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Research Progress of Mitosis and Meiosis in Mammalian Spermatogenesis |
LI Yun-Xiang, LI Na, HUA Jin-Lian* |
College of Veterinary Medicine, Northwest A&F University /Stem Cell Engineering Technology Research Center of Shaanxi Province, Yangling 712100, China |
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Abstract The fate of SSC is divided into two kinds in mammalian spermatogenesis, one is self-renewal through mitosis, and the other is differentiation into sperm through meiosis. The balance and orderly transition between SSC's mitosis and meiosis is the key to spermatogenesis in male animals. The review focuses on the key regulatory and influencing factors of SSC's mitosis and meiosis, and key point is the regulation of retinoic acid, methylation of mRNA, and hormones during mitosis to meiosis , it would help us to understand the reproductive mechanism of male mammals, and provide references for the treatment of male infertility or the breeding of excellent sires.
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Received: 29 April 2021
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Corresponding Authors:
*jinlianhua@nwsuaf.edu.cn
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[1] Acquaviva L, Michiel B, Karasu M, et al.2020. Ensuring meiotic DNA break formation in the mouse pseudoautosomal region[J]. Nature, 582(7812): 426-431. [2] Agostinho A, Manneberg O, Schendel R, et al.2016. High density of rec8 constrains sister chromatid axes and prevents illegitimate synaptonemal complex formation[J]. EMBO Reports, 17(6): 901-913. [3] Bellutti L, Emilie A, Sophie T, S Messiaen, et al.2019. Divergent roles of cyp26b1 and endogenous retinoic acid in mouse fetal gonads[J]. Biomolecules, 9(10): 536. [4] Bhang D, Dong H, Bang J K, et al.2018. Testicular endothelial cells are a critical population in the germline stem cell niche[j]. Nature Communications, 9(1): 4379. [5] Boekhout M, Karasu M, Juncheng W, et al.2019. REC114 partner ANKRD31 controls number, timing, and location of meiotic dna breaks[J]. Molecular Cell, 74(5): 1053-1068. [6] Busada J T, Geyer C B.2016. The role of retinoic acid (ra) in spermatogonial differentiation[J]. Biology of Reproduction, 94(1): 1-10. [7] Chen C, Wenjun O, Vadim G, et al.2005. ERM is required for transcriptional control of the spermatogonial stem cell niche[J]. Nature, 436(7053):1030. [8] Chen S R, Liu Y X.2015. Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by sertoli cell signaling[J]. Reproduction, 149(4): R159-R167. [9] Cruz I, Brochier-Armanet C, Ricardo B.2019. The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans[J]. BioRxiv, 20(1): 55. [10] Desimio M G, Eleonora C, Maria S, et al.2021. Stimulated by retinoic acid gene 8 (stra8) interacts with the germ cell specific bhlh factor sohlh1 and represses c-kit expression in vitro[J]. Journal of Cellular and Molecular Medicine, 25(1): 383-396. [11] Dunce J M,. Dunne O M, Ratcliff M, et al.2018. Structural basis of meiotic chromosome synapsis through sycp1 self-assembly[J]. Nature Structural and Molecular Biology, 25(7): 557-569. [12] Dunne O M, Davies O R.2019. A molecular model for self-assembly of the synaptonemal complex protein syce3[J]. Journal of Biological Chemistry, 294(23): 9260-9275. [13] Endo T, Maria M M, Peter K N, et al.2019. Retinoic acid and germ cell development in the ovary and testis[J]. Biomolecules, 9(12):775. [14] Eto K.2015. Nociceptin and meiosis during spermatogenesis in postnatal testes[J]. Vitamins and Hormones, 97:167-186. [15] Feng C W, Bowles J, Koopman P.2014. Molecular and cellular endocrinology control of mammalian germ cell entry into meiosis[J]. Molecular and Cellular Endocrinology, 382(1): 488-497. [16] Fukuda T, Fukuda N, Agostinho A, et al.2014. STAG3-mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis[J]. The EMBO Journal, 33(11): 1243-1256. [17] Goertz M J, Wu Z R, Gallardo T D, et al.2011. