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scRNA-seq reveals that origin recognition complex subunit 6 regulates mouse spermatogonial cell proliferation and apoptosis via activation of Wnt/β-catenin signaling

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Asian Journal of Andrology 2024年第1期26卷 46-56页

作者： Shi-Wei Liu Jia-Qiang Luo Liang-Yu Zhao Ning-Jing Ou Chao-Yang Yu-Xiang Zhang Hao-Wei Bai Hong-Fang Sun Jian-Xiong Zhang Chen-Cheng Yao Peng Li Ru-Hui Tian Zheng Li Zi-Jue Zhu Department of Andrology Center for Men's HealthUrologic Medical CenterShanghai General HospitalShanghai Jiao Tong University School of MedicineShanghai 200080China State Key Lab of Reproductive Medicine Nanjing Medical UniversityNanjing 211166China Shanghai Key Lab of Reproductive Medicine Shanghai Jiao Tong University School of MedicineShanghai 200080China Department of Urology Guangdong Provincial Key Laboratory of Biomedical ImagingThe Fifth Affiliated HospitalSun Yat-sen UniversityZhuhai 519000China Department of Urology First Affiliated Hospital of Nanjing Medical UniversityNanjing 210029China

The regulation of spermatogonial proliferation and apoptosis is of great significance for maintaining spermatogenesis.The single-cell RNA sequencing(scRNA-seq)analysis of the testis was performed to identify genes upregulated in spermatogonia.Using scRNAseq analysis,we identified the spermatogonia upregulated gene origin recognition complex subunit 6(Orc6),which is involved in DNA replication and cell cycle regulation;its protein expression in the human and mouse testis was detected by western blot and immunofluorescence.To explore the potential function of Orc6 in spermatogonia,the C18-4 cell line was transfected with control or Orc6 siRNA.Subsequently,5-ethynyl-2-deoxyuridine(EdU)and terminal deoxynucleotidyl transferase dUTP nick end labeling(TUNEL)assays,flow cytometry,and western blot were used to evaluate its effects on proliferation and apoptosis.It was revealed that ORC6 could promote proliferation and inhibit apoptosis of C18-4 cells.Bulk RNA sequencing and bioinformatics analysis indicated that Orc6 was involved in the activation of wingless/integrated(Wnt)/β-catenin signaling.Western blot revealed that the expression ofβ-catenin protein and its phosphorylation(Ser675)were significantly decreased when silencing the expression of ORC6.Our findings indicated that Orc6 was upregulated in spermatogonia,whereby it regulated proliferation and apoptosis by activating Wnt/β-catenin signaling.

关键词： cell proliferation ORCG scRNA-seq analysis spermatogonia Wnt/β-catenin signaling

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

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Zoological Research 2022年第4期43卷 537-551页

作者： Hong Zhang Wan-Wan Zhang Cheng-Yu Mo Meng-Dan Dong Kun-Tong Jia Wei Liu Mei-Sheng Yi School of Marine Sciences Sun Yat-Sen UniversityGuangzhouGuangdong 510275China Southern Marine Science and Engineering Guangdong Laboratory(Zhuhai) ZhuhaiGuangdong 519000China Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering GuangzhouGuangdong 510000China

In vitro production of functional gametes can revolutionize reproduction by reducing generation intervals and accelerating genetic breeding in aquaculture,especially in fish with relatively long generations.Nevertheless,functional sperm production from in vitro-cultured spermatogonia remains a challenge in most aquaculture fish.In this study,we isolated and characterized premeiotic spermatogonia from marine four-eyed sleepers(Bostrychus sinensis),which are prone to ovotesticular or sterile testicular development,and induced the differentiation of the spermatogonia into flagellated sperm in a three-dimensional(3D)culture system.Artificial insemination indicated that the in vitro-derived sperm were capable of fertilizing mature oocytes to develop into normal larvae.Furthermore,melatonin significantly promoted spermatogonia proliferation and differentiation through the ERK1/2 signaling pathway,and thus increased the efficiency in functional sperm production.The 3D culture system and resulting functional sperm hold great promise for improving the genetic breeding of aquaculture fish.

