留言板

尊敬的读者、作者、审稿人, 关于本刊的投稿、审稿、编辑和出版的任何问题, 您可以本页添加留言。我们将尽快给您答复。谢谢您的支持!

姓名
邮箱
手机号码
标题
留言内容
验证码

Production of functional sperm from in vitro-cultured premeiotic spermatogonia in a marine fish

Hong Zhang Wan-Wan Zhang Cheng-Yu Mo Meng-Dan Dong Kun-Tong Jia Wei Liu Mei-Sheng Yi

Hong Zhang, Wan-Wan Zhang, Cheng-Yu Mo, Meng-Dan Dong, Kun-Tong Jia, Wei Liu, Mei-Sheng Yi. Production of functional sperm from in vitro-cultured premeiotic spermatogonia in a marine fish. Zoological Research, 2022, 43(4): 537-551. doi: 10.24272/j.issn.2095-8137.2022.058
Citation: Hong Zhang, Wan-Wan Zhang, Cheng-Yu Mo, Meng-Dan Dong, Kun-Tong Jia, Wei Liu, Mei-Sheng Yi. Production of functional sperm from in vitro-cultured premeiotic spermatogonia in a marine fish. Zoological Research, 2022, 43(4): 537-551. doi: 10.24272/j.issn.2095-8137.2022.058

体外培养中华乌塘鳢精原细胞产生功能性精子

doi: 10.24272/j.issn.2095-8137.2022.058

Production of functional sperm from in vitro-cultured premeiotic spermatogonia in a marine fish

Funds: This work was supported by the National Key R&D Program of China (2018YFD0901205), National Natural Science Foundation of China (31771587, 31970535), and Guangdong Basic and Applied Basic Research Foundation (2020A1515010358)
More Information
  • 摘要: 体外培养生殖干细胞产生功能性配子快速获得种质资源,可缩短育种间隔。在性成熟周期较长的养殖鱼类中,它有望作为一种遗传育种的潜在策略。但在养殖鱼类中体外培养精原细胞产生功能性精子仍然是一种挑战。在该研究中,利用Percoll密度梯度离心从中华乌塘鳢精巢中分离了雄性生殖细胞。经细胞形态和分子标记鉴定表明,得到的细胞主要为减数分裂前精原细胞。随后,通过三维(3D)添加激素(Hor)的培养方法,对分离的高纯度中华乌塘鳢精原细胞进行培养,诱导产生游动精子,其比例为培养细胞的9.4%。人工授精实验结果表明,这些体外产生的精子能与中华乌塘鳢成熟卵子受精并产生正常的后代。该研究还发现,在培养系统中添加褪黑素,可显著提高精子产生效率,达到约16%。进一步研究表明,褪黑激素可能通过ERK1/2信号通路激活细胞周期、精子发生和减数分裂相关信号通路,促进精原细胞分化成功能性精子。该鱼类精原细胞3D培养系统有望作为一种新的干细胞育种策略,加速养殖鱼类遗传育种和种质改良。
  • Figure  1.  Isolation and characterization of premeiotic spermatogonia by Percoll density gradient centrifugation

    A–C: Structure of developing testis used for spermatogenic cell isolation. Whole testis (A); Immunofluorescence of Vasa in testes of 5-month-old males (B, C); Magnified image in panel B (C). Vasa and nucleus are shown in green and red, respectively. SG, spermatogonia; PSP, primary spermatocyte; SSP, secondary spermatocyte; SPD, spermatid; SPZ, spermatozoa. D–F: Representative images of testicular cell suspension (CS) before centrifugation (D) and whole cells in Percoll gradient after centrifugation (E) and in middle layer (F). G, H: Immunofluorescence of Vasa in CS (G) and middle-layer cells (H). I: Proportion of Vasa+ cell in CS and middle-layer cells. J: PCR amplification of different cell markers in CS and top-, middle-, and bottom-layer cells. Bars indicate mean of three biological replicates in at least three independent experiments. Scale bar: 10 μm.

