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Single-cell RNA sequencing of mitoticarrested prospermatogonia with DAZL::GFP chickens and revealing unique epigenetic reprogramming of chickens

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Journal of Animal Science and Biotechnology 2022年第5期13卷 1305-1325页

作者： Hyeon Jeong Choi Kyung Min Jung Deivendran Rengaraj Kyung Youn Lee Eunhui Yoo Tae Hyun Kim Jae Yong Han Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences Seoul National UniversitySeoul 08826South Korea Department of Animal Science Pennsylvania State UniversityState CollegePA 16801USA

Background:Germ cell mitotic arrest is conserved in many vertebrates,including birds,although the time of entry or exit into quiescence phase differs.Mitotic arrest is essential for the normal differentiation of male germ cells into spermatogonia and accompanies epigenetic reprogramming and meiosis inhibition from embryonic development to post-hatch.However,mitotic arrest was not well studied in chickens because of the difficulty in obtaining pure germ cells from relevant developmental stage.Results:We performed single-cell RNA sequencing to investigate transcriptional dynamics of male germ cells during mitotic arrest in DAZL::GFP chickens.Using differentially expressed gene analysis and K-means clustering to analyze cells at different developmental stages(E12,E16,and hatch),we found that metabolic and signaling pathways were regulated,and that the epigenome was reprogrammed during mitotic arrest.In particular,we found that histone H3K9 and H3K14 acetylation(by HDAC2)and DNA demethylation(by DNMT3B and HELLS)led to a transcriptionally permissive chromatin state.Furthermore,we found that global DNA demethylation occurred gradually after the onset of mitotic arrest,indicating that the epigenetic-reprogramming schedule of the chicken genome differs from that of the mammalian genome.DNA hypomethylation persisted after hatching,and methylation was slowly re-established 3 weeks later.Conclusions:We found a unique epigenetic-reprogramming schedule of mitotic-arrested chicken prospermatogonia and prolonged hypomethylation after hatching.This will provide a foundation for understanding the process of germ-cell epigenetic regulation in several species for which this process is not clearly described.Our findings on the biological processes related to sex-specific differentiation of prospermatogonia could help studying germline development in vitro more elaborately.

关键词： DAZL::GFP chickens DNA methylation epigenetic reprogramming Histone acetylation Male germ cell Mitotic arrest Prospermatogonia Single-cell RNA sequencing

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epigenetic reprogramming: roads to pluripotency

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Frontiers in Biology 2010年第1期5卷 8-11页

作者： Wei LI Qi ZHOU State Key Laboratory of Reproductive Biology Institute of ZoologyBeijing 100101China Graduate School Chinese Academy of SciencesBeijing 100049China

epigenetic reprogramming provides valuable resources for customized pluripotent stem cells generation,which are thought to be important bases of future regenerative medicine.Here we review the commonly used methods for epigenetic reprogramming:somatic cell nuclear transfer,cell fusion,cell extract treatment,inducing pluripotency by defined molecules,and briefly discuss their advantages and limitations.Finally we propose that mechanisms underlying epigenetic reprogramming and safety evaluation platform will be future research directions.

关键词： epigenetic reprogramming pluripotency regenerative medicine

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In vivo epigenetic reprogramming of primary human colon cancer cells enhances metastases

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分子细胞生物学报:英文版 2016年第2期8卷 157-173页

作者： Grigori Singovski Carolina Bernal Monika Kuciak Irene Siegl-Cachedenier Arwen Conod Ariel Ruiz i Altaba Department of Genetic Medicine and Development University of Geneva Medical SchoolCH-1211 GenevaSwitzerland

How metastases develop is not well understood and no genetic mutations have been reported as specific metastatic drivers.Here we have addressed the idea that epigenetic reprogramming by GLI-regulated pluripotent stemness factors promotes metastases.Using primary human colon cancer cells engrafted in mice,we find that transient expression of OCT4,SOX2,KLF41/2 cMYC establishes an enhanced pro-metastatic state in the primary tumor that is stable through sequential engraftments and is transmitted through clonogenic cancer stem cells.Metastatic reprogramming alters NANOG methylation and stably boosts NANOG and NANOGP8 expression.Metastases and reprogrammed EMT-like phenotypes require endogenous NANOG,but enhanced NANOG is not sufficient to induce these phenotypes.Finally,reprogrammed tumors enhance GLI2,and we show that GLI2high and AXIN2low,which are markers of the metastatic transition of colon cancers,are prognostic of poor disease outcome in patients.We propose that metastases arise through epigenetic reprogramming of cancer stem cells within primary tumors.

