Katie L Bidne, Kathryn E Erickson, Theresa L Powell, Thomas Jansson
{"title":"Mechanistic target of rapamycin signaling activity in the human placenta across gestation and in maternal obesity†.","authors":"Katie L Bidne, Kathryn E Erickson, Theresa L Powell, Thomas Jansson","doi":"10.1093/biolre/ioaf007","DOIUrl":"10.1093/biolre/ioaf007","url":null,"abstract":"<p><p>The mechanistic target of rapamycin system is vital to placental development, formation, and function. Alterations in this system in the placenta have been associated with altered fetal growth. However, changes in placental mechanistic target of rapamycin signaling across gestation are poorly understood. We collected 81 human placental samples from 4 to 40 weeks gestation to test the hypothesis that placental mechanistic target of rapamycin signaling activity increases over gestation and is activated in maternal obesity in early gestation. Proteins involved in upstream mechanistic target of rapamycin regulation and mTORC1/2 downstream signaling were quantified using immunoblotting in placentas of male or female fetuses. Readouts of mTORC1 activation, phospho-rpS6, and phospho-4EBP1 were highest in first trimester and decreased across gestation. Phosphorylation of AKT (308 and 473) increased over gestation. Interestingly, abundance of cytochrome c oxidase I and mitochondrial ATP synthase, key subunits of mitochondrial complexes III/IV and V, respectively, were elevated in first trimester obese placentas compared to control, but only in placenta from female fetuses. We suggest that the high placental mechanistic target of rapamycin signaling activity in early pregnancy may be related to the high anabolism and active trophoblast proliferation and invasion in the second half of the first trimester. In addition, we conclude that maternal obesity has only limited impact on this key placental signaling pathway across gestation in women.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"540-549"},"PeriodicalIF":3.1,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11911553/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142969470","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}
Hannah McDowell, Isaac Vieco-Martí, Maya VanZanten, Shravya Pant, Hana Kubo, Diane C Saunders, Monica M Laronda, Sofía Granados-Aparici
{"title":"Digital analysis of ovarian tissue: generating a standardized method of follicle analysis†.","authors":"Hannah McDowell, Isaac Vieco-Martí, Maya VanZanten, Shravya Pant, Hana Kubo, Diane C Saunders, Monica M Laronda, Sofía Granados-Aparici","doi":"10.1093/biolre/ioaf022","DOIUrl":"10.1093/biolre/ioaf022","url":null,"abstract":"","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"416-419"},"PeriodicalIF":3.1,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11911554/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143188049","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":"Green tea polyphenols alleviate di (2-ethylhexyl) phthalate-induced testicular injury in mice via lncRNA-miRNA-mRNA axis†.","authors":"Heng Shi, Xin-Hai Zhao, Qin Peng, Xian-Ling Zhou, Si-Si Liu, Chuan-Chuan Sun, Qiu-Yu Cao, Shi-Ping Zhu, Sheng-Yun Sun","doi":"10.1093/biolre/ioae179","DOIUrl":"10.1093/biolre/ioae179","url":null,"abstract":"<p><p>Di(2-ethylhexyl) phthalate (DEHP) is a commonly used plasticizer known for its toxic effects on the male reproductive system. Green tea polyphenols (GTPs), recognized for their antioxidant and anti-inflammatory properties, have demonstrated protective effects on various organs, but the mechanisms by which GTPs mitigate DEHP-induced testicular damage remain unclear. Healthy male C57BL/6J mice were divided into five groups: control, DEHP, DEHP + GTP treatment, GTP, and oil groups. Testicular histopathological changes were assessed using hematoxylin-eosin (H&E), periodic acid-Schiff (PAS), and Masson staining. Ultrastructural alterations were examined through transmission electron microscopy. High-throughput sequencing was performed to analyze the expression of mRNA, miRNA, and lncRNA and construct an lncRNA-miRNA-mRNA regulatory network for identifying key regulatory