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Sertoli cell and spermatogonial development in pigs

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 RNA-seq analysis of testicular somatic cell development in pigs

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Journal of Genetics and Genomics 2022年第11期49卷 1016-1028页

作者： Lingkai Zhang Ming Guo Zidong Liu Ruifang Liu Yi Zheng Taiyong Yu Yinghua Lv Hongzhao Lu wenxian zeng Tao Zhang Chuanying Pan College of Animal Science and Technology Northwest A&F UniversityYanglingShaanxi 712100China College of Chemistry and Pharmacy Northwest A&F UniversityYanglingShaanxi 712100China School of Biological Science and Engineering Shaanxi University of TechnologyHanzhongShaanxi 723001China

Spermatogenesis is the process by which diploid male germ cells propagate and differentiate into haploid flagellated spermatozoa.This highly complicated process is dependent on testicular somatic cells maturation.While the role of these somatic cells in spermatogenesis is relatively well established,knowledge about their development and maturation,particularly at the molecular level,is limited.In this study,we profiled the testicular single-cell transcriptomes of Guanzhong black pigs at the age of 7,30,60,90,and 150 days.Five types of Sertoli cells,five types of Leydig cells,and four types of peritubular myoid cells were identified.Histological analysis revealed the changes in proliferation levels and marker gene expressions,and the prion-like protein gene(PRND)was identified as a novel marker for Sertoli cells.Additionally,integrated analyses of porcine and human datasets revealed similarities between human and pig testicular somatic cells.Overall,the data obtained in this study contribute to the understanding of testicular development in pigs as a model species.

关键词： Pigs scRNA-seq Testis somatic cells Puberty

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Single-cell RNA-sequencing reveals the dynamic process and novel markers in porcine spermatogenesis

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Journal of Animal Science and Biotechnology 2022年第2期13卷 458-472页

作者： Lingkai Zhang Fuyuan Li Peipei Lei Ming Guo Ruifang Liu Ling Wang Taiyong Yu Yinghua Lv Tao Zhang wenxian zeng Hongzhao Lu Yi Zheng Key Laboratory for Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling 712100ShaanxiChina School of Biological Science and Engineering Shaanxi University of TechnologyHanzhong 723001ShaanxiChina College of Chemistry and Pharmacy Northwest A&F UniversityYangling 712100ShaanxiChina

Background:Spermatogenesis is the process by which male gametes are formed from spermatogonial stem cells and it is essential for the reliable transmission of genetic information between generations.To date,the dynamic transcriptional changes of defined populations of male germ cells in pigs have not been reported.Results:To characterize the atlas of porcine spermatogenesis,we profiled the transcriptomes of~16,966 testicular cells from a 150-day-old pig testis through single-cell RNA-sequencing(scRNA-seq).The scRNA-seq analysis identified spermatogonia,spermatocytes,spermatids and three somatic cell types in porcine testes.The functional enrichment analysis demonstrated that these cell types played diverse roles in porcine spermatogenesis.The accuracy of the defined porcine germ cell types was further validated by comparing the data from scRNA-seq with those from bulk RNA-seq.Since we delineated four distinct spermatogonial subsets,we further identified CD99 and PODXL2 as novel cell surface markers for undifferentiated and differentiating spermatogonia,respectively.Conclusions:The present study has for the first time analyzed the transcriptome of male germ cells and somatic cells in porcine testes through scRNA-seq.Four subsets of spermatogonia were identified and two novel cell surface markers were discovered,which would be helpful for studies on spermatogonial differentiation in pigs.The datasets offer valuable information on porcine spermatogenesis,and pave the way for identification of key molecular markers involved in development of male germ cells.