关键词： In vitro spermatogenesis 3D culture model spermatogonia Four-eyed sleeper Melatonin Genetic breeding

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Successful transplantation of cryopreserved spermatogonia in Sebastes schlegelii:A simple and suitable alternative approach for conservation of viviparous fish

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Water Biology and Security 2023年第3期2卷 75-86页

作者： Li Zhou Xueying Wang Shuran Du Shihong Xu Yanfeng Wang Zongcheng Song Qinghua Liu Jun Li The Key Laboratory of Experimental Marine Biology Center for Ocean Mega-ScienceInstitute of OceanologyChinese Academy of SciencesQingdao266071China College of Life Science Ningde Normal UniversityEngineering Research Center of Mindong Aquatic Product Deep-ProcessingFujian Province UniversityNingde352100China Laboratory for Marine Biology and Biotechnology Qingdao National Laboratory for Marine Science and TechnologyQingdao266071China Weihai Shenghang Aquatic Product Science and Technology Co.Ltd. Weihai264200China

Black rockfish(Sebastes schlegelii)is one of the most important marine economic viviparous fishes.Recently,germplasm degradation and genetic diversity reduction have occurred due to overfishing and long-term artificial breeding.Germ cell transplantation combined with cryopreservation may be an alternative way to protect genetic resources.However,in viviparous fish that undertake fertilization and embryo development in vivo,transplantation is more difficult than in oviparous fish,including selection of transplantation stage,isolation of germ stem cells,and preparation of sterile recipients.This seriously restricts the development of viviparous transplantation.Therefore,in this study,we aimed to explore a transplantation method suitable for these species.Donor cells were isolated from cryopreserved whole testes of 300–400g male Sebastes schlegelii in May,labeled by PKH26,and intra-peritoneally transplanted into allogeneic larvae at 5–10 days post-birth.Subsequently,the development of donor-derived cells in recipients were continuously detected by fluorescence labeling,histology,microsatellite markers,and fecundity tests.The results showed that donors were rich in spermatogonia(75%)and recipients maintained a high survival rate after transplantation,with a rate of>20%at sexual maturity.Further,donor-derived cells successfully migrated(100%),colonized,and incorporated into the developing recipient gonad(93.33%).Finally,transplanted recipients could normally develop and differentiate into male and female individuals,with donor-derived gametes found in 65.38%of mature recipients.In the present study,we first establish a simple and suitable transplantation method for Sebastes schlegelii using immature males and specific larvae,which will serve as a promising tool in the protection of germplasm resources for this transplantation-restricted marine viviparous species.

关键词： Allogeneic transplantation spermatogonia Sebastes schlegelii Germ cells Germplasm

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PLZF^posc-KIT^pos-delineated A1-A4-differentiating spermatogonia by subset and stage detection upon Bouin fixation

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Asian Journal of Andrology 2019年第3期21卷 309-318页

作者： Rui-Ling Tang Li-Qing Fan Institute of Reproduction and Stem Cell Engineering School of Basic Medicine Science Central South University Changsha 410078 China

While hallmarks of rodent spermatogonia stem cell biomarkers' heterogeneity have recently been identified, their stage and subset distributions remain unclear. Furthermore, it is currently difficult to accurately identify subset-specific SSC marker distributions due to the poor nuclear morphological characteristics associated with fixation in 4% paraformaldehyde. In the present study, testicular cross-sections and whole-mount samples were Bouin fixed to optimize nuclear resolution and visualized by immunohistochemistry (IHC) and immunofluorescence (IF). The results identified an expression pattern of PLZFhighc-KITpos in A1 spermatogonia, while A2–A4-differentiating spermatogonia were PLZFlowc-KITpos. Additionally, this procedure was used to examine asymmetrically expressing GFRA1 and PLZF clones, asymmetric Apr and false clones were distinguished based on the presence or absence of TEX14, a molecular maker of intercellular bridges, despite having identical nuclear morphology and intercellular distances that were <25 μm. In conclusion, this optimized Bouin fixation procedure facilitates the accurate identification of spermatogonium subsets based on their molecular profiles and is capable of distinguishing asymmetric and false clones. Therefore, the findings presented herein will facilitate further morphological and functional analysis studies and provide further insight into spermatogonium subtypes.