axes. Mice in the DEHP group exhibited significant testicular damage, including reduced sperm count, mitochondrial deformation, and endoplasmic reticulum dilation. GTP treatment notably improved testicular structural integrity, restored sperm count, and alleviated mitochondrial and endoplasmic reticulum damage. Additionally, DEHP significantly increased activated CD8+ T cells, which were reduced with GTP treatment. High-throughput sequencing revealed that GTP treatment exerted protective effects through the regulation of six key lncRNA-miRNA-mRNA axes. GTPs significantly protect against DEHP-induced testicular damage, and the lncRNA-miRNA-mRNA regulatory axes play a potential role in this process.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"485-500"},"PeriodicalIF":3.1,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142806075","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}
Bryan A Niedenberger, Heather A Belcher, Emma A Gilbert, Matthew A Thomas, Christopher B Geyer
{"title":"Utilization of the QuPath open-source software platform for analysis of mammalian spermatogenesis†.","authors":"Bryan A Niedenberger, Heather A Belcher, Emma A Gilbert, Matthew A Thomas, Christopher B Geyer","doi":"10.1093/biolre/ioaf011","DOIUrl":"10.1093/biolre/ioaf011","url":null,"abstract":"<p><p>The adult mammalian testis is filled with seminiferous tubules, which contain somatic Sertoli cells along with germ cells undergoing all phases of spermatogenesis. During spermatogenesis in postnatal mice, male germ cells undergo at least 17 different nomenclature changes as they proceed through mitosis as spermatogonia (=8), meiosis as spermatocytes (=6), and spermiogenesis as spermatids (=3). Adding to this complexity, combinations of germ cells at each of these stages of development are clumped together along the length of the seminiferous tubules. Due to this, considerable expertise is required for investigators to accurately analyze changes in spermatogenesis in animals that have spontaneous mutations, have been genetically modified (transgenic or knockout/knockin), or have been treated with pharmacologic agents. Here, we leverage our laboratory's expertise in spermatogenesis to optimize the open-source \"Quantitative Pathology & Bioimage Analysis\" software platform for automated analyses of germ and somatic cell populations in both the developing and adult mammalian testis.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"583-599"},"PeriodicalIF":3.1,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11911557/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142999563","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}
Mariângela Bueno Cordeiro Maldonado, Maria Belen Rabaglino, Gabrielle Heather Cannon, Peter James Hansen
{"title":"Effects of endometrial embryokines on the preimplantation bovine embryo to create a gene expression signature consistent with a high competence phenotype†.","authors":"Mariângela Bueno Cordeiro Maldonado, Maria Belen Rabaglino, Gabrielle Heather Cannon, Peter James Hansen","doi":"10.1093/biolre/ioaf014","DOIUrl":"10.1093/biolre/ioaf014","url":null,"abstract":"<p><p>Optimal embryonic development depends upon cell-signaling molecules released by the maternal reproductive tract called embryokines. The identity of specific embryokines that enhance the competence of the embryo for sustained survival is largely lacking. The current objective was to evaluate the effects of three putative embryokines in cattle on embryonic development to the blastocyst stage. The molecules tested were vascular endothelial growth factor A (VEGFA), C-X-C motif chemokine ligand 12 (CXCL12), and interleukin-6 (IL6). Molecules were added from day 4 to 7.5 of culture at 50 ng/mL (VEGFA and CXCL12) or 100 ng/mL (IL6). Endpoints were development to the blastocyst stage and transcript abundance for 94 specific genes involved in lineage commitment, epigenetic regulation, and other functions. Among the genes examined were eight whose transcript abundance has been related to embryo competence for survival after embryo transfer. None of the molecules increased the proportion of