    Figure  2.  In vitro spermatogenesis under different culture conditions

    A–D: Representative images of middle-layer cells after 1, 2, 3, and 4 weeks of culture in 2D and 3D systems in absence (2D, A1–A4; 3D, B1–B4) and presence (2D+Hor, C1–C4; 3D+Hor, D1–D4) of sex hormones. Scale bar: 50 μm. E: PCR amplification of meiosis markers dmc1 and acrosin in cells under different culture conditions at 4 WAC. F, G: DNA content in cells under different culture systems at 4 WAC. β-actin was used as a reference gene. Bars indicate mean of three biological replicates. **: P<0.01.

    Figure  3.  Dynamic changes, expression patterns, and DNA content in spermatogenic cells in 3D+Hor culture system

    A–D: Immunofluorescence of Vasa (green) in spermatogenic cells in 3D+Hor culture system at 1, 2, 3, and 4 WAC, respectively. E: Immunofluorescence of Vasa (red) and EdU (green) in spermatogenic cells in 3D+Hor culture system at 4 WAC. F: Immunofluorescence of Vasa (green) in mature testis. G: PCR analysis of meiosis markers in spermatogenic cells in 3D+Hor culture system at 0, 1, 2, 3, 4, and 5 WAC. H, I: DNA content in cells derived from fresh testis samples and spermatogenic cells in 3D+Hor culture system at 1, 2, 3, 4, and 5 WAC, respectively. J: Representative image of spermatogenic cells in 3D+Hor culture system at 4 WAC. Arrows indicate flagellated sperm. Scale bar: 50 μm (A–F) and 10 μm (J).

    Figure  4.  Representative images of embryos generated from mature oocytes fertilized with fresh sperm or in vitro-derived sperm at 4 WAC (Scale bar: 1 mm)

    Figure  5.  Melatonin promoted spermatogonia proliferation

    A–L: Immunofluorescence of Vasa (red) and EdU (green) in spermatogenic cells in 3D+Hor culture system exposed to 0 (A–C), 0.1 (D–F), 1 (G–I), and 10 (J–L) μmol/L melatonin (Mel), respectively. Scale bar: 20 μm. M–P: Proportion of EdU+, Vasa+, EdU+/Vasa+, and EdU+/Vasa cells in 3D+Hor culture system exposed to different doses of melatonin. Different letters indicate significant differences between groups. Bars indicate mean of three biological replicates in at least three independent experiments. (Q) QPCR analysis of different cell markers in spermatogenic cells in 3D+Hor culture system in absence or presence of 1 μmol/L melatonin. β-actin was used as a reference gene. Bars indicate mean of three biological replicates. *: P<0.05; **: P<0.01; ns: No significant difference. Statistical analysis was performed using one-way ANOVA followed by Tukey’s test (M-P) and Student’s t-test (Q), respectively.

    Figure  6.  Melatonin promoted spermatogonia proliferation via melatonin receptor 1 (MT1)

    A–E: Immunofluorescence of Vasa (green) in cells in 3D+Hor culture system or after exposure to melatonin (3D+Hor+Mel), melatonin and luzindole (3D+Hor+Mel+Luz), melatonin and 4-P-PDOT (3D+Hor+Mel+4PP), and 2-Iodomelatonin (3D+Hor+2-Iod). Scale bar: 20 μm. F: Proportion of Vasa+ cells in 3D+Hor culture system exposed to different stimuli. Bars indicate mean of three biological replicates in at least three independent experiments. G: QPCR analysis of cdk2, cyclin E, and pcna in spermatogenic cells in 3D+Hor culture system after 1 week of exposure to different stimuli. β-actin was used as a reference gene. Bars indicate mean of three biological replicates. Statistical analysis was performed using one-way ANOVA followed by Tukey’s test. Different letters indicate significant differences between groups.