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis[J]. Journal of Clinical Investigation, 121(9): 3456-3466. [18] Gómez-H L, Felipe-Medina1 N, Sánchez-Martín M, et al.2016. C14ORF39/SIX6OS1 is a constituent of the synaptonemal complex and is essential for mouse fertility[J]. Nature Communications, 7: 13298. [19] Gómez-H L, Felipe-Medina1 N, Yazmine B, et al.2019. The PSMA8 subunit of the spermatoproteasome is essential for proper meiotic exit and mouse fertility[J]. PLoS Genetics, 15(8): e1008316. [20] Griswold M D.2016. Spermatogenesis: The commitment to meiosis[J]. Physiological Reviews, 96(1): 1-17. [21] Gul M, Hildorf S, Dong L H, et al.2020. Review of injection techniques for spermatogonial stem cell transplantation[J]. Human Reproduction Update, 26(3): 368-391. [22] Guo R, Yang X, Zhang L, et al.2021. The ssDNA-binding protein MEIOB acts as a dosage-sensitive regulator of meiotic recombination[J]. Nucleic Acids Research, 48(21): 12219-12233. [23] Gustafson E A, Seymour K A, Sigrist K, et al.2020. ZFP628 is a TAF4b-Interacting transcription factor required for mouse spermiogenesis[J]. Molecular and Cellular Biology, 40(7): e00228. [24] Hobbs R M, Seandel M, Falciatori I, et al.2010. Plzf regulates germline progenitor self-renewal by opposing mTORC1[J]. Cell, 142(3): 468-479. [25] Hsu P J, Zhu Y F, Ma H H, et al.2017. Ythdc2 is an N6 -methyladenosine binding protein that regulates mammalian spermatogenesis[J]. Cell Research, 27(9): 1115-1127. [26] Id Y F, Horisawa-takada Y, Id E I, et al.2020. Meiotic cohesins mediate initial loading of HORMAD1 to the chromosomes and coordinate sc formation during meiotic prophase[J]. PLoS Genetics, 16(9): e1009048. [27] Ishiguro K I, Kumi M, Naoki T, et al.2020. MEIOSIN directs the switch from mitosis to meiosis in mammalian germ cells[J]. Developmental Cell, 52(4): 429-445. [28] Kanatsu-Shinohara M, Inoue K, Takashima S, et al.2012. Reconstitution of mouse spermatogonial stem cell niches in culture[J]. Cell Stem Cell, 11(4): 567-578. [29] Kang H S, Chen LY, Lichti-Kaiser K, et al.2016. Transcription factor GLIS3: A new and critical regulator of postnatal stages of mouse spermatogenesis[J]. Stem Cells, 34(11): 2772-2783. [30] Khanehzad M, Abbaszadeh R, Holakuyee M, et al.2021. FSH regulates RA signaling to commit spermatogonia into differentiation pathway and meiosis[J]. Reproductive Biology and Endocrinology, 19(1): 1-19. [31] Kim S M, Yokoyama T, Ng D, et al.2019. Retinoic acid-stimulated ERK1/2 pathway regulates meiotic initiation in cultured fetal germ cells[J]. PLoS ONE, 14(11): 1-24. [32] Kitadate Y, Jörg D J, Tokue M, et al.2019. Competition for mitogens regulates spermatogenic stem cell homeostasis in an open niche[J]. Cell Stem Cell, 24(1): 79-92. [33] Kolas N K, Yuan L, Hoog C, et al.2004. Male mouse meiotic chromosome cores deficient in structural proteins sycp3 and sycp2 align by homology but fail to synapse and have possible impaired specificity of chromatin loop attachment[J]. Cytogenetic and Genome Research, 188: 182-188. [34] Kotaja N.2014. Micrornas and spermatogenesis[J]. Fertility and Sterility, 101(6): 1552-1562. [35] Koubova J, Yueh-chiang H, Bhattacharyya T, et al.2014. Retinoic acid activates two pathways required for meiosis in mice[J]. PLoS Genetics, 10(8): e1004541. [36] Kubota H,. Avarbock M R, Brinster R L.2004. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells[J]. Proceedings of the National Academy of Sciences of the USA, 101(47): 16489-16494. [37] Larson E L, Kopania E E K, Good J M.2018. Spermatogenesis and the evolution of mammalian sex chromosomes[J]. Trends in Genetics, 34(9): 722-732. [38] Láscarez-Lagunas L, Martinez-Garcia M, Colaiácovo M.2020. “SnapShot: Meiosis - Prophase I[J].” Cell, 181(6): 1442-1442. [39] Lee C Y, Horn H F, Stewart C L,et al.2015. Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes[J]. Cell Reports, 11(4): 551-563. [40] Lee S J, Park J, Lee D J, et al.2020. Mast4 knockout shows the regulation of spermatogonial stem cell self-renewal via the FGF2/ERM pathway[J]. Cell Death and Differentiation, 28(5): 1441-1454. [41] Legrand J M D, Chan A L, La H M,et al.2019. DDX5 plays essential transcriptional and post-transcriptional roles in the maintenance and function of spermatogonia[J]. Nature Communications, 10(1): 2278. [42] Li M, Huang T, Li M J, et al.2019. The histone modification reader ZCWPW1 is required for meiosis prophase i in male but not in female mice[J]. Science Advances, 5(8): eaax1101. [43] Li T, Shi Q H, Davies B, et al.2020. Article the configuration of RPA, RAD51, and DMC1 binding in meiosis reveals the nature of critical recombination intermediates[J]. Molecular Cell, 79(4): 689-701. [44] Lin Z, Hsu P J, Xing X D, et al.2017. Mettl3-/Mettl14-mediated mRNA N6-methyladenosine modulates murine spermatogenesis[J]. Cell Research, 27(10): 1216-1230. [45] Link J, Leubner M, Schmitt J, et al.2014. Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic linc complex formation and function[j]. PLoS Genetics, 10(2): e1004099. [46] Liu H B, HuangT, Li M G, et al.2019. SCRE serves as a unique synaptonemal complex fastener and is essential for progression of meiosis prophase i in mice[J]. Nucleic Acids Research, 47(11): 5670-5683. [47] Liu W B, Wang F C, Xu Q H, et al.2017. BCAS2 is involved in alternative mRNA splicing in spermatogonia and the transition to meiosis[J]. Nature Communications, 8: 14182. [48] Lord T, Nixon B.2020. Metabolic changes accompanying spermatogonial stem cell differentiation[J]. Developmental Cell, 52(4): 399-411. [49] Lovasco L A, Gustafson E A, Seymour K A, et al.2015. Taf4b is required for mouse spermatogonial stem cell development[J]. Stem Cells, 33(4): 1267-1276. [50] Ma F L, Zhou Z, Li N, et al.2016. Lin28a promotes self-renewal and proliferation of dairy goat spermatogonial stem cells (SSCs) through regulation of mTOR and PI3K/AKT[J]. Scientific Reports, 6: 38805. [51] Matson C K., Murphy M W, Griswold M D, et al.2010. The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells[J]. Developmental Cell, 19(4): 612-624. [52] Meng X J, Lindahl M, Hyvönen M E, et al.2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF[J]. Science, 287(5457): 1489-1493. [53] Oatley J M, Oatley M J, Avarbock M R, 2009. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal[J]. Development, 136(7): 1191. [54] Ward A, Oatley M J, Avarbock M R.2016. Genetic interactions between the meiosis-specific cohesin components, STAG3, REC8 and RAD21L[J]. G3 (Bethesda, Md.), 6(6): 1713-1724. [55] Paiano J, Wu W, Yamada S, et al.2020. ATM and PRDM9 regulate SPO11-bound recombination intermediates during meiosis[J]. Nature Communications, 11(1): 857. [56] Papanikos F, Clément J A J, Testa E, et al.2019. Mouse ANKRD31 regulates spatiotemporal patterning of meiotic recombination initiation and ensures recombination between X and Y sex chromosomes[J]. Molecular Cell, 74(5): 1069-1085. [57] Robert T, Nore A, Brun C, et al.2016. The TopoVIB-Like protein family is required for meiotic DNA double-strand break formation[J]. Science, 351(6276): 943-949. [58] Rossi P, Rossi P.2013. Paracrine mechanisms involved in the control of early stages of mammalian spermatogenesis[J]. Frontiers in Endocrinology, 4: 181. [59] Shang Y L, Huang T, Liu H B, et al.2020. MEIOK21: A new component of meiotic recombination bridges required for spermatogenesis[J]. Nucleic Acids Research, 48(12): 6624-6639. [60] Smith L B, Walker W H.2014. The regulation of spermatogenesis by androgens[J]. Seminars in Cell and Developmental Biology, 30: 2-13. [61] Song H W, Wilkinson M F.2014. Transcriptional control of spermatogonial maintenance and differentiation[J]. Seminars in Cell and Developmental Biology. 30: 14-26. [62] Syrjänen J L, Pellegrini L, Davies O R.2014. A molecular model for the role of SYCP3 in meiotic chromosome organisation[J]. eLife, 3: e02963. [63] Takashima S, Kanatsu-Shinohara M, Tanaka T, et al.2015. Functional differences between GDNF-dependent and FGF2-dependent mouse spermatogonial stem cell self-renewal[J]. Stem Cell Reports, 4(3): 489-502. [64] Tassinari V, Campolo F, Cesarini V, et al.