y, Shiozawa T, Ishizuka O, Hochi S, Takashima S. FGF2 has distinct molecular functions from GDNF in the mouse germline niche. Stem Cell Reports, 2018, 10(6): 1782-1792. doi: S2213-6711(18)30143-7 pmid: 29681540
[62]	Zhou Z, Shirakawa T, Ohbo K, Sada A, Wu Q, Hasegawa K, Saba R, Saga Y. RNA binding protein Nanos2 organizes post-transcriptional buffering system to retain primitive state of mouse spermatogonial stem cells. Dev Cell, 2015, 34(1): 96-107. doi: 10.1016/j.devcel.2015.05.014 pmid: 26120033
[63]	Sariola H, Saarma M. Novel functions and signalling pathways for GDNF. J Cell Sci, 2003, 116(Pt 19): 3855-3862. doi: 10.1242/jcs.00786
[64]	Jain S, Naughton CK, Yang M, Strickland A, Vij K, Encinas M, Golden J, Gupta A, Heuckeroth R, Johnson EM, Milbrandt J. Mice expressing a dominant-negative ret mutation phenocopy human hirschsprung disease and delineate a direct role of ret in spermatogenesis. Development, 2004, 131(21): 5503-5513. pmid: 15469971
[65]	Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod, 2006, 74(2): 314-321. pmid: 16237148
[66]	Kanatsu-Shinohara M, Shinohara T. Spermatogonial stem cell self-renewal and development. Annu Rev Cell Dev Biol, 2013, 29: 163-187. doi: 10.1146/annurev-cellbio-101512-122353 pmid: 24099084
[67]	Sadri-Ardekani H, Mizrak SC, Korver CM, Roepers-Gajadien HL, Koruji M, Hovingh S, de Reijke TM, de la Rosette JJMCH, van der Veen F, de Rooij DG, Repping S, van Pelt AMM. Propagation of human spermatogonial stem cells in vitro. JAMA, 2009, 302(19): 2127-2134. doi: 10.1001/jama.2009.1689 pmid: 19920237
[68]	Parker N, Laychur A, Sukwani M, Orwig KE, Oatley JM, Zhang C, Rutaganira FU, Shokat K, Wright WW. Spermatogonial stem cell numbers are reduced by transient inhibition of GDNF signaling but restored by self-renewing replication when signaling resumes. Stem Cell Reports, 2021, 16(3): 597-609. doi: 10.1016/j.stemcr.2021.01.015
[69]	Zhang Y, Wang S, Wang XX, Liao SY, Wu YJ, Han CS. Endogenously produced FGF2 is essential for the survival and proliferation of cultured mouse spermatogonial stem cells. Cell Res, 2012, 22(4): 773-776. doi: 10.1038/cr.2012.17 pmid: 22290421
[70]	Sawaied A, Arazi E, AbuElhija A, Lunenfeld E, Huleihel M. 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, 2021, 22(5): 2325. doi: 10.3390/ijms22052325
[71]	Otsuka R, Wada H, Seino KI. IL-34, the rationale for its expression in physiological and pathological conditions. Semin Immunol, 2021, 54: 101517. doi: 10.1016/j.smim.2021.101517
[72]	Sato T, Yokonishi T, Komeya M, Katagiri K, Kubota Y, Matoba S, Ogonuki N, Ogura A, Yoshida S, Ogawa T. Testis tissue explantation cures spermatogenic failure in c-Kit ligand mutant mice. Proc Natl Acad Sci USA, 2012, 109(42): 16934-16938. doi: 10.1073/pnas.1211845109
[73]	Kokkinaki M, Lee TL, He ZP, Jiang JJ, Golestaneh N, Hofmann MC, Chan WY, Dym M. The molecular signature of spermatogonial stem/progenitor cells in the 6-day-old mouse testis. Biol Reprod, 2009, 80(4): 707-717. doi: 10.1095/biolreprod.108.073809 pmid: 19109221
[74]	Tao K, Sun Y, Chao YC, Xing L, Leng LZ, Zhou D, Zhu WB, Fan LQ. β-estradiol promotes the growth of primary human fetal spermatogonial stem cells via the induction of stem cell factor in sertoli cells. J Assist Reprod Genet, 2021, 38(9): 2481-2490. doi: 10.1007/s10815-021-02240-y
[75]	Yang QE, Kim D, Kaucher A, Oatley MJ, Oatley JM. CXCL12-CXCR4 signaling is required for the maintenance of mouse spermatogonial stem cells. J Cell Sci, 2013, 126(Pt 4): 1009-1020.