    Figure  7.  Melatonin promoted differentiation of spermatogonia into haploid cells

    A–C: QPCR analysis of spermatogenesis-related markers (A) and meiosis markers (B) in spermatogenic cells in 3D+Hor culture system after 4 weeks of exposure to different stimuli, as well as their corresponding DNA content (C). β-actin was used as a reference gene. Bars indicate mean of three biological replicates. Statistical analysis was performed using one-way ANOVA followed by Tukey’s test. Different letters indicate significant differences between groups.

    Figure  8.  Activation of ERK1/2 signaling pathway is required for spermatogenesis in vitro

    A: Western blot analysis of DMC1, ERK1/2, and pERK1/2 in cells in 3D culture system after 4 weeks of exposure to different stimuli. β-actin was used as an internal control. B–E: QPCR analysis of cdk2, cyclin E, and pcna (B) or meiosis markers (C) and apoptosis-related genes (D) in cells in 3D+Hor culture system after 4 weeks of exposure to different stimuli, as well as their corresponding DNA content (E). β-actin was used as a reference gene. Bars indicate mean of three biological replicates. RX indicates ERK-specific inhibitor ravoxertinib. Statistical analysis was performed using one-way ANOVA followed by Tukey’s test, and different letters indicate significant differences between groups.

    Table  1.   Proportion of embryos at different stages generated from mature oocytes mixed with fresh sperm or cultured cells in 3D+Hor culture system.

    Sperm or cultured cellsEggs (n=3)Cleavage (%)Somite (%)Hatching (%)
    Fresh sperm1 57384.72±6.6578.48±7.7555.09±5.91
    1 WAC741000
    2 WAC6920.66±0.6500
    3 WAC6599.77±4.335.05±1.163.50±0.36
    4 WAC69348.93±8.2331.23±3.2426.88±4.13
    5 WAC74651.68±8.2125.25±1.2219.65±2.31
    下载: 导出CSV

    Table  2.   Proportion of embryos at different stages generated from mature oocytes mixed with fresh sperm or cultured cells in 3D+Hor culture system exposed to different stimuli