关键词： Marker Pig scRNA-seq Spermatogenesis

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Transcriptome-wide Dynamics of m^(6)A mRNA Methylation During Porcine Spermatogenesis

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Genomics, Proteomics & Bioinformatics 2023年第4期21卷 729-741页

作者： Zidong Liu Xiaoxu Chen Pengfei Zhang Fuyuan Li Lingkai Zhang Xueliang Li Tao Huang Yi Zheng Taiyong Yu Tao Zhang wenxian zeng Hongzhao Lu Yinghua Lv Key Laboratory for Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling 712100China School of Biological Science and Engineering Shaanxi University of TechnologyHanzhong 723001China College of Chemistry and Pharmacy Northwest A&F UniversityYangling 712100China

Spermatogenesis is a continual process that occurs in the testes,in which diploid spermatogonial stem cells(SSCs)differentiate and generate haploid spermatozoa.This highly efficient and intricate process is orchestrated at multiple levels.N^(6)-methyladenosine(m^(6)A),an epigenetic modification prevalent in mRNAs,is implicated in the transcriptional regulation during spermatogenesis.However,the dynamics of m^(6)A modification in non-rodent mammalian species remains unclear.Here,we systematically investigated the profile and role of m^(6)A during spermatogenesis in pigs.By analyzing the transcriptomic distribution of m^(6)A in spermatogonia,spermatocytes,and round spermatids,we identified a globally conserved m^(6)A pattern between porcine and murine genes with spermatogenic function.We found that m^(6)A was enriched in a group of genes that specifically encode the metabolic enzymes and regulators.In addition,transcriptomes in porcine male germ cells could be subjected to the m^(6)A modification.Our data show that m^(6)A plays the regulatory roles during spermatogenesis in pigs,which is similar to that in mice.Illustrations of this point are three genes(SETDB1,FOXO1,and FOXO3)that are crucial to the determination of the fate of SSCs.To the best of our knowledge,this study for the first time uncovers the expression profile and role of m^(6)A during spermatogenesis in large animals and provides insights into the intricate transcriptional regulation underlying the lifelong male fertility in non-rodent mammalian species.

关键词： N^(6)-methyladenosine Spermatogonial stem cell Spermatogenesis SETDB1 Pig

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The roles of microRNAs in regulation of mammalian spermatogenesis

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Journal of Animal Science and Biotechnology 2017年第4期8卷 779-786页

作者： Xiaoxu Chen Xueliang Li Jiayin Guo Pengfei Zhang wenxian zeng College of Animal Science and Technology Northwest A&F UniversityYanglingShaanxi 712100China

Mammalian spermatogenesis contains three continuous and organized processes, by which spermatogonia undergo mitosis and differentiate to spermatocytes, follow on meiosis to form haploid spermatids and ultimately transform into spermatozoa. These processes require an accurately, spatially and temporally regulated gene expression patterns. The microRNAs are a novel class of post-transcriptional regulators. Cumulating evidences have demonstrated that microRNAs are expressed in a cell-specific or stage-specific manner during spermatogenesis. In this review, we focus on the roles of microRNAs in spermatogenesis. We highlight that N6-methyladenosine(m6A)is involved in the biogenesis of microRNAs and miRNA regulates the m6A modification on mRNA, and that specific mi RNAs have been exploited as potential biomarkers for the male factor infertility, which will provide insightful understanding of microRNA roles in spermatogenesis.

关键词： microRNAs RNA methylation Spermatogenesis

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A novel water index for urban high-resolution eight-band WorldView-2 imagery

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International Journal of Digital Earth 2016年第10期9卷 925-941页

作者： Cong Xie Xin Huang wenxian zeng Xing Fang State Key Laboratory of Information Engineering in Surveying Mapping and Remote Sensing(LIESMARS)Wuhan UniversityWuhanPeople’s Republic of China School of Remote Sensing and Information Engineering Wuhan UniversityWuhanPeople’s Republic of China School of Geodesy and Geomatics Wuhan UniversityWuhanPeople’s Republic of China

Land surface water mapping is one of the most important remote-sensing applications.However,water areas are spectrally similar and overlapped with shadow,making accurate water extraction from remote-sensing images still a challenging problem.This paper develops a novel water index named as NDWI-MSI,combining a new normalized difference water index(NDWI)and a recently developed morphological shadow index(MSI),to delineate water bodies from eight-band WorldView-2 imagery.The newly available bands(e.***.coastal,yellow,red-edge,and near-infrared 2)of WorldView-2 imagery provide more potential for constructing new NDWIs derived from various band combinations.Through our testing,a new NDWI is defined in this study.In addition,MSI,a recently developed automatic shadow extraction index from high-resolution imagery can be used to indicate shadow areas.The NDWI-MSI is created by combining NDWI and MSI,which is able to highlight water bodies and simultaneously suppress shadow areas.In experiments,it is shown that the new water index can achieve better performance than traditional NDWI,and even supervised classifiers,for example,maximum likelihood classifier,and support vector machine.