putative zygotes or cleaved embryos becoming blastocysts at day 7.5 of development. An embryo competence index based on a Bayesian multiple regression formula to weigh transcript abundance of the eight biomarker genes was not affected by treatment with VEGFA but was increased by both CXCL12 and IL6. The transcript abundance of 5 genes was modified by VEGFA, 19 by CXCL12, and 19 by IL6. A total of 11 genes were modified in a similar manner by CXCL12 and IL6. Most differentially expressed genes for CXCL12 and IL6 were downregulated, suggesting that the embryokines may promote a less energetically demanding metabolic state than would be the case in their absence.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"447-457"},"PeriodicalIF":3.1,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143051455","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}
Yuru Luo, Shuang Liu, Yuan Fang, Hongyu Su, Jinling Dong, Baochang Lai, Zhen Wang, Juan Yang, Donghong Zhang, Yidong Wang
{"title":"Loss of N-6 adenine-specific DNA methyltransferase 1 leads to meiotic prophase abnormalities and male sub-fertility in mice.","authors":"Yuru Luo, Shuang Liu, Yuan Fang, Hongyu Su, Jinling Dong, Baochang Lai, Zhen Wang, Juan Yang, Donghong Zhang, Yidong Wang","doi":"10.1093/biolre/ioaf052","DOIUrl":"https://doi.org/10.1093/biolre/ioaf052","url":null,"abstract":"<p><p>Mammalian sexual reproduction critically relies on the generation of haploid gametes following a specialized cell division process known as meiosis. Here, we demonstrate that N-6 Adenine-Specific DNA methyltransferase 1 (N6AMT1) plays a crucial role in the progression of meiosis during spermatogenesis, as follows. N6AMT1 was expressed in germ cells throughout the entire process of spermatogenesis, with a peak in mRNA levels in spermatocytes at the prophase I stage of meiosis. Germ cell-specific deletion of N6amt1 in mice resulted in male subfertility as well as a significant reduction in sperm count. Notably, N6amt1-null spermatocytes exhibited meiotic arrest at prophase I and extensive apoptosis. Chromosome spreading assays revealed that N6amt1 loss impaired meiotic sex chromosome inactivation (MSCI) and delayed DNA double-strand break (DSB) repair. Correspondingly, transcriptomic analysis identified a substantial increase in transcript levels for genes mapping to sex chromosomes in N6amt1-null mutants, consistent with disruptions in MSCI. Moreover, N6AMT1 deficiency led to a significant upregulation in the steady-state mRNA levels of genes involved in the p53 pathway and functionally activated p53 signaling. Through integrated analysis of data from single-cell RNA-seq and bulk RNA-seq experiments, we found that knockout of N6amt1 primarily affected the transcriptomic profiles of normal pachytene spermatocytes. Taken together, our findings demonstrate that N6AMT1 is required for quantitatively normal male fertility in mice and involved in the molecular mechanisms for meiotic progression during spermatogenesis, including MSCI and DSB repair.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":""},"PeriodicalIF":3.1,"publicationDate":"2025-03-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143613345","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":"Novel insights into human CRISP2: localization in reproductive tissues and sperm, and molecular characterization.","authors":"Thibault Masai, Amandine Delnatte, Marie Dendievel, Denis Nonclercq, Annica Frau, Jean-François Simon, Vanessa Arcolia, Ruddy Wattiez, Baptiste Leroy, Patricia S Cuasnicu, Pascale Lybaert, Elise Hennebert","doi":"10.1093/biolre/ioaf051","DOIUrl":"https://doi.org/10.1093/biolre/ioaf051","url":null,"abstract":"<p><p>CRISP2 is enriched in the male reproductive system of mammals and plays roles in spermatogenesis, sperm motility, and fertilization. Although extensively investigated in rodents and boars, human CRISP2 (hCRISP2) remains poorly studied, particularly concerning its localization in testicular and epididymal tissues and its molecular features. In this study, we used immunofluorescence to determine the localization of hCRISP2 in testis, epididymis, and