    Sperm or cultured cellsEggs (n=3)Cleavage (%)Somite (%)Hatching (%)
    Fresh sperm86175.76±4.1765.14±5.8253.83±5.30
    3D+Hor77340.15±2.7730.19±3.1826.00±3.70
    3D+Hor+Mel71253.44±6.3243.19±4.8738.56±4.86
    3D+Hor+Mel+Luz58242.51±4.2934.57±3.6225.26±3.91
    3D+Hor+2-Iod64758.66±7.2345.74±4.3436.74±3.45
    下载: 导出CSV
  • [1] Abu Elhija M, Lunenfeld E, Schlatt S, Huleihel M. 2012. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian Journal of Andrology, 14(2): 285−293. doi: 10.1038/aja.2011.112
    [2] Ahmad R, Haldar C. 2010. Effect of intra-testicular melatonin injection on testicular functions, local and general immunity of a tropical rodent Funambulus pennanti. Endocrine, 37(3): 479–488.
    [3] Boutin JA, Witt-Enderby PA, Sotriffer C, Zlotos DP. 2020. Melatonin receptor ligands: a pharmaco-chemical perspective. Journal of Pineal Research, 69(3): e12672.
    [4] Cao MJ, Wang YF, Yang F, Li JZ, Qin XS. 2021. Melatonin rescues the reproductive toxicity of low-dose glyphosate-based herbicide during mouse oocyte maturation via the GPER signaling pathway. Journal of Pineal Research, 70(3): e12718.
    [5] Chen M, Cecon E, Karamitri A, Gao WW, Gerbier R, Ahmad R, et al. 2020. Melatonin MT1 and MT2 receptor ERK signaling is differentially dependent on Gi/o and Gq/11 proteins. Journal of Pineal Research, 68(4): e12641.
    [6] Deng SL, Chen SR, Wang ZP, Zhang Y, Tang JX, Li J, et al. 2016. Melatonin promotes development of haploid germ cells from early developing spermatogenic cells of Suffolk sheep under in vitro condition. Journal of Pineal Research, 60(4): 435−447. doi: 10.1111/jpi.12327
    [7] Dong MD, Zhang H, Mo CY, Li WJ, Zhang WW, Jia KT, et al. 2021. The CXC chemokine receptors in four-eyed sleeper (Bostrychus sinensis) and their involvement in responding to skin injury. International Journal of Molecular Sciences, 22(18): 10022. doi: 10.3390/ijms221810022
    [8] Forger NG, Zucker I. 1985. Photoperiodic regulation of reproductive development in male white-footed mice (Peromyscus leucopus) born at different phases of the breeding season. Journal of Reproduction and Fertility, 73(1): 271−278. doi: 10.1530/jrf.0.0730271
    [9] Forsberg M, Madej A. 1990. Effects of melatonin implants on plasma concentrations of testosterone, thyroxine and prolactin in the male silver fox (Vulpes vulpes). Journal of Reproduction and Fertility, 89(1): 351−358. doi: 10.1530/jrf.0.0890351
    [10] Goszczynski DE, Denicol AC, Ross PJ. 2019. Gametes from stem cells: status and applications in animal reproduction. Reproduction in Domestic Animals, 54(S4): 22−31.
    [11] Gui JF, Zhou L, Li XY. 2022. Rethinking fish biology and biotechnologies in the challenge era for burgeoning genome resources and strengthening food security. Water Biology and Security, 1(1): 100002. doi: 10.1016/j.watbs.2021.11.001
    [12] Hamazaki N, Kyogoku H, Araki H, Miura F, Horikawa C, Hamada N, et al. 2021. Reconstitution of the oocyte transcriptional network with transcription factors. Nature, 589(7841): 264−269. doi: 10.1038/s41586-020-3027-9
    [13] Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. 2011. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell, 146(4): 519−532. doi: 10.1016/j.cell.2011.06.052
    [14] Higaki S, Nishie T, Todo T, Teshima R, Kusumi K, Mitsumori R, et al. 2021. Germ cell–specific expression of Venus by Tol2-mediated transgenesis in endangered endemic cyprinid Honmoroko (Gnathopogon caerulescens). Journal of Fish Biology, 99(4): 1341−1347. doi: 10.1111/jfb.14840
