Ana Luiza Camargos Morato, Carolina Gennari Verruma, Cristiana Libardi Miranda Furtado, Rosana Maria Dos Reis
{"title":"In vitro maturation of oocytes: what is already known?†.","authors":"Ana Luiza Camargos Morato, Carolina Gennari Verruma, Cristiana Libardi Miranda Furtado, Rosana Maria Dos Reis","doi":"10.1093/biolre/ioae147","DOIUrl":"10.1093/biolre/ioae147","url":null,"abstract":"<p><p>Assisted reproductive technologies (ARTs) involve the laboratory manipulation of gametes and embryos to help couples with fertility problems become pregnant. One of these procedures, controlled ovarian stimulation, uses pharmacological agents to induce ovarian and follicular maturation in vivo. Despite the effectiveness in achieving pregnancy and live births, some patients may have complications due to over-response to gonadotropins and develop ovarian hyperstimulation syndrome. In vitro maturation (IVM) of oocytes has emerged as a technique to reduce the risk of ovarian hyperstimulation syndrome, particularly in women with polycystic ovary syndrome, and for fertility preservation in women undergoing oncological treatment. Although there are some limitations, primarily due to oocyte quality, recent advances have improved pregnancy success rates and neonatal and infant outcomes. Different terms have been coined to describe variations of IVM, and the technique has evolved with the introduction of hormones to optimize results. In this review, we provide a comprehensive overview of IVM relating hormonal priming, culture system and media, and clinical indications for IVM with its reproductive outcomes during ARTs.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"18-30"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142457239","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Correction to: In vitro production of viable eggs from undeveloped oocytes in mouse preantral follicles by reconstructing granulosa cell-oocyte complexes.","authors":"","doi":"10.1093/biolre/ioae155","DOIUrl":"10.1093/biolre/ioae155","url":null,"abstract":"","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"203"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11736420/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142520916","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ying Han, Junrong Diao, Xinyan Wang, Shuai Zhang, Lina Yuan, Yaqiong Ping, Ge Gao, Yunshan Zhang, Haining Luo
{"title":"Single-cell RNA sequencing reveals common interactions between follicle immune cells and granulosa cells in premature ovarian insufficiency patients†.","authors":"Ying Han, Junrong Diao, Xinyan Wang, Shuai Zhang, Lina Yuan, Yaqiong Ping, Ge Gao, Yunshan Zhang, Haining Luo","doi":"10.1093/biolre/ioae157","DOIUrl":"10.1093/biolre/ioae157","url":null,"abstract":"<p><p>This study aims to investigate the follicle microenvironment of individuals with premature ovarian insufficiency (POI), normal ovarian reserve (normal), and advanced maternal age (AMA), and identify potential therapeutic targets. A total of nine women, including three POI, three normal, and three AMA women, who underwent in vitro fertilization or intracytoplasmic sperm injection were included in this study. For each participant, the first punctured follicle not containing cumulus cells were submitted to single-cell RNA sequencing to explore the characteristics of the follicle microenvironment of POI, normal, and AMA individuals. A total of 87,323 cells were isolated and grouped into six clusters: T cells, B cells, neutrophils, basophils, mononuclear phagocytes, and granulosa cells. Further analysis demonstrated that the population of granulosa cells in cluster 6 was increased in AMA and POI patients, whereas the population of gamma delta T (GDT) cells was decreased. We also found that the genes that were differentially expressed between GDT cells and monocytes were enriched in ribosome- and endoplasmic reticulum (ER)-related pathways. In addition, it showed that VEGFA-FLT1 interaction between the monocytes and granulosa cells may be lost in the AMA and POI patients as compared with the normal group. Loss of the VEGFA-FLT1 interaction in monocytes and granulosa cells, along with enriched ER- and ribosome-related pathways, may drive excess inflammation, accelerating granulosa cell senility and contributing to infertility. This study provides new insights into the pathogenesis of POI and aging and highlights the VEGFA-FLT1 interaction may be a potential therapeutic target for reducing inflammation and treating POI.