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Comprehensive Transcriptomic Analysis of Mouse Gonadal Development Involving Sexual Differentiation, Meiosis and Gametogenesis Jian Wang1†, Geng G

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Comprehensive Transcriptomic Analysis of Mouse Gonadal Development Involving Sexual Differentiation, Meiosis and Gametogenesis Jian Wang1†, Geng G Wang et al. Biological Procedures Online (2019) 21:20 https://doi.org/10.1186/s12575-019-0108-y RESEARCH Open Access Comprehensive Transcriptomic Analysis of Mouse Gonadal Development Involving Sexual Differentiation, Meiosis and Gametogenesis Jian Wang1†, Geng G. Tian1†, Zhuxia Zheng1†,BoLi2, Qinghe Xing4* and Ji Wu1,2,3* Abstract Background: Mammalian gonadal development is crucial for fertility. Sexual differentiation, meiosis and gametogenesis are critical events in the process of gonadal development. Abnormalities in any of these events may cause infertility. However, owing to the complexity of these developmental events, the underlying molecular mechanisms are not fully understood and require further research. Results: In this study, we employed RNA sequencing to examine transcriptomeprofilesofmurinefemaleandmalegonads at crucial stages of these developmental events. By bioinformatics analysis, we identified a group of candidate genes that may participate in sexual differentiation, including Erbb3, Erbb4,andPrkg2. One hundred and two and 134 candidate genes that may be important for female and male gonadal development, respectively, were screened by analyzing the global gene expression patterns of developing female and male gonads. Weighted gene co-expression network analysis was performed on developing female gonads, and we identified a gene co-expression module related to meiosis. By alternative splicing analysis, we found that cassette-type exon and alternative start sites were the main forms of alternative splicing in developing gonads. A considerable portion of differentially expressed and alternatively spliced genes were involved in meiosis. Conclusion: Taken together, our findings have enriched the gonadal transcriptome database and provided novel candidate genes and avenues to research the molecular mechanisms of sexual differentiation, meiosis, and gametogenesis. Keywords: Gonad, RNA-Seq, Sex-biased expressed genes, Time series cluster, WGCNA, Alternative splicing Introduction Gonads are the important reproductive organs for Infertility is estimated to affect as many as 48.5 million mammals. The process of gonadal development includes couples worldwide [1]. Its incidence may be as high as critical developmental events, such as sexual differenti- 15%. Following cancer, cardiovascular and cerebrovascular ation, meiosis and gametogenesis. Abnormalities in any diseases, infertility has become the third major disorder of these events may cause infertility. The molecular that seriously affects human health and causes consider- regulatory mechanisms of these crucial developmental able stress to patients and their families. events have been the focus of many studies in repro- ductive biology. * Correspondence: [email protected]; [email protected] † Many genes that are important for gonadal development Jian Wang, Geng G. Tian and Zhuxia Zheng contributed equally to this have been discovered. For example, the Sry, Sox9, M33, work. 4Children’s Hospital & Institutes of Biomedical Sciences, Fudan University, 131 Dax1, Wt1, Rspo1, Sf1, Dmrt1, Atrx, Wnt4, Amh, Fgf9, Dong-Chuan Road, Shanghai 200032, China Lhr, Dhh, Insl3, Foxl2 and Sox3 genes play important roles 1 Renji Hospital, Key Laboratory for the Genetics of Developmental & in sexual determination and differentiation [2–5]. The Neuropsychiatric Disorders (Ministry of Education), Bio-X Institutes, School of Medicine, Shanghai Jiao Tong University, Shanghai 200032, China Stra8, Sycp1, Sycp2, Sycp3, Spo11, Rce8, Dmc1, Dazl, Mlh1 Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Wang et al. Biological Procedures Online (2019) 21:20 Page 2 of 13 and Msh5 genes regulate meiosis [5–9]. The Figla, Lhx8, provide novel candidate genes and potential pathways Nobox, Sohlh1, Sohlh2, Bax, Ahr, Gdf9, Pten, Scf, Bcl2 and for further investigation into the molecular mechanisms Rps6 genes have roles in follicular and oocyte develop- of sexual differentiation, meiosis and gametogenesis in ment [5, 10]. The Adamts2, Bcl2l2, Cadm1, Ddx25, Piwil1, gonadal development. Prm1, Prm2, Tbpl1, Tlp, Tnp1, Tnp2 and Ube2b genes are involved in regulating spermatogenesis [5]. Materials and Methods Many previous studies of gonadal development used Animals gene knockout mouse models, and only a small number