    [15] Higaki S, Shimada M, Kawamoto K, Todo T, Kawasaki T, Tooyama I, et al. 2017. In vitro differentiation of fertile sperm from cryopreserved spermatogonia of the endangered endemic cyprinid honmoroko (Gnathopogon caerulescens). Scientific Reports, 7: 42852. doi: 10.1038/srep42852
    [16] Hong WS, Chen SX, Zheng WY, Xiao Y, Zhang QY. 2006. Hermaphroditism in cultured Chinese black sleeper (Bostrichthys sinensis L. ). Journal of the World Aquaculture Society, 37(4): 363−369. doi: 10.1111/j.1749-7345.2006.00049.x
    [17] Hong YH, Liu TM, Zhao HB, Xu HY, Wang WJ, Liu R, et al. 2004. Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proceedings of the National Academy of Sciences of the United States of America, 101(21): 8011–8016.
    [18] Houston RD, Bean TP, Macqueen DJ, Gundappa MK, Jin YH, Jenkins TL, et al. 2020. Harnessing genomics to fast-track genetic improvement in aquaculture. Nature Reviews Genetics, 21(7): 389−409. doi: 10.1038/s41576-020-0227-y
    [19] Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, et al. 2007. A role for piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell, 129(1): 69−82. doi: 10.1016/j.cell.2007.03.026
    [20] Ishikura Y, Ohta H, Sato T, Murase Y, Yabuta Y, Kojima Y, et al. 2021. In vitro reconstitution of the whole male germ-cell development from mouse pluripotent stem cells. Cell Stem Cell, 28(12): 2167−2179.e9. doi: 10.1016/j.stem.2021.08.005
    [21] Iwasaki-Takahashi Y, Shikina S, Watanabe M, Banba A, Yagisawa M, Takahashi K, et al. 2020. Production of functional eggs and sperm from in vitro-expanded type A spermatogonia in rainbow trout. Communications Biology, 3(1): 308. doi: 10.1038/s42003-020-1025-y
    [22] Jia KT, Wu YY, Liu ZY, Mi S, Zheng YW, He J, et al. 2013. Mandarin fish caveolin 1 interaction with major capsid protein of infectious spleen and kidney necrosis virus and its role in early stages of infection. Journal of Virology, 87(6): 3027−3038. doi: 10.1128/JVI.00552-12
    [23] Juszczak M, Roszczyk M, Kowalczyk E, Stempniak B. 2014. The influence od melatonin receptors antagonists, luzindole and 4-phenyl-2-propionamidotetralin (4-P-PDOT), on melatonin-dependent vasopressin and adrenocorticotropic hormone (ACTH) release from the rat hypothalamo-hypophysial system. In vitro and in vivo studies. Journal of Physiology and Pharmacology, 65(6): 777−784.
    [24] Kanatsu-Shinohara M, Toyokuni S, Shinohara T. 2004. CD9 is a surface marker on mouse and rat male germline stem cells. Biology of Reproduction, 70(1): 70−75. doi: 10.1095/biolreprod.103.020867
    [25] Kawasaki T, Saito K, Sakai C, Shinya M, Sakai N. 2012. Production of zebrafish offspring from cultured spermatogonial stem cells. Genes to Cells, 17(4): 316−325. doi: 10.1111/j.1365-2443.2012.01589.x
    [26] Kawasaki T, Siegfried KR, Sakai N. 2016. Differentiation of zebrafish spermatogonial stem cells to functional sperm in culture. Development, 143(4): 566−574.
    [27] Lacerda SMSN, Batlouni SR, Costa GMJ, Segatelli TM, Quirino BR, Queiroz BM, et al. 2010. A new and fast technique to generate offspring after germ cells transplantation in adult fish: the Nile tilapia (Oreochromis niloticus) model. PLoS One, 5(5): e10740. doi: 10.1371/journal.pone.0010740
    [28] Lavoie H, Gagnon J, Therrien M. 2020. ERK signalling: a master regulator of cell behaviour, life and fate. Nature Reviews Molecular Cell Biology, 21(10): 607−632. doi: 10.1038/s41580-020-0255-7