关键词： metastases epigenetic reprogramming NANOG GLI cancer stem cells

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A REF6-dependent H3K27me3-depleted state facilitates gene activation during germination in Arabidopsis

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Journal of Genetics and Genomics 2023年第3期50卷 178-191页

作者： Jie Pan Huairen Zhang Zhenping Zhan Ting Zhao Danhua Jiang State Key Laboratory of Plant Genomics Institute of Genetics and Developmental BiologyThe Innovative Academy for Seed DesignChinese Academy of SciencesBeijing 100101China University of Chinese Academy of Sciences Beijing 100049China

Seed germination is a critical developmental switch from a quiescent state to active growth,which involves extensive changes in metabolism,gene expression,and cellular identity.However,our understanding of epigenetic and transcriptional reprogramming during this process is limited.The histone H3 lysine 27 trimethylation(H3K27me3)plays a key role in regulating gene repression and cell fate specification.Here,we profile H3K27me3 dynamics and dissect the function of H3K27 demethylation during germination in Arabidopsis.Our temporal genome-wide profiling of H3K27me3 and transcription reveals delayed H3K27me3reprogramming compared with transcriptomic changes during germination,with H3K27me3 changes mainly occurring when the embryo is entering into vegetative development.RELATIVE OF EARLY FLOWERING 6(REF6)-mediated H3K27 demethylation is necessary for robust germination but does not significantly contribute to H3K27me3 dynamics during germination,but rather stably establishes an H3K27me3-depleted state that facilitates the activation of hormone-related and expansin-coding genes important for germination.We also show that the REF6 chromatin occupancy is gradually established during germination to counteract increased Polycomb repressive complex 2(PRC2).Our study provides key insights into the H3K27me3 dynamics during germination and suggests the function of H3K27me3 in facilitating cell fate switch.Furthermore,we reveal the importance of H3K27 demethylation-established transcriptional competence in gene activation during germination and likely other developmental processes.

关键词： H3K27me3 epigenetic reprogramming H3K27 demethylation REF6 Germination Arabidopsis thaliana

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Nuclear TIGAR mediates an epigenetic and metabolic autoregulatory loop via NRF2 in cancer therapeutic resistance

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Acta Pharmaceutica Sinica B 2022年第4期12卷 1871-1884页

作者： Hong Wang Qianqian Wang Guodi Cai Zhijian Duan Zoann Nugent Jie Huang Jianwei Zheng Alexander D.Borowsky Jian Jian Li Peiqing Liu Hsing-Jien Kung Leigh Murphy Hong-Wu Chen Junjian Wang School of Pharmaceutical Sciences Sun Yat-sen UniversityGuangzhou 510006China Department of Biochemistry and Molecular Medicine University of CaliforniaDavisSacramentoCA 95817USA Research Institute in Oncology and Hematology University of Manitoba and CancerCare ManitobaWinnipeg R3E 0V9Canada Guangdong Lung Cancer Institute Guangdong Provincial Key Laboratory of Translational Medicine in Lung CancerGuangdong Provincial People’s Hospital and Guangdong Academy of Medical SciencesGuangzhou 510080China Department of Pathology and Laboratory Medicine University of CaliforniaDavisSacramentoCA 95817USA Department of Radiation Oncology University of CaliforniaDavisSacramentoCA 95817USA National-Local Joint Engineering Laboratory of Druggability and New Drugs Evaluation Guangdong Provincial Key Laboratory of New Drug Design and EvaluationSun Yat-sen UniversityGuangzhou 510006China UC Davis Comprehensive Cancer Center School of MedicineUniversity of CaliforniaDavisSacramentoCA 95817USA

Metabolic and epigenetic reprogramming play important roles in cancer therapeutic resistance.However,their interplays are poorly understood.We report here that elevated TIGAR(TP53-induced glycolysis and apoptosis regulator),an antioxidant and glucose metabolic regulator and a target of oncogenic histone methyltransferase NSD2(nuclear receptor binding SET domain protein 2),is mainly localized in the nucleus of therapeutic resistant tumor cells where it stimulates NSD2 expression and elevates global H3K36me2 mark.Mechanistically,TIGAR directly interacts with the antioxidant master regulator NRF2 and facilitates chromatin recruitment of NRF2,H3K4me3 methylase MLL1 and elongating Pol-II to stimulate the expression of both new(NSD2)and established(NQO1/2,PRDX1 and GSTM4)targets of NRF2,independent of its enzymatic activity.Nuclear TIGAR confers cancer cell resistance to chemotherapy and hormonal therapy in vitro and in tumors through effective maintenance of redox homeostasis.In addition,nuclear accumulation of TIGAR is positively associated with NSD2 expression in clinical tumors and strongly correlated with poor survival.These findings define a nuclear TIGAR-mediated epigenetic autoregulatory loop in redox rebalance for tumor therapeutic resistance.