关键词： asymmetric division cellular homolog of feline sarcoma viral oncogene v-kit false clones glial cell line-derived neurotrophic factor receptor alpha 1 promyelocytic leukemia zinc finger spermatogonia stem cell

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Downregulation of Col lal induces differentiation in mouse spermatogonia

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Asian Journal of Andrology 2012年第6期14卷 842-849页

作者： Sun-Hong Chen Ding Li Chen Xu Department of Histology and Embryology Shanghai Jiao Tong University School of Medicine Shanghai Key Laboratory of Reproductive Medicine Shanghai 200025 China

Col la I （one of the subunit of collagen type I） is a collagen, which belongs to a family of extracellular matrix （ECM） proteins that play an important role in cellular proliferation and differentiation. However, the role of Col lal in spermatogenesis, especially in the control of proliferation and differentiation of spermatogonial stem cells （SSCs）, remains unknown. In this study, we explored effects of downregulation of Collal on differentiation and proliferation of mouse spermatogonia. Loss-of-function study revealed that Oct4 and Plzf, markers of SSC self-renewal, were significantly decreased, whereas the expression of c-kit and haprin, hallmarks of SSC differentiation, was enhanced after Col la I knockdown. Cell cycle analyses indicated that two-thirds of spermatogonia were arrested in S phase after Collal knockdown. In vivo experiments, DNA injection and electroporation of the testes showed that spermatogonia self-renewal ability was impaired remarkably with the loss-of-function of Collal. Our data suggest that silencing of Collal can suppress spermatogonia self-renewal and promote spermatogonia differentiation.

关键词： Collal differentiation extracellular matrix （ECM） spermatogenesis spermatogonia

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Gene expression dynamics during the gonocyte to spermatogonia transition and spermatogenesis in the domestic yak

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Journal of Animal Science and Biotechnology 2019年第4期10卷 907-918页

作者： Guowen Wang Yongchang Li Qilin Yang Shangrong Xu Shike Ma Rongge Yan Ruina Zhang Gongxue Jia Deqiang Ai Qi’en Yang Key Laboratory of Adaptation and Evolution of Plateau Biota Northwest Institute of Plateau BiologyChinese Academy of SciencesXining 810000QinghaiChina University of Chinese Academy of Sciences Beijing 100049China Department of Veterinary Sciences Qinghai Vocational and Technical Institute of Animal Husbandry and VeterinaryQinghai UniversityXining 810016China Qinghai Academy of Animal Science and Veterinary Medicine Qinghai UniversityXining 810016China Animal Husbandry Technology Extension Station of Qinghai Province Xining 810001QinghaiChina Qinghai Key Laboratory of Animal Ecological Genomics Northwest Institute of Plateau BiologyChinese Academy of SciencesXining 810001QinghaiChina CAS Center for Excellence in Tibetan Plateau Earth Sciences Chinese Academy of SciencesBeijing 100101China

Background:Spermatogenesis is a cellular differentiation process that includes three major events:mitosis of spermatogonia,meiosis of spermatocytes and spermiogenesis.Steady-state spermatogenesis relies on functions of spermatogonial stem cells(SSCs).Establishing and maintaining a foundational SSC pool is essential for continued spermatogenesis in mammals.Currently,our knowledge about SSC and spermatogenesis is severely limited in domestic animals.Results:In the present study,we examined transcriptomes of testes from domestic yaks at four different stages(3,5,8 and 24 months of age)and attempted to identify genes that are associated with key developmental events of spermatogenesis.Histological analyses showed that the most advanced germ cells within seminiferous tubules of testes from 3,5,8 and 24 months old yaks were gonocytes,spermatogonia,spermatocytes and elongated spermatids,respectively.RNA-sequencing(RNA-seq)analyses revealed that 11904,4381 and 2459 genes were differentially expressed during the gonocyte to spermatogonia transition,the mitosis to meiosis transition and the meiosis to post-meiosis transition.Further analyses identified a list of candidate genes than may regulate these important cellular processes.CXCR4,a previously identified SSC niche factor in mouse,was one of the up-regulated genes in the 5 months old yak testis.Results of immunohistochemical staining confirmed that CXCR4 was exclusively expressed in gonocytes and a subpopulation of spermatogonia in the yak testis.Conclusions:Together,these findings demonstrated histological changes of postnatal testis development in the domestic yak.During development of spermatogonial lineage,meiotic and haploid germ cells are supported by dynamic transcriptional regulation of gene expression.Our transcriptomic analyses provided a list of candidate genes that potentially play crucial roles in directing the establishment of SSC and spermatogenesis in yak.

