Biology of Reproduction最新文献

{"title":"Effect of gestational age and fetal sex on metabolism of creatine by uteri, placentae, and fetuses of pigs†.","authors":"Nirvay Sah, Claire Stenhouse, Katherine M Halloran, Robyn M Moses, Makenzie G Newton, Heewon Seo, Joe W Cain, Carli M Lefevre, Gregory A Johnson, Guoyao Wu, Fuller W Bazer","doi":"10.1093/biolre/ioaf015","DOIUrl":"10.1093/biolre/ioaf015","url":null,"abstract":"<p><p>The creatine (Cr) biosynthesis pathway buffers adenosine triphosphate in metabolically active tissues. We investigated whether sex of fetus and day of gestation influence Cr in endometrial and conceptus tissues from gilts on days 60 and 90 (n = 6 gilts/day) of gestation. Uterine and conceptus tissues associated with one male and one female fetus from each gilt were analyzed for creatine, messenger RNAs (mRNAs), and proteins for Cr biosynthesis. Total Cr decreased in amniotic fluid but increased in allantoic fluid between days 60 and 90 of gestation for male (P < 0.05) but not for female fetuses (P > 0.05). Endometrial expression of creatine kinase, muscle (CKM), creatine kinase mitochondrial type 1 (CKMT1), and solute carrier family 6, member 8 (SLC6A8) mRNAs increased (P < 0.05) between days 60 and 90 only for female fetuses. On day 60, expression of creatine kinase, brain (CKB) and CKMT1 mRNAs was greater (P < 0.05) for placentae of female than male fetuses. Livers of male fetuses had greater expression of arginine:glycine amidinotransferase (AGAT) and CKB than for females on day 60, while kidneys of female fetuses had greater expression of guanidinoacetate-N-methyltransferase (GAMT) than male fetuses on day 90 (P < 0.05). Localization of GAMT, CKB, CKMT1, and SLC6A8 proteins to uterine and chorionic epithelium was not influenced by gestational age or fetal sex. Arginine-glycine amidinotransferase localized to fetal kidneys and appeared greater on day 90 than on day 60 in both sexes. Thus, expression of the creatine-creatine kinase-phosphocreatine system at the uterine-conceptus interface is affected by gestational age and fetal sex to influence energy homeostasis in pigs.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"728-742"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142999561","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":"Effect of introducing somatic mitochondria into an early embryo on zygotic gene activation†.","authors":"Yoshihiro Hayashi, Hanako Bai, Masashi Takahashi, Tomohiro Mitani, Manabu Kawahara","doi":"10.1093/biolre/ioaf010","DOIUrl":"10.1093/biolre/ioaf010","url":null,"abstract":"<p><p>Unlike differentiated somatic cells, which possess elongated mitochondria, undifferentiated cells, such as those of preimplantation embryos, possess round, immature mitochondria. Mitochondrial morphology changes dynamically during cell differentiation in a process called mitochondrial maturation. The significance of the alignment between cell differentiation and mitochondrial maturity in preimplantation development remains unclear. In this study, we analyzed mouse embryos into which liver-derived somatic mitochondria were introduced (SM-embryos). Most SM-embryos were arrested at the two-cell stage. Some of the introduced somatic mitochondria became round, while others remained elongated and large. RNA-sequencing revealed a disruption of both minor and major zygotic gene activation (ZGA) in SM-embryos. Minor ZGA did not terminate before major ZGA, and the onset of major ZGA was inhibited, as shown by histone modification analyses of histone H3 lysine 4 trimethylation and histone H3 lysine 27 acetylation. Further analysis of metabolites involved in histone modification regulation in SM-embryos showed a significantly lower NAD+/NADH ratio in SM-embryos than in control embryos. Additionally, the mitochondrial membrane potential, an indicator of mitochondrial function, was lower in SM-embryos than in control embryos. Our results demonstrated that introducing somatic mitochondria into an embryo induces mitochondrial dysfunction, thereby disrupting metabolite production, leading to a disruption in ZGA and inducing developmental arrest. Our findings reveal that the alignment between cell differentiation and mitochondrial maturity is essential for early embryonic development.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"614-627"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142982595","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":"Anti-Müllerian hormone concentration measured before gonadotropin stimulation is associated with quality of subsequent ovarian response in the cheetah (Acinonyx jubatus) and domestic cat (Felis catus)†.","authors":"Rhasaan T M Bovell, Pierre Comizzoli, Jennifer B Nagashima, Jenny Santiestevan, Adrienne E Crosier, Ned J Place","doi":"10.1093/biolre/ioaf025","DOIUrl":"10.1093/biolre/ioaf025","url":null,"abstract":"<p><p>Relationships between anti-Müllerian hormone concentrations and subsequent ovarian stimulation outcomes have been demonstrated in several mammalian species, but comprehensive reports are lacking in felids. Our objective was to characterize relationships between anti-Müllerian hormone concentrations and responses to exogenous gonadotropin stimulation in