关键词： TIGAR NSD2 NRF2 Metabolism Oxidative stress epigenetic reprogramming Therapeutic resistance Redox homeostasis

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DNA methylation dynamics during germline development

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Journal of Integrative Plant Biology 2022年第12期64卷 2240-2251页

作者： Shengbo He Xiaoqi Feng Guangdong Laboratory for Lingnan Modern Agriculture College of AgricultureSouth China Agricultural UniversityGuangzhou510642 China John Innes Centre Colney LaneNorwichNR47UH UK

DNA methylation plays essential homeostatic functions in eukaryotic genomes.In animals,DNA methylation is also developmentally regulated and,in turn,regulates development.In the past two decades,huge research effort has endorsed the understanding that DNA methylation plays a similar role in plant development,especially during sexual reproduction.The power of whole-genome sequencing and cell isolation techniques,as well as bioinformatics tools,have enabled recent studies to reveal dynamic changes in DNA methylation during germline development.Furthermore,the combination of these technological advances with genetics,developmental biology and cell biology tools has revealed functional methylation reprogramming events that control gene and transposon activities in flowering plant germlines.In this review,we discuss the major advances in our knowledge of DNA methylation dynamics during male and female germline development in flowering plants.

关键词： chromatin DNA methylation epigenetic reprogramming germline small interfering RNA

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Toward pluripotency by reprogramming:mechanisms and application

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Protein & Cell 2013年第11期4卷 820-832页

作者： Tao Wang Stephen TWarren Peng Jin Department of Human Genetics Emory UniversityAtlantaGA 30322USA Genetics and Molecular Biology Graduate Program Emory UniversityAtlantaGA 30322USA

The somatic epigenome can be reprogrammed to a pluri-potent state by a combination of transcription factors.Altering cell fate involves transcription factors coopera-tion,epigenetic reconfi guration,such as DNA methylation and histone modification,posttranscriptional regulation by microRNAs,and so on.Nevertheless,such reprogram-ming is inefficient.Evidence suggests that during the early stage of reprogramming,the process is stochastic,but by the late stage,it is deterministic.In addition to con-ventional reprogramming methods,dozens of small mol-ecules have been identifi ed that can functionally replace reprogramming factors and signifi cantly improve induced pluripotent stem cell(iPSC)reprogramming.Indeed,iPS cells have been created recently using chemical com-pounds only.iPSCs are thought to display subtle genetic and epigenetic variability;this variability is not random,but occurs at hotspots across the genome.Here we dis-cuss the progress and current perspectives in the fi eld.Research into the reprogramming process today will pave the way for great advances in regenerative medicine in the future.

关键词： epigenetic reprogramming induced pluripo-tent stem cells embryonic stem cells disease modeling

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Aberrant MicroRNA Expression and epigenetic reprogramming in Cloned Preimplantation Embryos

Aberrant MicroRNA Expression and Epigenetic Reprogramming in...

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中国畜牧兽医学会动物繁殖学分会第十五届学术研讨会

作者：崔香顺 Laboratory Animal Center of Jilin University Changchun

Low efficiency of somatic cell nuclear transfer(SCNT) is attributed to incomplete reprogramming of transfered nuclei into oocytes.The microRNA(miRNA) genes mir-127 and mir-136 are located near two CpG islands in the imprinted mouse retrotransposon-like gene Rt11,a key gene involved in placenta formation.Mir-15,16,21 and 34a are known as apoptotic related miRNAs. In the mouse preimplantat ion embryos,mir-127 and mir-136 were highly expressed in the parthenotes, but rarely expressed in the androgenotes,and much lower in the cloned embryos than fertilized embryos.Furthermore aberrant methylation status of mir-127 and Rtll were observed in the mouse cloned embryos.In the bovine cloned embryos,TSA treatment significantly improved total and inner cell mass(ICM) cell number and ratio of ICM:trophectoderm(TE),and also decreased the apoptotic index including total,ICM and ratio of ICM:TE.Four apoptotic-related miRNAs,mir-15, 16,21 and 34a were measured by real time RT-PCR.Mir-21 was low expressed in the NT embryos, but enhanced by TSA treatment.These results suggest that analysis of the aberrant epigenetic reprogramming of specific miRNAs in cloned embryos may help to explain the nuclear reprogramming procedures that occur in donor cells following somatic cell nuclear transfer(SCNT).