Eight-week-old C57BL/6 mice were purchased from the of genes could be studied at a time. Gene chips were SLAC Laboratory Animal Co., Shanghai, China. Mice also used to research gonadal development [11–14]. Al- were housed in a 12 h light: 12 h dark cycle. Protocols and though higher throughput was obtained by gene chip use of animals for this study were approved by the Institu- analysis, this research was typically limited to the more tional Animal Care and Use Committee of Shanghai highly expressed known genes. Classical gene chip ana- (SYXK-2018-0028) and were conducted in accordance lysis was unable to research unknown or low abundance with the National Research Council Guide for Care and gene transcripts, nor alternative splicing. Use of Laboratory Animals. In recent years, high-throughput RNA sequencing (RNA-Seq) overcame the above technical shortcomings of Gonad Collection and RNA Extraction gene chips, and also allowed high-throughput investiga- Timed matings were performed by placing a male mouse tion of the whole transcriptome [15]. Previous studies with two females in a cage. Females were checked for have used RNA-Seq to investigate the development of the presence of vaginal plugs the next morning. Noon of mouse gonads. However, these studies either focused on the day when the mating plug was observed was desig- single sex gonads at certain developmental stages, or spe- nated 0.5 dpc. On the relevant days of gestation (12.5, cific cell types in the gonads. Gong et al. investigated the 13.5 and 16.5 dpc), pregnant females were euthanized transcriptome profiling of mouse testes at three postnatal with carbon dioxide. Embryonic gonads were dissected ages: 6 days postnatal, 4 weeks old and 10 weeks old, free of the mesonephros, snap frozen in liquid nitrogen, representing infant, juvenile and adult stages, respectively and stored at − 80 °C. The gonads of 6 dpp mice were [16]. Pan et al. performed a comparative transcriptomic also collected, immediately frozen in liquid nitrogen and analysis using RNA-Seq of ovaries isolated from mice aged stored at − 80 °C. 1weekand8weeksold[17]. McClelland et al. carried out Total RNA was isolated from the gonads of 12.5, 13.5 transcriptomic analysis of mouse fetal Leydig cells [18]. and 16.5 dpc and 6 dpp mice using TRIzol reagent (Invi- Sexual differentiation, meiosis and gametogenesis require trogen, Waltham, Massachusetts, USA) according to the the joint participation and interaction of germ and som- manufacturer’s instructions. An Agilent 2100 Bioanaly- atic cells in the gonads. Therefore, a better understanding zer (Agilent Technologies, Santa Clara, USA) was used of the mechanisms of sexual differentiation may be ob- to measure total RNA quantity and assess RNA tained by comparing female and male gonadal transcrip- integrity. tomes. It is possible that more insight into the molecular mechanisms of sexual differentiation, meiosis and gameto- RNA-Seq Library Construction and Sequencing genesis may be obtained by transcriptomic analysis of The cDNA library was constructed with a SMARTer® murine female and male gonads covering the key stages of Ultra Low Input RNA for lllumina® Sequencing kit developmental corresponding to these critical develop- (Clontech Laboratories, Mountain View, USA). Briefly, mental events. However, such a comparison has not been first-strand cDNA was synthesized using SMARTScribe reported to date. Reverse Transcriptase and then purified using SPRI Here, we systematically compared the transcriptomes Ampure Beads. After amplification using the Polymerase of female and male gonads covering the developmental Mix, double-stranded complementary DNA was purified stages corresponding to sexual differentiation, meiosis using SPRI Ampure Beads. and gametogenesis. Our study used gonads at 12.5 days High-throughput sequencing was performed by Shang- post-coitum (dpc), at which time female and male go- hai Biotechnology Inc. (Shanghai, China) via 100-nt nads begin to show discernible differences, 13.5 dpc paired-end sequencing on an Illumina HiSeq 2500 sys- when female germ cells begin to undergo meiosis, and tem (Illumina, San Diego, USA). male germ cells begin to stop mitosis, 16.5 dpc when most female germ cells are undergoing meiosis, and Reads Mapping and Measurement of Gene Expression male germ cells arrest at the G1/G0 stage, and 6 days After sequencing, clean reads were obtained by remov- post-partum (dpp) when most male germ cells are at the ing reads containing the adaptor sequences, reads with spermatogonial stem cell stage. The current results > 5% ambiguous bases, and low-quality reads, then Wang et al.
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