[76]	Kanatsu-Shinohara M, Inoue K, Takashima S, Takehashi M, Ogonuki N, Morimoto H, Nagasawa T, Ogura A, Shinohara T. Reconstitution of mouse spermatogonial stem cell niches in culture. Cell Stem Cell, 2012, 11(4): 567-578. doi: 10.1016/j.stem.2012.06.011 pmid: 23040482
[77]	Han R, Shang KG. Germ cells in the murine embryonic development. Hereditas(Beijing), 2002, 24(1): 77-81.
	韩嵘, 尚克刚. 小鼠生殖细胞的胚胎发育. 遗传, 2002, 24(1): 77-81.
[78]	Jenab S, Morris PL. Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat sertoli but not germ cells. Endocrinology, 1998, 139(4): 1883-1890. pmid: 9528974
[79]	Curley M, Milne L, Smith S, Atanassova N, Rebourcet D, Darbey A, Hadoke PWF, Wells S, Smith LB. Leukemia inhibitory factor-receptor is dispensable for prenatal testis development but is required in sertoli cells for normal spermatogenesis in mice. Sci Rep, 2018, 8(1): 11532. doi: 10.1038/s41598-018-30011-w pmid: 30068994
[80]	Piquet-Pellorce C, Dorval-Coiffec I, Pham MD, Jégou B. Leukemia inhibitory factor expression and regulation within the testis. Endocrinology, 2000, 141(3): 1136-1141. pmid: 10698190
[81]	Kim YH, Kang HG, Kim BJ, Jung SE, Karmakar PC, Kim SM, Hwang S, Ryu BY. Enrichment and in vitro culture of spermatogonial stem cells from pre- pubertal monkey testes. Tissue Eng Regen Med, 2017, 14(5): 557-566. doi: 10.1007/s13770-017-0058-x
[82]	Medrano JV, Rombaut C, Simon C, Pellicer A, Goossens E. Human spermatogonial stem cells display limited proliferation in vitro under mouse spermatogonial stem cell culture conditions. Fertil Steril, 2016, 106(6): 1539-1549.e8. doi: S0015-0282(16)62478-0 pmid: 27490045
[83]	Aponte PM, Soda T, Teerds KJ, Mizrak SC, van de Kant HJ, de Rooij DG. Propagation of bovine spermatogonial stem cells in vitro. Reproduction, 2008, 136(5): 543-557. doi: 10.1530/REP-07-0419 pmid: 18663014
[84]	Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Yoshida S, Toyokuni S, Lee J, Ogura A, Shinohara T. Leukemia inhibitory factor enhances formation of germ cell colonies in neonatal mouse testis culture. Biol Reprod, 2007, 76(1): 55-62. pmid: 17021343
[85]	Martin-Inaraja M, Ferreira M, Taelman J, Eguizabal C, Chuva De Sousa Lopes SM. Improving in vitro culture of human male fetal germ cells. Cells, 2021, 10(8): 2033. doi: 10.3390/cells10082033
[86]	Morimoto H, Kanastu-Shinohara M, Ogonuki N, Kamimura S, Ogura A, Yabe-Nishimura C, Mori Y, Morimoto T, Watanabe S, Otsu K, Yamamoto T, Shinohara T. ROS amplification drives mouse spermatogonial stem cell self-renewal. Life Sci Alliance, 2019, 2(2): e201900374.
[87]	Morimoto H, Kanatsu-Shinohara M, Shinohara T. ROS- generating oxidase Nox3 regulates the self-renewal of mouse spermatogonial stem cells. Biol Reprod, 2015, 92(6): 147. doi: 10.1095/biolreprod.114.127647 pmid: 25947060
[88]	Morimoto H, Iwata K, Ogonuki N, Inoue K, Atsuo O, Kanatsu-Shinohara M, Morimoto T, Yabe-Nishimura C, Shinohara T. ROS are required for mouse spermatogonial stem cell self-renewal. Cell Stem Cell, 2013, 12(6): 774-786. doi: 10.1016/j.stem.2013.04.001 pmid: 23746981
[89]	Morimoto H, Yamamoto T, Miyazaki T, Ogonuki N, Ogura A, Tanaka T, Kanatsu-Shinohara M, Yabe-Nishimura C, Zhang HL, Pommier Y, Trumpp A, Shinohara T. An interplay of NOX1-derived ROS and oxygen determines the spermatogonial stem cell self-renewal efficiency under hypoxia. Genes Dev, 2021, 35(3-4): 250-260. doi: 10.1101/gad.339903.120
[90]	Cui WH, He XL, Zhai XH, Zhang H, Zhang YW, Jin F, Song XM, Wu DQ, Shi QH, Li L. CARF promotes spermatogonial self-renewal and proliferation through wnt signaling pathway. Cell Discov, 2020, 6(1): 85. doi: 10.1038/s41421-020-00212-7 pmid: 33298864
[91]	Yang F, Whelan EC, Guan XB, Deng BQ, Wang S, Sun JC, Avarbock MR, Wu X, Brinster RL. FGF9 promotes mouse spermatogonial stem cell proliferation mediated by p38 MAPK signalling. Cell Prolif, 2021, 54(1): e12933.