关键词： WorldView-2 water extraction water index shadow detection

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Establishment of cell lines with porcine spermatogonial stem cell properties

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Journal of Animal Science and Biotechnology 2020年第3期11卷 678-689页

作者： Yi Zheng Tongying Feng Pengfei Zhang Peipei Lei Fuyuan Li wenxian zeng Key Laboratory for Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling 712100ShaanxiChina

Background:Spermatogonial stem cells(SSCs)are capable of both self-renewal and differentiation to mature functional spermatozoa,being the only adult stem cells in the males that can transmit genetic information to the next generation.Porcine SSCs hold great value in transgenic pig production and in establishment of porcine models for regenerative medicine.However,studies and applications of porcine SSCs have been greatly hampered by the low number of SSCs in the testis as well as the lack of an ideal stable long-term culture system to propagate porcine SSCs perpetually.Results:In the present study,by lentiviral transduction of plasmids expressing the simian virus 40(SV40)large T antigen into porcine primary SSCs,we developed two immortalized cell lines with porcine SSC attributes.The established cell lines,with the expression of porcine SSC and germ cell markers UCHL1,PLZF,THY1,VASA and DAZL,could respond to retinoic acid(RA),and could colonize the recipient mouse testis without tumor formation after transplantation.The cell lines displayed infinite proliferation potential,and have now been cultured for more than 7 months and passaged for over 35 times without morphological abnormalities.Conclusions:We have for the first time established porcine SSC lines that could provide abundant cell sources for mechanistic studies on porcine SSC self-renewal and differentiation,thereby facilitating development of an optimal long-term culture system for porcine primary SSCs and their application to animal husbandry and medicine.

关键词： Immortalization Pig Self-renewal Spermatogonial stem cells SV40 large T antigen

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Meclofenamic acid represses spermatogonial proliferation through modulating m^6A RNA modification

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Journal of Animal Science and Biotechnology 2019年第4期10卷 919-930页

作者： Tao Huang Jiayin Guo Yinghua Lv Yi Zheng Tongying Feng Qiang Gao wenxian zeng Key Laboratory of Animal Genetics Breeding and Reproduction of Shaanxi Province College of Animal Science and Technology Northwest A&F University

Background: N6-Methyladenosine(m^6A), the most prevalent modification in mammalian m RNA, plays important roles in numerous biological processes. Several m^6A associated proteins such as methyltransferase like 3(METTL3),methyltransferase like 14(METTL14), α-ketoglutarate-dependent dioxygenase Alk B homolog 5(ALKBH5) and YTH domain containing 2(YTHDC2) are involved in the regulation of spermatogenesis and oogenesis. However, the role of the first detected m^6A demethylase, fat mass and obesity associate protein(FTO), in germ cells remains elusive.Elucidation of FTO roles in the regulation of germ cell fate will provide novel insights into the mammalian reproduction.Methods: Mouse GC-1 spg cells were treated with the ester form of meclofenamic acid(MA2) to inhibit the demethylase activity of FTO. The cellular m^6A and m^6Amlevel were analyzed through high performance liquid chromatography combined with tandem mass spectrometry(HPLC/MS-MS). The cell apoptosis was detected via TUNEL and flow cytometry. The cell proliferation was detected through Ed U and western blot. The m RNA level of core cyclin dependent kinases(CDKs) was quantified via q-PCR. RNA decay assay were performed to detect RNA stability. Dual fluorescence assay was conducted to study whether MA2 affects the expression of CDK2 dependent on the m^6A modification at 3’UTR.Results: MA2 significantly increased the cellular m^6A level and down-regulated the expression of CDK1, CDK2, CDK6 and Cd C25 a, resulting in arrest of G1/S transition and decrease of cell proliferation. MA2 downregulated CDK2 m RNA stability. Additionally, mutation of the predicted m^6A sites in the Cdk2–3’UTR could mitigated the degradation of CDK2 m RNA after MA2 treatment.Conclusion: MA2 affected CDKs expression through the m^6A-dependent m RNA degradation pathway, and thus repressed spermatogonial proliferation.