关键词： Cloned embryo Moses Bovine raiRNA epigenetic reprogramming

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Aberrant DNA methylation in 5′ regions of DNA methyltransferase genes in aborted bovine clones

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Journal of Genetics and Genomics 2008年第9期35卷 559-568页

作者： Jinghe Liu Xingwei Liang Jiaqiao Zhu Liang Wei Yi Hou Da-Yuan Chen Qing-Yuan Sun State Key Laboratory of Reproductive Biology Institute of Zoology Chinese Academy of Sciences Beijing 100101 China Graduate School of Chinese Academy of Sciences Beijing 100101 China

High rate of abortion and developmental abnormalities is thought to be closely associated with inefficient epigenetic reprogramming of the transplanted nuclei during bovine cloning. It is known that one of the important mechanisms for epigenetic reprogramming is DNA methylation. DNA methylation is established and maintained by DNA methyltransferases （DNMTs）, therefore, it is postulated that the inefficient epigenetic reprogramming of transplanted nuclei may be due to abnormal expression of DNMTs. Since DNA methylation can strongly inhibit gene expression, aberrant DNA methylation of DNMT genes may disturb gene expression. But presently, it is not clear whether the methylation abnormality of DNMT genes is related to developmental failure of somatic cell nuclear transfer embryos. In our study, we analyzed methylation patterns of the 5＇ regions of four DNMT genes including Dnmt3a, Dnmt3b, Dnmtl and Dnmt2 in four aborted bovine clones. Using bisulfite sequencing method, we found that 3 out of 4 aborted bovine clones （AF1, AF2 and AF3） showed either hypermethylation or hypomethylation in the 5＇ regions of Dnmt3a and Dnmt3b, indicating that Dnmt3a and Dnmt3b genes are not properly reprogrammed. However, the individual AF4 exhibited similar methylation level and pattern to age-matched in vitro fertilized （IVF） fetuses. Besides, we found that the 5＇ regions of Dnmtl and Dnmt2 were nearly completely unmethylated in all normal adults, IVF fetuses, sperm and aborted clones. Together, our results suggest that the aberrant methylation of Dnmt3a and Dnmt3b 5＇ regions is probably associated with the high abortion of bovine clones.

关键词： DNA methylation DNA methyltransferase epigenetic reprogramming somatic cell nuclear transfer cow

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Insights into epigenetic patterns in mammalian early embryos

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Protein & Cell 2021年第1期12卷 7-28页

作者： Ruimin Xu Chong Li Xiaoyu Liu Shaorong Gao Clinical and Translational Research Center of Shanghai First Maternity and Infant Hospital Shanghai Key Laboratory of Signaling and Disease ResearchFrontier Science Center for Stem Cell ResearchSchool of Life Sciences and TechnologyTongji UniversityShanghai 200092China Institute for Regenerative Medicine Shanghai East HospitalShanghai Key Laboratory of Signaling and Disease ResearchFrontier Science Center for Stem Cell ResearchSchool of Life Sciences and TechnologyTongji UniversityShanghai 200092China Tsingtao Advanced Research Institute Tongji UniversityQingdao 266071China

Mammalian fertilization begins with the fusion of two specialized gametes,followed by major epigenetic remodeling leading to the formation of a totipotent embryo.During the development of the pre-implantation embryo,precise reprogramming progress is a prerequisite for avoiding developmental defects or embryonic lethality,but the underlying molecular mechanisms remain elusive.For the past few years,unprecedented breakthroughs have been made in mapping the regulatory network of dynamic epigenomes during mammalian early embryo development,taking advantage of multiple advances and innovations in low-input genome-wide chromatin analysis technologies.The aim of this review is to highlight the most recent progress in understanding the mechanisms of epigenetic remodeling during early embryogenesis in mammals,including DNA methylation,histone modifications,chromatin accessibility and 3D chromatin organization.

关键词： epigenetic reprogramming DNA methylation histone modifications early embryo development

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