[92]	Sawaied A, Lunenfeld E, Huleihel M. Interleukin-34, a novel paracrine/autocrine factor in mouse testis, and its possible role in the development of spermatogonial cells in vitro. Int J Mol Sci, 2020, 21(21): 8143. doi: 10.3390/ijms21218143
[93]	Teletin M, Vernet N, Yu JS, Klopfenstein M, Jones JW, Féret B, Kane MA, Ghyselinck NB, Mark M. Two functionally redundant sources of retinoic acid secure spermatogonia differentiation in the seminiferous epithelium. Development, 2019, 146(1): dev170225.
[94]	Kent T, Arnold SL, Fasnacht R, Rowsey R, Mitchell D, Hogarth CA, Isoherranen N, Griswold MD. ALDH enzyme expression is independent of the spermatogenic cycle, and their inhibition causes misregulation of murine spermatogenic processes. Biol Reprod, 2016, 94(1): 12. doi: 10.1095/biolreprod.115.131458 pmid: 26632609
[95]	Endo T, Romer KA, Anderson EL, Baltus AE, de Rooij DG, Page DC. Periodic retinoic acid-STRA8 signaling intersects with periodic germ-cell competencies to regulate spermatogenesis. Proc Natl Acad Sci USA, 2015, 112(18): E2347-E2356.
[96]	Wang S, Wang XX, Ma LF, Lin XW, Zhang DQ, Li Z, Wu YJ, Zheng CW, Feng X, Liao SY, Feng YM, Chen J, Hu XJ, Wang M, Han CS. Retinoic acid is sufficient for the in vitro induction of mouse spermatocytes. Stem Cell Reports, 2016, 7(1): 80-94. doi: 10.1016/j.stemcr.2016.05.013 pmid: 27346680
[97]	Endo T, Freinkman E, de Rooij DG, Page DC. Periodic production of retinoic acid by meiotic and somatic cells coordinates four transitions in mouse spermatogenesis. Proc Natl Acad Sci USA, 2017, 114(47): E10132-E10141.
[98]	Wang S, Wang X, Ma L, Lin X, Zhang D, Li Z, Wu Y, Zheng C, Feng X, Liao S, Feng Y, Chen J, Hu X, Wang M, Han C. Retinoic acid is sufficient for the in vitro induction of mouse spermatocytes. Stem Cell Reports, 2016, 7(1): 80-94. doi: 10.1016/j.stemcr.2016.05.013 pmid: 27346680
[99]	Mahabadi JA, Tameh AA, Talaei SA, Karimian M, Rahiminia T, Enderami SE, Gheibi Hayat SM, Nikzad H. Retinoic acid and/or progesterone differentiate mouse induced pluripotent stem cells into male germ cells in vitro. J Cell Biochem, 2020, 121(3): 2159-2169. doi: 10.1002/jcb.29439 pmid: 31646671
[100]	Nagano M, Ryu BY, Brinster CJ, Avarbock MR, Brinster RL. Maintenance of mouse male germ line stem cells in vitro. Biol Reprod, 2003, 68(6): 2207-2214. doi: 10.1095/biolreprod.102.014050
[101]	Carlomagno G, van Bragt MPA, Korver CM, Repping S, de Rooij DG, van Pelt AMM. BMP4-induced differentiation of a rat spermatogonial stem cell line causes changes in its cell adhesion properties. Biol Reprod, 2010, 83(5): 742-749. doi: 10.1095/biolreprod.110.085456 pmid: 20650884
[102]	Hai YN, Sun M, Niu MH, Yuan QQ, Guo Y, Li Z, He ZP. BMP4 promotes human sertoli cell proliferation via smad1/5 and ID2/3 pathway and its abnormality is associated with azoospermia. Discov Med, 2015, 19(105): 311-325. pmid: 25977194
[103]	Yang YG, Feng YM, Feng X, Liao SY, Wang XX, Gan HY, Wang LX, Lin XW, Han CS. BMP4 cooperates with retinoic acid to induce the expression of differentiation markers in cultured mouse spermatogonia. Stem Cells Int, 2016, 2016: 9536192.