关键词： Cell cycle FTO Meclofenamic acid N6-methyladenosine Spermatogonial proliferation

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An efficient strategy for generation of transgenic mice by lentiviral transduction of male germline stem cells in vivo

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Journal of Animal Science and Biotechnology 2016年第2期7卷 158-166页

作者： Jinzhou Qin Haixia Xu Pengfei Zhang Conghui Zhang Zhendong Zhu Rongfeng Qu Yuwei Qin wenxian zeng College of Animal Science and Technology Northwest A&F University

Background： Male germline stem cells（MGSCs） are a subpopulation of germ cells in the testis tissue. MGSCs are capable of differentiation into spermatozoa and thus are perfect targets for genomic manipulation to generate transgenic animals.Method： The present study was to optimize a protocol of production of transgenic mice through transduction of MGSCs in vivo using lentiviral-based vectors. The recombinant lentiviral vectors with either EF-1 or CMV promoter to drive the expression of enhanced green fluorescent protein（e GFP） transgene were injected into seminiferous tubules or inter-tubular space of 7-day-old and 28-day-old mouse testes. At 5 or 6 wk post-surgery, these pre-founders were mated with wild-type C57BL/6J female mice（1.5 to 2.0-month-old）.Results： Sixty-seven percent of F1 generation and 55.56 % of F2 offspring were positive for eG FP transgene under the control of EF-1 promoter via PCR analysis. The transgenic pups were generated in an injection site-and age-independent manner. The expression of transgene was displayed in the progeny derived from lentiviral vector containing CMV promoter to drive transgene, but it was silenced or undetectable in the offspring derived from lentiviral vector with transgene under EF-1 promoter. The methylation level of g DNA in the promoter region of transgene was much higher in the samples derived lentiviral vectors with EF-1 promoter than that with CMV promoter,suggesting e GFP transgene was suppressed by DNA methylation in vivo.Conclusion： This research reported here an effective strategy for generation of transgenic mice through transduction of MGSCs in vivo using lentivirus vectors with specific promoters, and the transgenic offspring were obtained in an injection site-and age-independent manner. This protocol could be applied to other animal species, leading to advancement of animal transgenesis in agricultural and biomedical fields.

关键词： In vivo Lentivirus vectors Male germline stem cells Transgenesis

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MicroRNA-382 inhibits the proliferation of mouse spermatogoniaby targeting Kmt5a

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BIOCELL 2020年第2期44卷 201-207页

作者： YI ZHENG PENGFEI ZHANG JINSHENG ZHU LINGKAI ZHANG wenxian zeng Key Laboratory for Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling712100China

Spermatogenesis is a highly efficient and intricate process in the testis by which mature spermatozoa are produced daily to maintain lifelong male fertility.Essential to this process are spermatogonia capable of both proliferation and differentiation.Nevertheless,the underlying mechanisms for spermatogonial proliferation and differentiation remain poorly understood.MicroRNAs(miRNAs)are a category of non-coding small RNAs with regulatory functions by binding to the 3’untranslated region(UTR)of the target mRNA.Previous studies have demonstrated that miRNAs are capable of modulating cell proliferation,differentiation and apoptosis,but the roles of individual miRNAs in spermatogonial fate determination remain largely elusive.Here,by using a mouse spermatogonial cell line(GC-1),we investigated the role for miRNA-382 in spermatogonial proliferation.We found that pre-miRNA-382 was expressed in spermatogonia.The luciferase reporter assay demonstrated Kmt5a but not Top1 as a target gene of miRNA-382.Overexpression of miRNA-382 by transfecting a miRNA mimic downregulated Kmt5a at both RNA and protein levels,and further reduced the proliferation and viability of spermatogonia.Knockdown of Kmt5a by RNA interference(RNAi)resulted in a uniform phenotype in spermatogonia.We therefore conclude that miRNA-382 inhibits the proliferation of mouse spermatogonia by targeting Kmt5a.Our finding extends the knowledge about the regulatory roles of miRNAs in spermatogonia and lays the groundwork for diagnosis and treatment of male infertility.

关键词： Spermatogenesis Self-renewal Testis

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