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"156-168"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11736418/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142602953","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Taurine is essential for mouse uterine luminal fluid resorption during implantation window via the SCNN1A and AQP8 signaling†.","authors":"Yewen Zhou, Shaona Pei, Guobin Qiu, Jinglin Zhang, Hongzhou Guo, Sheng Cui, Zongping Liu, Di Zhang","doi":"10.1093/biolre/ioae152","DOIUrl":"10.1093/biolre/ioae152","url":null,"abstract":"<p><p>Uterine fluid homeostasis during peri-implantation is crucial for successful embryo implantation. Taurine (Tau) plays a crucial role in regulating osmotic pressure and ion transport. However, the precise mechanisms underlying Tau-mediated regulation of uterine fluid homeostasis during peri-implantation in mice remain unclear. In this study, we generated a Tau-deficient mouse model by administering Tau-free diet to Csad knockout (Csad-/-) mice to block endogenous Tau synthesis and exogenous Tau absorption (Csad-/--Tau free). Our findings demonstrated that Csad-/--Tau free mice with diminished level of Tau exhibited decreased rates of embryo implantation and impaired fertility. Further analysis revealed that the expression of Scnn1a was down-regulated during the implantation window, while Aqp8 was upregulated in Csad-/--Tau free mice, leading to uterine luminal fluid retention and defects in luminal closure, resulting in failed embryo implantation. Additionally, it was also found that E2 inhibited uterine Csad expression and Tau synthesis, while P4 promoted them. Therefore, our findings suggest that ovarian steroid hormones regulate Csad expression and Tau synthesis, thereby affecting release and resorption of uterine luminal fluid, ultimately impacting embryo implantation success.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"140-155"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142457241","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hao Zhang, Xinlu Wang, Meng Dong, Jie Wang, Weidong Ren
{"title":"Unveiling novel regulatory mechanisms of miR-5195-3p in pelvic organ prolapse pathogenesis†.","authors":"Hao Zhang, Xinlu Wang, Meng Dong, Jie Wang, Weidong Ren","doi":"10.1093/biolre/ioae162","DOIUrl":"10.1093/biolre/ioae162","url":null,"abstract":"<p><p>Pelvic organ prolapse is a condition that significantly affects women's quality of life. The pathological mechanism of pelvic organ prolapse is not yet fully understood, and its pathogenesis is often caused by multiple factors, including the metabolic imbalance of the extracellular matrix. This study aims to investigate the role of miR-5195-3p, a microRNA, in the pathology of pelvic organ prolapse and its regulatory mechanism. Using various molecular biology techniques such as real-time reverse transcription Polymerase Chain Reaction (PCR), fluorescence in situ hybridization, immunohistochemistry, and Western blot, miR-5195-3p expression was examined in vaginal wall tissues obtained from pelvic organ prolapse patients. Results revealed an up-regulation of miR-5195-3p expression in these tissues, showing a negative correlation with the expression of extracellular matrix-related proteins. Further analysis using bioinformatics tools identified Lipoxygenase (LOX) as a potential target in pelvic organ prolapse. Dual luciferase reporter gene experiments confirmed LOX as a direct target of miR-5195-3p. Interestingly, regulating the expression of LOX also influenced the transforming growth factor β1 signaling pathway and had an impact on extracellular matrix metabolism. This finding suggests that miR-5195-3p controls extracellular matrix metabolism by targeting LOX and modulating the TGF-β1 signaling pathway. In conclusion, this study unveils the involvement of miR-5195-3p in the pathological mechanism of pelvic organ prolapse by regulating extracellular matrix metabolism through the LOX/TGF-β1 axis. These findings reveal new mechanisms in the pathogenesis of pelvic organ prolapse, providing a theoretical foundation and therapeutic targets for further research on pelvic organ prolapse treatment.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"86-101"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142614338","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The loss of dNK1/2 and EVT1 cells at the maternal-fetal interface is associated with recurrent miscarriage†.","authors":"Yijun Yang, Jiangnan Qiu, Qiaoqiao Xu, Yun Fan, Hui Wang, Hong Qian, Zhu Wu, Yuchen Zhang, Yingchun Gao, Can Shi, Chuncheng Lu, Yankai Xia, Wenjun Cheng","doi":"10.1093/biolre/ioae136","DOIUrl":"10.1093/biolre/ioae136","url":null,"abstract":"<p><p>Recurrent miscarriage is a chronic and heterogeneous pregnancy disorder lacking effective treatment. Alterations at the maternal-fetal interface are commonly observed in recurrent miscarriage, with the loss of certain cell subpopulations believed to be a key cause. Through single-cell sequencing of recurrent miscarriage patients and healthy donors, we aim to identify aberrancy of cellular features in recurrent miscarriage tissues, providing new insights into the research. Natural killer cells, the most abundant immune cells in the decidua, are traditionally classified into dNK1, dNK2, and dNK3. In this study, we identified a new subset, dNK1/2, absent in recurrent miscarriage tissues. This subset was named because it expresses biomarkers of both dNK1 and dNK2. With further analysis, we discovered that dNK1/2 cells play roles in immunoregulation and cytokine secretion. On the villous side of the interface, a notable decrease of extravillous trophoblast cells was identified in recurrent miscarriage tissues. We clustered extravillous trophoblasts into EVT1 (absent in recurrent miscarriage) and EVT2 (retained in recurrent miscarriage). Pseudotime analysis revealed distinct differentiation paths, identifying CCNB1, HMGB1, and NPM1 as EVT1 biomarkers. Additionally, we found that EVT1 is involved in the regulation of cell death, while EVT2 exhibited more angiogenic activity. Cell communication analysis revealed that interaction between EVT1 and dNK1/2 mediates chemotaxis and endothelial cell regulation, crucial for spiral artery remodeling. The loss of this interaction may impair decidualization, which is associated with recurrent miscarriage. In summary, we propose that the loss of dNK1/2 and EVT1 cells is a significant pathological feature of recurrent miscarriage.