[104]	Mauduit C, Hamamah S, Benahmed M. Stem cell factor/c-kit system in spermatogenesis. Hum Reprod Update, 1999, 5(5): 535-545. pmid: 10582791
[105]	Ohmura M, Ogawa T, Ono M, Dezawa M, Hosaka M, Kubota Y, Sawada H. Increment of murine spermatogonial cell number by gonadotropin-releasing hormone analogue is independent of stem cell factor c-kit signal. Biol Reprod, 2003, 68(6): 2304-2313. pmid: 12606404
[106]	Figueira MI, Cardoso HJ, Correia S, Maia CJ, Socorro S. The stem cell factor (SCF)/c-KIT system in carcinogenesis of reproductive tissues: what does the hormonal regulation tell us? Cancer Lett, 2017, 405: 10-21. doi: S0304-3835(17)30452-4 pmid: 28751268
[107]	Cardoso HJ, Figueira MI, Socorro S. The stem cell factor (SCF)/c-KIT signalling in testis and prostate cancer. J Cell Commun Signal, 2017, 11(4): 297-307. doi: 10.1007/s12079-017-0399-1 pmid: 28656507
[108]	Chui K, Trivedi A, Cheng CY, Cherbavaz DB, Dazin PF, Huynh ALT, Mitchell JB, Rabinovich GA, Noble- Haeusslein LJ, John CM. Characterization and functionality of proliferative human sertoli cells. Cell Transplant, 2011, 20(5): 619-635.
[109]	Nasimi M, Jorsaraei SGA, Fattahi E, Tabari MG, Neyshaburi EZ. SCF improves in vitro differentiation of SSCs through transcriptionally up-regulating PRTM1, STRA8, c-KIT, PIWIL2, and OCT4 genes. Reprod Sci, 2021, 28(4): 963-972. doi: 10.1007/s43032-020-00326-z
[110]	Dolci S, Pellegrini M, Di Agostino S, Geremia R, Rossi P. Signaling through extracellular signal-regulated kinase is required for spermatogonial proliferative response to stem cell factor. J Biol Chem, 2001, 276(43): 40225-40233. doi: 10.1074/jbc.M105143200 pmid: 11502745
[111]	Hakovirta H, Yan W, Kaleva M, Zhang F, Vänttinen K, Morris PL, Söder M, Parvinen M, Toppari J. Function of stem cell factor as a survival factor of spermatogonia and localization of messenger ribonucleic acid in the rat seminiferous epithelium. Endocrinology, 1999, 140(3): 1492-1498. pmid: 10067878
[112]	Abé K, Jin Y, Yamamoto T, Abé S. Human recombinant stem cell factor promotes spermatogonial proliferation, but not meiosis initiation in organ culture of newt testis fragments. Biochem Biophys Res Commun, 2002, 294(3): 695-699. doi: 10.1016/S0006-291X(02)00537-5
[113]	Alpaugh WF, Voigt AL, Dardari R, Su L, Al Khatib I, Shin W, Goldsmith TM, Coyle KM, Tang LA, Shutt TE, Klein C, Biernaskie J, Dobrinski I. Loss of ubiquitin carboxy- terminal hydrolase l1 impairs long-term differentiation competence and metabolic regulation in murine spermatogonial stem cells. Cells, 2021, 10(9): 2265. doi: 10.3390/cells10092265
[114]	Wei YD, Yang DH, Du XM, Yu XW, Zhang MF, Tang FR, Ma FL, Li N, Bai CL, Li GP, Hua JL. Interaction between DMRT1 and PLZF protein regulates self-renewal and proliferation in male germline stem cells. Mol Cell Biochem, 2021, 476(2): 1123-1134. doi: 10.1007/s11010-020-03977-3 pmid: 33200378
[115]	Zhang T, Oatley J, Bardwell VJ, Zarkower D. DMRT1 is required for mouse spermatogonial stem cell maintenance and replenishment. PLoS Genet, 2016, 12(9): e1006293. doi: 10.1371/journal.pgen.1006293
[116]	Barrios F, Filipponi D, Campolo F, Gori M, Bramucci F, Pellegrini M, Ottolenghi S, Rossi P, Jannini EA, Dolci S. SOHLH1 and SOHLH2 control Kit expression during postnatal male germ cell development. J Cell Sci, 2012, 125(Pt 6): 1455-1464. doi: 10.1242/jcs.092593 pmid: 22328502