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[J]. Cell Death and Disease, 6(3): e1688. [65] Wang C X, Wang Z L, Xiong Z, et al.2016. MTORC1 activation promotes spermatogonial differentiation and causes subfertility in mice[J]. Biology of Reproduction, 95(5): 97. [66] Wang G S, Wu X L, Zhou L W, et al.2020. Tethering of telomeres to the nuclear envelope is mediated by SUN1-MAJIN and possibly promoted by SPDYA-CDK2 during meiosis[J]. Frontiers in Cell and Developmental Biology, 8(September): 1-11. [67] Wang L N, TuZ W, Liu C, et al.2018. Dual roles of TRF1 in tethering telomeres to the nuclear envelope and protecting them from fusion during meiosis[J]. Cell Death & Differentiation, 25(6): 1174-1188. [68] Wang H P, Xu X J, Li J L, et al.2019a. Sertoli cell-only phenotype and scRNA-Seq define PRAMEF12 as a factor essential for spermatogenesis in mice[J].Nature Communications, 10(1): 5196. [69] Wang Y, Chen Y Y, Chen J, et al.2019b. The meiotic TERB1-TERB2-MAJIN complex tethers telomeres to the nuclear envelope[J]. Nature Communications, 10(1): 1-19. [70] Wang Y J, Li X Y, Gong X W, et al.2019c. MicroRNA-322 regulates self-renewal of mouse spermatogonial stem cells through Rassf8[J].International Journal of Biological Sciences, 15(4): 857-869. [71] Xiong M L, Ferder I C, Ferder I C, et al.2015. Quantitative analysis of male germline stem cell differentiation reveals a role for the P53-mTORC1 pathway in spermatogonial maintenance[J]. Cell Cycle, 14(18): 2905-2913. [72] Xu H Z, Tong Z S, Ye Q, et al.2019. Molecular organization of mammalian meiotic chromosome axis revealed by expansion STORM microscopy[J]. Proceedings of the National Academy of Sciences of the USA, 116(37): 18423-18428. [73] Xu K, Yang Y, Feng G H, et al.2017. Mettl3-Mediated m6A regulates spermatogonial differentiation and meiosis initiation[J]. Cell Research, 27(9): 1100-1114. [74] Yamauchi Y, Riel J M, Ruthig V A, et al.2016. Two genes substitute for the mouse Y chromosome for spermatogenesis and reproduction[J]. Science, 351(6272): 514-516. [75] Yang F, Whelan E C, Guan X B, et al.2021. Fgf9 promotes mouse spermatogonial stem cell proliferation mediated by P38 MAPK signalling[J]. Cell Proliferation, 54(1): e12933. [76] Yuan Y, Li L H, Cheng Q, et al.2020. In vitro testicular organogenesis from human fetal gonads produces fertilization-competent spermatids[J]. Cell Research, 30(3): 244-255. [77] Zhang B, Tang Z H, Li L J.2020. NBS1 Is required for SPO11-linked DNA double-strand break repair in male meiosis[J]. Cell Death & Differentiation, 27(7): 2176-2190. [78] Zhang J D, Eto K, Honmyou A, et al.2011. Neuregulins are essential for spermatogonial proliferation and meiotic initiation in neonatal mouse testis[J]. Development, 138(15): 3159-3168. [79] Zhang M Fi, Li Na, Liu W Q, et al.2021. Eif2s3y promotes the proliferation of spermatogonial stem cells by activating ERK signaling[J]. Stem Cells International, 2021: 6668658. [80] Zhang Q T, Shu Y J, Busayavalasa K, et al.2019. Meiosis I progression in spermatogenesis requires a type of testis-specific 20s core proteasome[J]. Nature Communications, 10(1): 3387. [81] Zhou Z, Kawabe H, Suzuki A, et al.2017. NEDD4 controls spermatogonial stem cell homeostasis and stress response by regulating messenger ribonucleoprotein complexes[J]. Nature Communications, 8: 15662. [82] Zhou Z, Shirakawa T, Ohbo K, et al.2015. RNA binding protein Nanos2 organizes post-transcriptional buffering system to retain primitive state of mouse spermatogonial stem cells[J]. Developmental Cell, 34(1): 96-107. [83] Yu X W, Li T T, Du X M, et al.2021. Single-cell RNA sequencing reveals atlas of dairy goat testis cells[J]. Zoological Research, 42(4): 401-405. [84] Wei Y D, Du X M, Yang D H, et al.2021. Dmrt1 regulates the immune response by repressing the TLR4 signaling pathway in goat male germline stem cells[J]. Zoological Research. 42(1): 14-27. |
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