    [29] Lee JH, Kim HJ, Kim H, Lee SJ, Gye MC. 2006. In vitro spermatogenesis by three-dimensional culture of rat testicular cells in collagen gel matrix. Biomaterials, 27(14): 2845−2853. doi: 10.1016/j.biomaterials.2005.12.028
    [30] Li DY, Smith DG, Hardeland R, Yang MY, Xu HL, Zhang L, et al. 2013. Melatonin receptor genes in vertebrates. International Journal of Molecular Sciences, 14(6): 11208−11223. doi: 10.3390/ijms140611208
    [31] Li MY, Hong N, Xu HY, Yi MS, Li CM, Gui JF, et al. 2009. Medaka Vasa is required for migration but not survival of primordial germ cells. Mechanisms of Development, 126(5-6): 366−381. doi: 10.1016/j.mod.2009.02.004
    [32] Li SZ, Liu W, Li Z, Wang Y, Zhou L, Yi MS, et al. 2016. Molecular characterization and expression pattern of a germ cell marker gene dnd in gibel carp (Carassius gibelio). Gene, 591(1): 183−190. doi: 10.1016/j.gene.2016.07.027
    [33] Lin QH, Mei J, Li Z, Zhang XM, Zhou L, Gui JF. 2017. Distinct and cooperative Roles of amh and dmrt1 in self-renewal and differentiation of male germ cells in zebrafish. Genetics, 207(3): 1007−1022. doi: 10.1534/genetics.117.300274
    [34] Lincoln GA, Clarke IJ. 1997. Refractoriness to a static melatonin signal develops in the pituitary gland for the control of prolactin secretion in the ram. Biology of Reproduction, 57(2): 460−467. doi: 10.1095/biolreprod57.2.460
    [35] Liu W, Zhang H, Xiang YX, Jia KT, Luo MF, Yi MS. 2019. Molecular characterization of Vasa homologue in marbled goby, Oxyeleotris marmorata: transcription and localization analysis during gametogenesis and embryogenesis. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 229: 42−50. doi: 10.1016/j.cbpb.2018.12.005
    [36] Liu W, Zhang H, Xiang YX, Jia KT, Luo MF, Yi MS. 2020. A novel germline and somatic cell expression of two sexual differentiation genes, Dmrt1 and Foxl2 in marbled goby (Oxyeleotris marmorata). Aquaculture, 516: 734619. doi: 10.1016/j.aquaculture.2019.734619
    [37] Mäkelä JA, Hobbs RM. 2019. Molecular regulation of spermatogonial stem cell renewal and differentiation. Reproduction, 158(5): R169−R187. doi: 10.1530/REP-18-0476
    [38] Mei J, Gui JF. 2015. Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Science China Life Sciences, 58(2): 124−136. doi: 10.1007/s11427-014-4797-9
    [39] Meroni SB, Galardo MN, Rindone G, Gorga A, Riera MF, Cigorraga SB. 2019. Molecular mechanisms and signaling pathways involved in Sertoli cell proliferation. Frontiers in Endocrinology, 10: 224. doi: 10.3389/fendo.2019.00224
    [40] Miura T, Yamauchi K, Takahashi H, Nagahama Y. 1991. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proceedings of the National Academy of Sciences of the United States of America, 88(13): 5774−5778. doi: 10.1073/pnas.88.13.5774
    [41] Mohammadzadeh E, Mirzapour T, Nowroozi MR, Nazarian H, Piryaei A, Alipour F, et al. 2019. Differentiation of spermatogonial stem cells by soft agar three-dimensional culture system. Artificial Cells, Nanomedicine, and Biotechnology, 47(1): 1772−1781. doi: 10.1080/21691401.2019.1575230
    [42] Nasiri Z, Hosseini SM, Hajian M, Abedi P, Bahadorani M, Baharvand H, et al. 2012. Effects of different feeder layers on short-term culture of prepubertal bovine testicular germ cells in-vitro. Theriogenology, 77(8): 1519–1528.
    [43] Naylor RL, Hardy RW, Buschmann AH, Bush SR, Cao L, Klinger DH, et al. 2021. A 20-year retrospective review of global aquaculture. Nature, 591(7851): 551−563. doi: 10.1038/s41586-021-03308-6