</p><p><strong>Summary sentence: </strong>The communication between EVT1 and dNK1/2 mediated the chemotaxis of EVT1 and facilitated regulation of endothelial cell death, initiating spiral artery remodeling. The loss of this specific cellular interaction may result in impaired decidualization, leading to recurrent miscarriage.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"119-129"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142280110","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Brianna L Kline, Nicole A Siddall, Fernando Wijaya, Catherine J Stuart, Luisa Orlando, Shabnam Bakhshalizadeh, Fateme Afkhami, Katrina M Bell, Sylvie Jaillard, Gorjana Robevska, Jocelyn A van den Bergen, Shirin Shahbazi, Ambro van Hoof, Katie L Ayers, Gary R Hime, Andrew H Sinclair, Elena J Tucker
{"title":"Functional characterization of human recessive DIS3 variants in premature ovarian insufficiency†.","authors":"Brianna L Kline, Nicole A Siddall, Fernando Wijaya, Catherine J Stuart, Luisa Orlando, Shabnam Bakhshalizadeh, Fateme Afkhami, Katrina M Bell, Sylvie Jaillard, Gorjana Robevska, Jocelyn A van den Bergen, Shirin Shahbazi, Ambro van Hoof, Katie L Ayers, Gary R Hime, Andrew H Sinclair, Elena J Tucker","doi":"10.1093/biolre/ioae148","DOIUrl":"10.1093/biolre/ioae148","url":null,"abstract":"<p><p>Premature ovarian insufficiency (POI) is characterized by the loss or complete absence of ovarian activity in women under the age of 40. Clinical presentation of POI varies with phenotypic severity ranging from premature loss of menses to complete gonadal dysgenesis. POI is genetically heterogeneous with >100 causative gene variants identified thus far. The etiology of POI varies from syndromic, idiopathic, monogenic to autoimmune causes the condition. Genetic diagnoses are beneficial to those impacted by POI as it allows for improved clinical management and fertility preservation. Identifying novel variants in candidate POI genes, however, is insufficient to make clinical diagnoses. The impact of missense variants can be predicted using bioinformatic algorithms but computational approaches have limitations and can generate false positive and false negative predictions. Functional characterization of missense variants, is therefore imperative, particularly for genes lacking a well-established genotype:phenotype correlation. Here we used whole-exome sequencing (WES) to identify the first case of a homozygous missense variant in DIS3 (c.2320C > T; p.His774Tyr) a critical component of the RNA exosome in a POI patient. This adds to the previously described compound heterozygous patient. We perform the first functional characterization of a human POI-associated DIS3 variant. A slight defect in mitotic growth was caused by the variant in a Saccharomyces cerevisiae model. Transgenic rescue of Dis3 knockdown in Drosophila melanogaster with human DIS3 carrying the patient variant led to aberrant ovarian development and egg chamber degeneration. This supports a potential deleterious impact of the human c.2320C > T; p.His774Tyr variant.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"102-118"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11736438/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142457236","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eliza Winek, Lidia Wolińska-Nizioł, Katarzyna Szczepańska, Anna Szpakowska, Olga Gewartowska, Izabela Wysocka, Magdalena Grzesiak, Aneta Suwińska
{"title":"Zygotic activin A is dispensable for the mouse preimplantation embryo development and for the derivation and pluripotency of embryonic stem cells†.","authors":"Eliza Winek, Lidia Wolińska-Nizioł, Katarzyna Szczepańska, Anna Szpakowska, Olga Gewartowska, Izabela Wysocka, Magdalena Grzesiak, Aneta Suwińska","doi":"10.1093/biolre/ioae156","DOIUrl":"10.1093/biolre/ioae156","url":null,"abstract":"<p><p>In this work, we aimed to determine the role of activin A during crucial events of mouse embryogenesis and distinguish the function of the protein of zygotic origin and the one secreted by the maternal reproductive tract. To this end, we recorded the progression of development and phenotype of Inhba knockout embryos and compared them with the heterozygotes and wild-type embryos using time-lapse imaging and detection of lineage-specific markers. We revealed that the zygotic activin A deficiency does not impair the course and rate of development of embryos to the blastocyst stage. Inhba knockout embryos form functional epiblast, as evidenced by their ability to give rise to embryonic stem cells. Our study is the first to show that derivation, maintenance in culture, and pluripotency of embryo-derived embryonic stem cells are exogenous and endogenous activin A independent. However, the implantation competence of activin A-deficient embryos may be compromised as indicated in the outgrowth assay.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"31-45"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11736436/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142590105","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ramsés Santacruz-Márquez, Adira M Safar, Mary J Laws, Endia J Fletcher, Daryl D Meling, Romana A Nowak, Lori T Raetzman, Jodi A Flaws