cheetahs and domestic cats. Blood samples collected before stimulation were used to measure serum anti-Müllerian hormone concentrations, which were compared to post-stimulation outcomes, including counts of retrievable oocytes or ovulation sites, oocyte quality, embryonic cleavage after in vitro fertilization, and progestogen concentrations. Anti-Müllerian hormone concentrations were also compared to outcomes in domestic cats induced to ovulate by mechanical stimulation of the vagina and cervix (simulated coitus). Greater anti-Müllerian hormone concentrations were associated with greater ovulatory response, progestogen production, and embryonic cleavage success among gonadotropin-treated cheetahs, and with greater ovulatory response among gonadotropin-treated domestic cats. Associations were moderated by age, with anti-Müllerian hormone concentration generally a greater determinant of these outcomes in older animals. Anti-Müllerian hormone concentrations alone could distinguish domestic cats with high and low ovulatory responses to exogenous hormones. However, this marker was unrelated to ovulatory response in domestic cats after simulated coitus. These results demonstrate the potential for anti-Müllerian hormone concentrations to predict responses of cheetahs and domestic cats to ovarian stimulation treatment commonly used in assisted reproductive technologies. Associations between anti-Müllerian hormone concentrations and ovarian stimulation outcomes in these species might reflect relationships between anti-Müllerian hormone concentration and antral follicle count or oocyte/embryo cellular function, as reported in other mammals; however, this remains to be tested.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"754-766"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143187995","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":"Collagen turnover during cervical remodeling involves both intracellular and extracellular collagen degradation pathways†.","authors":"Mariano Colon-Caraballo, Serena R Russell, Kristin M Myers, Mala Mahendroo","doi":"10.1093/biolre/ioaf012","DOIUrl":"10.1093/biolre/ioaf012","url":null,"abstract":"<p><p>Reproductive success requires accurately timed remodeling of the cervix to orchestrate the maintenance of pregnancy, the process of labor, and birth. Prior work in mice established that a combination of continuous turnover of fibrillar collagen and reduced formation of collagen cross-links allows for the gradual increase in tissue compliance and delivery of the fetus during labor. However, the mechanism for continuous collagen degradation to ensure turnover during cervical remodeling is still unknown. This study demonstrates the functional role of extracellular and intracellular collagen degradative pathways in two different settings of cervical remodeling: physiological term remodeling and inflammation-mediated premature remodeling. Extracellular collagen degradation is achieved by the activity of fibroblast-derived matrix metalloproteases MMP14, MMP2, and fibroblast activation protein (FAP). In parallel, we demonstrate the function of an intracellular collagen degradative pathway in fibroblast cells mediated by the collagen endocytic mannose receptor type-2 (MRC2). These pathways appear to be functionally redundant as loss of MRC2 does not obstruct collagen turnover or cervical function in pregnancy. While both extracellular and intracellular pathways are also utilized in inflammation-mediated premature cervical remodeling, the extracellular collagen degradation pathway uniquely employs fibroblast and immune-cell-derived proteases. In sum, these findings identify the dual utilization of two distinct degradative pathways as a failsafe mechanism to achieve continuous collagen turnover in the cervix, thereby allowing dynamic shifts in cervical tissue mechanics and function.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"709-727"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11996760/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142999560","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":"Roles of the EF-hand domain of PLCZ1 in establishing species-specific Ca2+ oscillations in mouse and rat fertilization†.","authors":"Hoi Chang Lee, Hiroki Akizawa, Rafael A Fissore","doi":"10.1093/biolre/ioaf021","DOIUrl":"10.1093/biolre/ioaf021","url":null,"abstract":"<p><p>Periodic increases in cytosolic calcium concentration (Ca2+ oscillations) during mammalian fertilization induce all the events collectively known as egg activation. The sperm-specific phospholipase C, Phospholipase C zeta 1 (PLCZ1) represents the \"sperm factor\" vital for initiating the persistent Ca2+ oscillations in mammals. Despite sequence conservation, the Ca2+ oscillation-inducing properties of the enzyme differ vastly among species, and this is particularly salient between mouse and rat PLCZ1, where the activities vary at least one order of magnitude in favor of the former. As previously shown, injecting wild-type rat Plcz1 mRNA into metaphase II mouse eggs induced delayed Ca2+ oscillations with low specific activity compared to the homologous mouse Plcz1 mRNA. We, therefore, sought to uncover the factor(s) diversifying these