ejaculated sperm. While no expression was observed in the epididymal epithelium, hCRISP2 was detected at different stages during spermatogenesis. Specifically, hCRISP2 was found in the nucleus of primary spermatocytes and of both round and early elongated spermatids. In elongated spermatids, it was additionally observed in the cytoplasm, the flagellum, and the equatorial segment of the acrosome (EqS). The presence of aggregated material with hCRISP2 immunoreactivity in the apical pole of Sertoli cells suggests that most of the hCRISP2 involved in spermatogenesis is phagocytized by these cells during spermiation. In ejaculated sperm, hCRISP2 was found in the cytoplasmic droplet, flagellum, and EqS, consistent with its described roles in sperm motility and gamete fusion. Native and SDS-PAGE combined with western blot analyses depicted the ability of hCRISP2 to form stable high molecular weight complexes and mass spectrometry revealed that these complexes likely consist exclusively of hCRISP2. Furthermore, we showed that hCRISP2 undergoes only limited post-translational modifications. These findings shed light into the dynamic localization of hCRISP2 throughout spermatogenesis and in ejaculated sperm, as well as its molecular features, enhancing our understanding of its pivotal functional roles and relevance for male fertility.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":""},"PeriodicalIF":3.1,"publicationDate":"2025-03-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143613349","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}
Cheng Yang, Xinyu Feng, Yingfang Guo, Aftab Shaukat, Zhimin Wu, Yu Chen, Lu Meng, Ganzhen Deng
{"title":"Bta-miR-93 regulates the maternal-fetal tolerance in dairy cows via promoting PD-L1-mediated M2 macrophage polarization†.","authors":"Cheng Yang, Xinyu Feng, Yingfang Guo, Aftab Shaukat, Zhimin Wu, Yu Chen, Lu Meng, Ganzhen Deng","doi":"10.1093/biolre/ioaf046","DOIUrl":"https://doi.org/10.1093/biolre/ioaf046","url":null,"abstract":"<p><p>Bovine embryo resorption is one of the key factors restricting the reproductive efficiency in dairy cattle, which mainly occurs in the early stage of maternal recognition of pregnancy (MRP), causing substantial economic losses to the dairy industry. Macrophages, the most numerous endometrial immune cells in cows during early pregnancy, are critical in developing maternal-fetal immune tolerance. However, the mechanism of their action on the maternal-fetal interface of dairy cows remains unknown. MicroRNAs have important roles in immune tolerance and macrophage polarization, but the underlying mechanisms still need further investigation. In previous laboratory studies, RNA-sequencing revealed that bta-miR-93 was dramatically reduced in bovine endometrial luminal epithelial cells (bEECs) upon IFN-τ stimulation. In current study, it is revealed that the expression of bta-miR-93 was decreased substantially in the endometrium of pregnant cows, and negatively correlated with that of PD-L1. In vitro experiments displayed that suppression of bta-miR-93 promoted M2 Polarization via promoting PD-L1/PD-1/AKT/mTOR signaling pathway in bEECs and bovine macrophages (BoMac) co-culture model, and vice versa. The 3'-UTR of PD-L1 is directly regulated by bta-miR-93. Furthermore, our in vivo studies revealed that overexpression of bta-miR-93 efficiently leads to embryo resorption and suppression of M2 polarization in mice. Overall, the findings suggested that reduced bta-miR-93 levels were found to be implicated in pregnancy immune tolerance by boosting M2 macrophage polarization via promoting PD-L1/PD-1/AKT/mTOR signaling pathway. Bta-miR-93 might be investigated as auspicious identification signal for a successful pregnancy and a potential therapeutic target for reproductive disorders.