关键词： Gonocyte Meiosis Spermatogenesis spermatogonia Transcriptome

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17beta-estradiol stimulates proliferation of spermatogonia in experimental cryptorchid mice

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Asian Journal of Andrology 2007年第5期9卷 659-667页

作者： En-Zhong Li De-Xue Li Shi-Qing Zhang Chang-Yong Wang Xue-Ming Zhang Jing-Yan Lu Cui-Mi Duan Xiang-Zhong Yang Li-Xin Feng Beijing Institute of Basic Medical Sciences Beijing 100850 China Department of Agriculture and Forestry Huanghuai University Zhumadian 463000 China College of Animal Sciences and Veterinary Medicine.Jilin llniversitv. Changchun 170002. China Department of Animal Science and Center for Regenerative Biology University of Connecticut Storrs Connecticut 06269-4243 USA

Aim： To investigate whether estrogen stimulates the proliferation of spermatogonia or induces spermatogenesis in cryptorchid mice. Methods： Mice were surgically rendered cryptorchid, then treated with different doses of 17β- estradiol （E2） s.c. once a day. Mice were killed at sexual maturity （45 days of age）, and histological analysis and inununofluorescence were performed. Serum follicle stimulating hormone （FSH）, estradiol, testosterone and luteinizing hormone （LH） were measured. Results： Low doses of E2 had no notable effect on spermatogonia, but at higher doses, E2 stimulated the proliferation of spermatogonia. Conclusion： E2 has a dose-related mitogenic effect on spermatogonia.

关键词： 17β-estradiol cryptorchid mice proliferation spermatogonia

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Isolation of Subtype spermatogonia in Juvenile Rats

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Journal of Huazhong University of Science and Technology(Medical Sciences) 2008年第4期28卷 435-438页

作者：白杨叶哲伟曾甫清 Department of Urology Union Hospital Tongji Medical College Huazhong University of Science and Technology Department of Orthopedics Union Hospital Tongji Medical College Huazhong University of Science and Technology

The present study was aimed at finding an effective method to isolate and purify the subtype of type A spermatogonial stem cells （SSCs） in juvenile rats. Testes from 9-days-old rats were used to isolate germ cells by using two-step enzymatic digestion. The expression of c-kit in the testes of the rats was immunohistochemically detected. After isolation, cell suspension was enriched further by discontinuous density gradient centrifugation. Then type A1-A4 spermatogonia was isolated from the purified spermatogonia with c-kit as the marker by using fluorescence-activated cell sorting （FACS）. Electron microscopy was used to observe their ultrastructure. Finally, highly purified and viable subtype of SSCs was obtained. Cells separation with discontinuous density gradient centrifugation significantly increased the concentration of c-kit positive cells [（18.65±1.69）% after the centrifugation versus （3.16±0.84）% before the centrifugation, P〈0.01]. Furthermore, the recovery and viability were also high [（65.9±1.24）% and （85.6±1.14）%]. It is concluded that FACS with c-kit as the marker in combination with discontinuous density gradient centrifugation can well enrich type A1-A4 spermatogonia from the testes of 9-days-old rats.

关键词： spermatogonia subtype FACS

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Sertoli cell and spermatogonial development in pigs

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Journal of Animal Science and Biotechnology 2022年第4期13卷 1028-1044页

作者： Yi Zheng Qiang Gao Tianjiao Li Ruifang Liu Zechao Cheng Ming Guo Jinhong Xiao De Wu Wenxian Zeng Key Laboratory for Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling 712100ShaanxiChina Zhumei Porcine Breeding Corporation ZhengzhouHenanChina Key Laboratory for Animal Disease Resistance Nutrition of the Ministry of Education of China Institute of Animal NutritionSichuan Agricultural UniversityChengdu 611100SichuanChina.