enzymes by swapping functional domains between species, creating chimeric PLCZ1s. When injected into mouse metaphase II eggs, mouse Plcz1 mRNA with the whole- or part of the EF-hand domains swapped with the rat showed a substantial reduction in activity compared to WT. Consistently, the opposite exchange enhanced the rat's enzyme activity. EF-hand domains 1 and 2 seemed to underlie most differences, and mutations of the divergent amino acids within these domains, substitutions for Glu(m-30; r-29) and Gln(m-58; r-57), changed the activity of both species' PLCZ1s in opposite directions. Collectively, our findings support the view that differences in the sequences of EF-hand domains, especially in several of its charged residues, underpin the distinct PLCZ1 activities between these species, revealing the gametes and species' adaptability to optimize the fertilization signal and early development.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"663-674"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143073663","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":"Region-specific roles of oviductal motile cilia in oocyte/embryo transport and fertility†.","authors":"Deirdre M Scully, Tian Xia, Guzel R Musina, Michaela A McCown, Kohei Umezu, Bonnie K Kircher, Richard R Behringer, Irina V Larina","doi":"10.1093/biolre/ioaf005","DOIUrl":"10.1093/biolre/ioaf005","url":null,"abstract":"<p><p>The physiological and clinical importance of motile cilia in reproduction is well recognized; however, the specific role they play in transport through the oviduct and how ciliopathies lead to subfertility and infertility are still unclear. The contribution of cilia beating, fluid flow, and smooth muscle contraction to overall progressive transport within the oviduct remains under debate. Therefore, we investigated the role of cilia in the oviduct transport of preimplantation eggs/embryos using a combination of genetic and advanced imaging approaches. We show that the region of the oviduct where cumulus-oocyte complex circling occurs, around the time of fertilization, is correlated with asymmetrical mucosal fold arrangement and non-radially distributed ciliated epithelium. Our results suggest that motile cilia, as well as mucosal fold asymmetry, may contribute to the local flow fields that help steer luminal contents away from the epithelial walls. We also present, in vivo, volumetric evidence of delayed egg transport in a genetic mouse model with disrupted motile cilia function in the female reproductive system. Females with Dnah5 deleted in the oviduct epithelium are subfertile and demonstrate disrupted motile cilia activity within the oviduct mucosa. Fifty percent of Dnah5 mutant females have delayed egg transport where cumulus-oocyte complexes did not progress to the ampulla at the expected time point and remained within the ovarian bursa. The integration of advanced imaging with genetic dysfunction of motile cilia provides valuable insights into oviductal transport. Potentially, these data could be valuable for better understanding and management of tubal pathologies and human infertility.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"651-662"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11996758/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143728354","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":"Deletion of an evolutionarily conserved TAD boundary impacts spermatogenesis in mice†.","authors":"Ana C Lima, Mariam Okhovat, Alexandra M Stendahl, Ran Yang, Jake VanCampen, Kimberly A Nevonen, Jarod Herrera, Weiyu Li, Lana Harshman, Lev M Fedorov, Katinka A Vigh-Conrad, Nadav Ahituv, Donald F Conrad, Lucia Carbone","doi":"10.1093/biolre/ioaf017","DOIUrl":"10.1093/biolre/ioaf017","url":null,"abstract":"<p><p>Spermatogenesis is a complex process that can be disrupted by genetic and epigenetic changes, potentially leading to male infertility. Recent research has rapidly increased the number of coding mutations causally linked to impaired spermatogenesis in humans and mice. However, the role of noncoding mutations remains largely unexplored. To evaluate the effects of noncoding mutations on spermatogenesis, we first identified an evolutionarily conserved topologically associated domain boundary near two genes with important roles in mammalian testis function: Dmrtb1 and Lrp8. We then used CRISPR-Cas9 to generate a mouse line where 26 kb of the boundary was removed including a strong and evolutionarily conserved CTCF binding site. ChIP-seq and Hi-C experiments confirmed the removal of the CTCF site and a resulting mild increase in the DNA-DNA interactions across the domain boundary. Mutant mice displayed significant changes in testis gene expression, a higher frequency of histological abnormalities, a drop of 47-52% in efficiency of meiosis, a 15-18% reduction in efficiency of spermatogenesis, and, consistently, a 12-28% decrease in daily sperm production compared to littermate controls. Despite these quantitative changes in testis function, mutant mice show no significant changes in fertility. This suggests that noncoding deletions affecting testis gene regulation may have smaller effects on fertility compared to coding mutations of the same genes. Our results demonstrate that disruption of a topologically associated domain boundary can have a negative impact on sperm production and highlight the importance of considering noncoding mutations in the analysis of patients with male infertility.