    [44] Niu ZW, Mu HL, Zhu HJ, Wu J, Hua JL. 2017. p38 MAPK pathway is essential for self-renewal of mouse male germline stem cells (mGSCs). Cell Proliferation, 50(1): e12314. doi: 10.1111/cpr.12314
    [45] Niu ZW, Zheng LM, Wu SY, Mu HL, Ma FL, Song WC, et al. 2015. Ras/ERK1/2 pathway regulates the self-renewal of dairy goat spermatogonia stem cells. Reproduction, 149(5): 445−452. doi: 10.1530/REP-14-0506
    [46] Okutsu T, Shikina S, Kanno M, Takeuchi Y, Yoshizaki G. 2007. Production of trout offspring from triploid salmon parents. Science, 317(5844): 1517. doi: 10.1126/science.1145626
    [47] Okutsu T, Suzuki K, Takeuchi Y, Takeuchi T, Yoshizaki G. 2006. Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proceedings of the National Academy of Sciences of the United States of America, 103(8): 2725−2729. doi: 10.1073/pnas.0509218103
    [48] Panda RP, Barman HK, Mohapatra C. 2011. Isolation of enriched carp spermatogonial stem cells from Labeo rohita testis for in vitro propagation. Theriogenology, 76(2): 241−251. doi: 10.1016/j.theriogenology.2011.01.031
    [49] Reda A, Albalushi H, Montalvo SC, Nurmio M, Sahin Z, Hou M, et al. 2017. Knock-out serum replacement and melatonin effects on germ cell differentiation in murine testicular explant cultures. Annals of Biomedical Engineering, 45(7): 1783−1794. doi: 10.1007/s10439-017-1847-z
    [50] Reda A, Hou M, Winton TR, Chapin RE, Söder O, Stukenborg JB. 2016. In vitro differentiation of rat spermatogonia into round spermatids in tissue culture. Molecular Human Reproduction, 22(9): 601−612. doi: 10.1093/molehr/gaw047
    [51] Saiki A, Tamura M, Matsumoto M, Katowgi J, Watanabe A, Onitake K. 1997. Establishment of in vitro spermatogenesis from spermatocytes in the medaka. Oryzias latipes. Development, Growth & Differentiation, 39(3): 337−344.
    [52] Sakai N. 2002. Transmeiotic differentiation of zebrafish germ cells into functional sperm in culture. Development, 129(14): 3359−3365. doi: 10.1242/dev.129.14.3359
    [53] Schulz RW, De França LR, Lareyre JJ, Legac F, Chiarini-Garcia H, Nobrega RH, et al. 2010. Spermatogenesis in fish. General and Comparative Endocrinology, 165(3): 390−411. doi: 10.1016/j.ygcen.2009.02.013
    [54] Shikina S, Ihara S, Yoshizaki G. 2008. Culture conditions for maintaining the survival and mitotic activity of rainbow trout transplantable type A spermatogonia. Molecular Reproduction and Development, 75(3): 529−537. doi: 10.1002/mrd.20771
    [55] Shinohara T, Avarbock MR, Brinster RL. 1999. β1- and α6-integrin are surface markers on mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences of the United States of America, 96(10): 5504−5509. doi: 10.1073/pnas.96.10.5504
    [56] Subash SK, Kumar PG. 2021. Self-renewal and differentiation of spermatogonial stem cells. Frontiers in Bioscience (Landmark Edition), 26(1): 163−205. doi: 10.2741/4891
    [57] Sun PB, Wang YY, Gao T, Li K, Zheng DW, Liu AJ, et al. 2021. Hsp90 modulates human sperm capacitation via the Erk1/2 and p38 MAPK signaling pathways. Reproductive Biology and Endocrinology, 19(1): 39. doi: 10.1186/s12958-021-00723-2
    [58] Takeuchi Y, Yoshizaki G, Takeuchi T. 2004. Surrogate broodstock produces salmonids. Nature, 430(7000): 629−630. doi: 10.1038/430629a
    [59] Tassinari V, Campolo F, Cesarini V, Todaro F, Dolci S, Rossi P. 2015. Fgf9 inhibition of meiotic differentiation in spermatogonia is mediated by Erk-dependent activation of Nodal-Smad2/3 signaling and is antagonized by Kit Ligand. Cell Death & Disease, 6(3): e1688.