{"title":"Dietary exposure to di(2-ethylhexyl) phthalate for 6 months alters markers of female reproductive aging in mice†.","authors":"Ramsés Santacruz-Márquez, Adira M Safar, Mary J Laws, Endia J Fletcher, Daryl D Meling, Romana A Nowak, Lori T Raetzman, Jodi A Flaws","doi":"10.1093/biolre/ioae164","DOIUrl":"10.1093/biolre/ioae164","url":null,"abstract":"<p><p>The female reproductive system ages before any other physiological system, making it a sensitive indicator of aging. Early reproductive aging is associated with the early onset of infertility and an increased risk of several diseases. During aging, systemic and reproductive oxidative stress and inflammation levels increase through inflammasome activation, leading to ovarian follicle loss. Other markers of reproductive aging include increased fibrosis and shortening of telomeres in ovarian cells. The factors that accelerate reproductive aging are unclear, but likely involve exposure to endocrine-disrupting chemicals such as phthalates. Di(2-ethylhexyl) phthalate (DEHP) is a widely used phthalate and humans are exposed to it daily. Several studies show that DEHP induces reproductive toxicity by affecting estrous cyclicity, follicle numbers, and hormone levels. However, little is known about the mechanisms underlying DEHP-induced early onset of reproductive aging. Thus, this study tested the hypothesis that dietary exposure to DEHP induces early reproductive aging by affecting inflammation, fibrosis, and the expression of telomere regulators and antioxidant enzymes. Adult CD-1 female mice were exposed to vehicle (corn oil) or DEHP (0.5, 1.5, or 1500 ppm) via the chow for 6 months. Exposure to DEHP increased the expression of antioxidant enzymes and Caspase 3, increased expression of telomere-associated genes, and increased fibrosis levels in the ovary. In addition, DEHP exposure for 6 months altered ovarian and systemic inflammatory status. Collectively, our novel data suggest that 6-month dietary exposure to DEHP may accelerate reproductive aging by affecting several reproductive aging markers in female mice.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"191-202"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142614333","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jiaying Qin, Bo Lv, Yao Yao, Xuan Han, Zhigang Xue, Chao-Po Lin, Jinfeng Xue, Yazhong Ji
{"title":"CTNND1 affects trophoblast proliferation and specification during human embryo implantation.","authors":"Jiaying Qin, Bo Lv, Yao Yao, Xuan Han, Zhigang Xue, Chao-Po Lin, Jinfeng Xue, Yazhong Ji","doi":"10.1093/biolre/ioae163","DOIUrl":"10.1093/biolre/ioae163","url":null,"abstract":"<p><p>The placenta, serving as the crucial link between maternal and infant, plays a pivotal role in maintaining a healthy pregnancy. Placental dysplasia can lead to various complications, underscoring the importance of understanding trophoblast lineage development. During peri-implantation, the trophectoderm undergoes differentiation into cytotrophoblast, syncytiotrophoblast, and extravillous trophoblast. However, the specification and regulation of human trophoblast lineage during embryo implantation, particularly in the peri-implantation phase, remain to be explored. In this study, we employed a co-culture model of human endometrial cells and native embryos and analyzed the single-cell transcriptomic data of 491 human embryonic trophoblasts during E6 to E10 to identify the key regulatory factors and the lineage differentiation process during peri-implantation. Our data identified four cell subpopulations during the implantation, including a specific transitional state toward the differentiation in which the CTNND1, one crucial component of Wnt signaling pathway activated by cadherins, acted as a crucial factor. Knockdown of CTNND1 impacted the proliferative capacity of human trophoblast stem cells, leading to early extravillous trophoblast-like differentiation. Intriguingly, ablation of CTNND1 compromised the terminal differentiation of human trophoblast stem cells toward syncytiotrophoblast or extravillous trophoblast in vitro. These findings contribute valuable insights into trophoblast lineage dynamics and offer a reference for research on placental-related diseases.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"46-53"},"PeriodicalIF":3.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142675032","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}