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":""},"PeriodicalIF":3.1,"publicationDate":"2025-03-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143623391","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 effects of sika deer oviduct epithelial cell-derived extracellular vesicles on oocytes and parthenogenetic embryos.","authors":"Bing Hu, Shu-Ming Shi, Xian-Feng Yu, Yu-Yan He, Zhi-Chao Chi, Lai-Ming Tian, Guan-Lin Jia, Ilkeun Kong, Yong-Xun Jin, Ming-Jun Zhang","doi":"10.1093/biolre/ioaf048","DOIUrl":"https://doi.org/10.1093/biolre/ioaf048","url":null,"abstract":"<p><p>Oviducts contain various nutrients that provide energy during oocyte development. This study aimed to improve the efficiency of in vitro reproduction using extracellular vesicles (EVs) produced by the oviduct epithelial cells of sika deer (Cervus nippon). Surprisingly, the uptake of deer oviduct epithelial cell extracellular vesicles (DOEC-EVs) by cumulus-oocyte complexes, which were encapsulated by dense cumulus cells (CCs), occurred only in CCs during maturation. Therefore, we hypothesized that DOEC-EVs are transported to oocytes through CCs to exert their effects. We first investigated the effects of DOEC-EVs on the expansion capacity of the cumulus-oocyte complexes, as well as cell cycle progression, proliferation, apoptosis, and lactate and pyruvate levels in CCs, and examined reactive oxygen species levels, mitochondrial function, and key gene expression. The results showed that DOEC-EVs regulated cell cycle progression, promoted proliferation, reduced apoptosis, and improved antioxidant capacity and glycolysis, and through the oocyte first polar body excretion rate, reactive oxygen levels and mitochondrial membrane potential, it was shown that CC promoted in vitro oocyte maturation, improved the antioxidant capacity and mitochondrial function of oocytes, and promoted parthenogenetic embryo development. These results suggest that DOEC-EVs improve the efficiency of oocyte development in deer in vitro by acting on CCs, laying the foundation for further research on in vitro deer reproduction.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":""},"PeriodicalIF":3.1,"publicationDate":"2025-03-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143603422","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}
Camilla H K Hughes, Adelaide C Hellmers, M Isabel Silva, Troy L Ott, Joy L Pate
{"title":"Interferon tau-dependent and -independent changes in the bovine corpus luteum of early pregnancy.","authors":"Camilla H K Hughes, Adelaide C Hellmers, M Isabel Silva, Troy L Ott, Joy L Pate","doi":"10.1093/biolre/ioaf044","DOIUrl":"https://doi.org/10.1093/biolre/ioaf044","url":null,"abstract":"<p><p>The effect of interferon tau (IFNT) on the uterus is critical for maternal recognition of pregnancy in ruminants, while its direct role in luteal function is less well understood. To address this, we performed two experiments. In experiment 1, cattle received intrauterine infusions of either: bovine serum albumin (BSA; vehicle) or vehicle with IFNT from day 14 to 16 of the estrous cycle or vehicle with IFNT from day 14 to 19 or vehicle with IFNT from day 14 to 19 with pregnancy associated glycoprotein (PAG) from day 17 to 19. Corpora lutea (CL) were collected on day 17 or 20 and RNAseq was performed. In experiment 2, cultured luteal steroidogenic cells from cyclic (day 10-12) cattle were treated with IFNT and RNAseq was performed. Treatment with IFNT resulted in luteal changes (in vivo: 130 transcripts; in vitro: 2981 transcripts), while addition of PAG resulted in 13 changed transcripts. Only 31% of the genes that changed in the CL during early pregnancy (Hughes et al., 2020) were regulated by IFNT; these were antiviral and immune regulators. In contrast, 50% of the genes that changed during early pregnancy were not regulated by IFNT and were associated with cellular proliferation and extracellular matrix organization. The remaining 19% of genes were not conclusively identified as either IFNT regulated or non-regulated. This suggests that the temporal changes in the CL during early pregnancy are only partially regulated by IFNT, drawing into question identities of other luteal regulators or the effect of age of CL.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":""},"PeriodicalIF":3.1,"publicationDate":"2025-03-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143583800","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}