    [60] Wolf K, Quimby MC. 1962. Established eurythermic line of fish cells in vitro. Science, 135(3508): 1065–1066.
    [61] Xie X, Nóbrega R, Pšenička M. 2020. Spermatogonial stem cells in fish: characterization, isolation, enrichment, and recent advances of in vitro culture systems. Biomolecules, 10(4): 644. doi: 10.3390/biom10040644
    [62] Xu HY, Gui JF, Hong YH. 2005. Differential expression of Vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp (Carassius auratus gibelio), a bisexually and gynogenetically reproducing vertebrate. Developmental Dynamics, 233(3): 872−882. doi: 10.1002/dvdy.20410
    [63] Ye D, Zhu L, Zhang QF, Xiong F, Wang HP, Wang XP, et al. 2019. Abundance of early embryonic primordial germ cells promotes zebrafish female differentiation as revealed by lifetime labeling of germline. Marine Biotechnology, 21(2): 217−228. doi: 10.1007/s10126-019-09874-1
    [64] Yi MS, Hong N, Hong YH. 2010. Derivation and characterization of haploid embryonic stem cell cultures in medaka fish. Nature Protocols, 5(8): 1418−1430. doi: 10.1038/nprot.2010.104
    [65] Yu K, Deng SL, Sun TC, Li YY, Liu YX. 2018. Melatonin regulates the synthesis of steroid hormones on male reproduction: a review. Molecules, 23(2): 447. doi: 10.3390/molecules23020447
    [66] Zhang FH, Hao YK, Li XM, Li Y, Ye D, Zhang R, et al. 2021a. Surrogate production of genome-edited sperm from a different subfamily by spermatogonial stem cell transplantation. Science China Life Sciences,doi: 10.1007/s11427-021-1989-9.
    [67] Zhang MF, Li N, Liu WQ, Du XM, Wei YD, Yang DH, et al. 2021b. Eif2s3y promotes the proliferation of spermatogonial stem cells by activating ERK signaling. Stem Cells International, 2021: 6668658.
    [68] Zhang WW, Jia KT, Jia P, Xiang YX, Lu XB, Liu W, et al. 2020. Marine medaka heat shock protein 90ab1 is a receptor for red-spotted grouper nervous necrosis virus and promotes virus internalization through clathrin-mediated endocytosis. PLoS Pathogens, 16(7): e1008668. doi: 10.1371/journal.ppat.1008668
    [69] Zhang XJ, Zhou L, Gui JF. 2019. Biotechnological innovation in genetic breeding and sustainable green development in Chinese aquaculture. Scientia Sinica Vitae, 49(11): 1409−1429. (in Chinese)
    [70] Zhao CY, Liu QH, Xu SH, Xiao YS, Wang WQ, Yang JK, et al. 2018. Identification of type A spermatogonia in turbot (Scophthalmus maximus) using a new cell-surface marker of Lymphocyte antigen 75 (ly75/CD205). Theriogenology, 113: 137−145. doi: 10.1016/j.theriogenology.2017.12.016
    [71] Zhou L, Wang XY, Liu QH, Yang JK, Xu SH, Wu ZH, et al. 2021. Successful spermatogonial stem cells transplantation within pleuronectiformes: first breakthrough at inter-family level in marine fish. International Journal of Biological Sciences, 17(15): 4426−4441. doi: 10.7150/ijbs.63266
    [72] Zhou Q, Wang M, Yuan Y, Wang XP, Fu R, Wan HF, et al. 2016. Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell, 18(3): 330–340.
    [73] Zhu J, Wang JX, Wang X, Gao MJ, Guo BB, Gao MM, et al. 2021. Prediction of drug efficacy from transcriptional profiles with deep learning. Nature Biotechnology, 39(11): 1444−1452. doi: 10.1038/s41587-021-00946-z
  • 加载中
图(8) / 表(2)
计量
  • 文章访问数:  251
  • HTML全文浏览量:  121
  • PDF下载量:  61
  • 被引次数: 0
出版历程
  • 收稿日期:  2022-04-07
  • 录用日期:  2022-05-23
  • 网络出版日期:  2022-05-24

目录

    /

    返回文章
    返回