[117]	Suzuki H, Ahn HW, Chu TJ, Bowden W, Gassei K, Orwig K, Rajkovic A. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Dev Biol, 2012, 361(2): 301-312. doi: 10.1016/j.ydbio.2011.10.027 pmid: 22056784
[118]	Song WX, Shi XL, Xia Q, Yuan M, Liu JX, Hao KY, Qian YJ, Zhao XD, Zou K. PLZF suppresses differentiation of mouse spermatogonial progenitor cells via binding of differentiation associated genes. J Cell Physiol, 2020, 235(3): 3033-3042. doi: 10.1002/jcp.29208 pmid: 31541472
[119]	Du XM, Wu SY, Wei YD, Yu XW, Ma FL, Zhai YX, Yang DH, Zhang MF, Liu WQ, Zhu HJ, Wu J, Liao MZ, Li N, Bai CL, Li GP, Hua JL. PAX7 promotes CD49f-positive dairy goat spermatogonial stem cells’ self-renewal. J Cell Physiol, 2021, 236(2): 1481-1493. doi: 10.1002/jcp.29954
[120]	Tan K, Song HW, Wilkinson MF. RHOX10 drives mouse spermatogonial stem cell establishment through a transcription factor signaling cascade. Cell Rep, 2021, 36(3): 109423. doi: 10.1016/j.celrep.2021.109423
[121]	Binsila BK, Selvaraju S, Ghosh SK, Ramya L, Arangasamy A, Ranjithkumaran R, Bhatta R. EGF, GDNF, and IGF-1 influence the proliferation and stemness of ovine spermatogonial stem cells in vitro. J Assist Reprod Genet, 2020, 37(10): 2615-2630. doi: 10.1007/s10815-020-01912-5
[122]	Yao JF, Zuo HY, Gao J, Wang MM, Wang D, Li XD. The effects of IGF-1 on mouse spermatogenesis using an organ culture method. Biochem Biophys Res Commun, 2017, 491(3): 840-847. doi: 10.1016/j.bbrc.2017.05.125
[123]	Neirijnck Y, Kühne F, Mayère C, Pavlova E, Sararols P, Foti M, Atanassova N, Nef S. Tumor suppressor PTEN regulates negatively sertoli cell proliferation, testis size, and sperm production in vivo. Endocrinology, 2019, 160(2): 387-398. doi: 10.1210/en.2018-00892 pmid: 30576429
[124]	Shen GQ, Wu RP, Liu B, Dong WH, Tu Z, Yang JR, Xu Z, Pan TJ. Upstream and downstream mechanisms for the promoting effects of IGF-1 on differentiation of spermatogonia to primary spermatocytes. Life Sci, 2014, 101(1-2): 49-55. doi: 10.1016/j.lfs.2014.02.016 pmid: 24582811
[125]	Smith EP, Dickson BA, Chernausek SD. Insulin-like growth factor binding protein-3 secretion from cultured rat sertoli cells: dual regulation by follicle stimulating hormone and insulin-like growth factor-I. Endocrinology, 1990, 127(6): 2744-2751.
[126]	Oduwole OO, Peltoketo H, Poliandri A, Vengadabady L, Chrusciel M, Doroszko M, Samanta L, Owen L, Keevil B, Rahman NA, Huhtaniemi IT. Constitutively active follicle-stimulating hormone receptor enables androgen-independent spermatogenesis. J Clin Invest, 2018, 128(5): 1787-1792. doi: 10.1172/JCI96794 pmid: 29584617
[127]	Yokonishi T, McKey J, Ide S, Capel B. Sertoli cell ablation and replacement of the spermatogonial niche in mouse. Nat Commun, 2020, 11(1): 40. doi: 10.1038/s41467-019-13879-8 pmid: 31896751
[128]	Zou X, He YH, He JY, Wang Y, Shu DM, Luo CL. Optimization of transfection conditions of chicken primordial germ cells. Hereditas(Beijing), 2021, 43(3): 280-288. doi: 10.16288/j.yczz.20-212 pmid: 33724212
	邹娴, 何燕华, 何静怡, 王艳, 舒鼎铭, 罗成龙. 鸡原始生殖细胞转染条件优化. 遗传, 2021, 43(3): 280-288. doi: 10.16288/j.yczz.20-212 pmid: 33724212
[129]	Chen WY, Yan YD, Luan XJ, Wang M, Fang J. Functional analysis of CG8005 gene in Drosophila testis. Hereditas(Beijing), 2020, 42(11): 1122-1132. doi: 10.16288/j.yczz.20-163 pmid: 33229318
	陈万银, 颜一丹, 栾晓瑾, 王敏, 方杰. CG8005基因在果蝇睾丸生殖细胞中的功能分析. 遗传, 2020, 42(11): 1122-1132. doi: 10.16288/j.yczz.20-163 pmid: 33229318

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