Background:Spermatogenesis is an intricate developmental process during which undifferentiated spermatogonia,containing spermatogonial stem cells(SSCs),undergo self-renewal and differentiation to generate eventually mature spermatozoa.Spermatogenesis occurs in seminiferous tubules within the testis,and the seminiferous tubules harbor Sertoli and germ cells.Sertoli cells are an essential somatic cell type within the microenvironment that support and steer male germ cell development,whereas spermatogonia are the primitive male germ cells at the onset of spermatogenesis.While the developmental progression of Sertoli cells and spermatogonia has been well established in mice,much less is known in other mammalian species including pigs.Results:To acquire knowledge of Sertoli cell and spermatogonial development in pigs,here we collected as many as nine ages of Duroc porcine testes from the neonate to sexual maturity,i.e.,testes from 7-,30-,50-,70-,90-,110-,130-,150-and 210-day-old boars,and performed histological and immunohistochemical analyses on testis sections.We first examined the development of spermatogenic cells and seminiferous tubules in porcine testes.Then,by immunofluorescence staining for marker proteins(AMH,SOX9,DBA,UCHL1,VASA,KIT,Ki67 and/or PCNA),we delved into the proliferative activity and development of Sertoli cells and of spermatogonial subtypes(pro-,undifferentiated and differentiating spermatogonia).Besides,by immunostaining forβ-catenin and ZO-1,we studied the establishment of the blood-testis barrier in porcine testes.Conclusions:In this longitudinal study,we have systematically investigated the elaborate Sertoli cell and spermatogonial developmental patterns in pigs from the neonate to sexual maturity that have so far remained largely unknown.The findings not only extend the knowledge about spermatogenesis and testicular development in pigs,but also lay the theoretical groundwork for porcine breeding and rearing.

关键词： Pig Sertoli cell Spermatogenesis spermatogonia Testis

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Single-cell-resolution transcriptome map revealed novel genes involved in testicular germ cell progression and somatic cells specification in Chinese tongue sole with sex reversal

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Science China(Life Sciences) 2023年第5期66卷 1151-1169页

作者： Hong-Yan Wang Xiang Liu Jian-Yang Chen Yingyi Huang Yifang Lu Fujian Tan Qun Liu Mingming Yang Shuo Li Xianghui Zhang Yating Qin Wenxiu Ma Yingming Yang Liang Meng Kaiqiang Liu Qian Wang Guangyi Fan Rafael H.Nóbrega Shanshan Liu Francesc Piferrer Changwei Shao Key Lab of Sustainable Development of Marine Fisheries Ministry of Agriculture and Rural AffairsYellow Sea Fisheries Research InstituteChinese Academy of Fishery SciencesQingdao 266072China Laboratory for Marine Fisheries Science and Food Production Processes Qingdao National Laboratory for Marine Science and TechnologyQingdao 266071China College of Fisheries and Life Science Shanghai Ocean UniversityShanghai 201306China BGI Research-Qingdao BGIQingdao 266555China BGI-Shenzhen Shenzhen 518083China School of Marine Sciences Ningbo UniversityNingbo 315211China College of Marine Technology and Environment Dalian Ocean UniversityDalian 116023China Qingdao-Europe Advanced Institute for Life Sciences BGI-ShenzhenQingdao 266555China College of Life Sciences Shandong Normal UniversityJinan 250014China Reproductive and Molecular Biology Group Department of Structural and Functional BiologyInstitute of BiosciencesSão Paulo State University(UNESP)BotucatuSão PauloBrazil Institut de Ciències del Mar(ICM) Spanish National Research Council(CSIC)BarcelonaSpain

Female-to-male sex reversals(pseudomales)are common in lower vertebrates and have been found in natural populations,which is a concern under rapid changes in environmental conditions.Pseudomales can exhibit altered spermatogenesis.However,the regulatory mechanisms underlying pseudomale spermatogenesis remain unclear.Here,we characterized spermatogenesis in Chinese tongue sole(Cynoglossus semilaevis),a species with genetic and environmental sex determination,based on a highresolution single-cell RNA-seq atlas of cells derived from the testes of genotypic males and pseudomales.We identified five germ cell types and six somatic cell types and obtained a single-cell atlas of dynamic changes in gene expression during spermatogenesis in Chinese tongue sole,including alterations in pseudomales.We detected decreased levels of Ca^(2+)signaling pathway-related genes in spermatogonia,insufficient meiotic initiation in spermatocytes,and a malfunction of somatic niche cells in pseudomales.However,a cluster of CaSR genes and MAPK signaling factors were upregulated in undifferentiated spermatogonia of pseudomales.Additionally,we revealed that Z chromosome-specific genes,such as piwil2,dhx37,and ehmt1,were important for spermatogenesis.These results improve our understanding of reproduction after female-to-male sex-reversal and provide new insights into the adaptability of reproductive strategies in lower vertebrates.

关键词： Cynoglossus semilaevis spermatogenesis single-cell transcriptome sex reversal spermatogonia

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