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"767-779"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11996757/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143187996","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":"Correction to: Digital analysis of ovarian tissue: generating a standardized method of follicle analysis.","authors":"","doi":"10.1093/biolre/ioaf039","DOIUrl":"10.1093/biolre/ioaf039","url":null,"abstract":"","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"782"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11996755/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143555807","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":"Acute and long-term transcriptomic responses of granulosa cells to obesogenic diet and concomitant effects on oocyte quality: insight from an outbred mouse model†.","authors":"Waleed F A Marei, Kerlijne Moorkens, Yannick Gansemans, Filip Van Nieuwerburgh, Jo L M R Leroy","doi":"10.1093/biolre/ioaf027","DOIUrl":"10.1093/biolre/ioaf027","url":null,"abstract":"<p><p>Diet-induced obesity can cause long-term alterations in ovarian functions, but the acute effects of obesogenic diets on the follicular cells and their progression over time, when intake is continued and obesity develops, remain unclear. We aimed to determine the onset and progression of changes in the granulosa cell transcriptomic profile after starting a high-fat/high sugar (HFHS)-diet feeding in mice. We also examined the changes in oocyte lipid droplet content and mitochondrial ultrastructural abnormalities. Swiss (outbred) mice were sacrificed at 24 h, 3 days, and at 1, 4, 8, 12, and 16 weeks of feeding HFHS and control diets. Lipid droplet content significantly increased in the HFHS oocytes within 24 h compared to controls (P < 0.05). Oocyte mitochondrial abnormalities only increased starting from 8 weeks. Granulosa RNA-seq revealed altered transcriptomic gene-set enrichments (GO terms and KEGG pathways, Padj < 0.05) already at 3 days and 1 week indicating acute endoplasmic reticulum unfolded protein responses, with concomitant fluctuations in several cellular metabolic pathways and gene sets related to mitochondrial bioenergetic functions, some of which persisted after 8 weeks. Interestingly, the short- and long-term patterns of changes in cytochrome P450, steroid hormone biosynthesis, retinol metabolism, bile acid metabolism, fatty acid metabolism, and Pi3K/Akt signaling pathways were most prominent and highly correlated; all being acutely upregulated, then chronically downregulated. These results show that the impact of obesogenic diet on the oocyte and granulosa cells is prompt, while the response depends on the duration of feeding and occurs in a multiphasic cascade together with a progressive deterioration in oocyte quality.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"692-708"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143363554","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":"Developmental proteome dynamics in granulosa and thecal layers from growing follicles to pre-ovulatory duck follicles†.","authors":"Weiguang Xia, Chenglong Jin, Shuang Wang, Yanan Zhang, Kaichao Li, Xuebing Huang, Chuntian Zheng, Wei Chen","doi":"10.1093/biolre/ioaf026","DOIUrl":"10.1093/biolre/ioaf026","url":null,"abstract":"<p><p>Granulosa and thecal layer cells play important roles in the post-hatching follicular growth in laying birds. To examine the biochemical processes of granulosa and thecal layers associated with follicular growth, the technique of data independent acquisition was used in this study to explore protein profiling in granulosa and thecal layers from growing follicles in laying ducks. We identified and quantitatively analyzed 8032 proteins in granulosa cells and 9552 proteins in thecal layer cells. Hierarchical clustering of the resulting profiles revealed differential changes of expression of proteins linked to cell metabolism, signaling, cell junction, especially in steroid synthesis, peroxisome proliferator-activated receptor, and gap junction signaling pathway at different stages of follicles. The highest expression of proteins related to gap junction and peroxisome proliferator-activated receptor signaling pathway occurred in granulosa cells of 3-6 mm or 6-8 mm follicles. In granulosa cells, decreases in the enzymes that catalyze the transformation of estrone into estradiol and proteins related to calcium transport and apoptosis occurred during follicular growth. As follicles grew, proteins related to androgens biosynthesis and involved in gap junction and peroxisome proliferator-activated receptor signaling pathway decreased in the thecal layer cells. Three main group functional clusters extracted from the protein-protein interaction network, were mainly responsible for apoptosis, steroid hormone biosynthesis, and the peroxisome proliferator-activated receptor signaling pathway. These proteomic data provide a holistic framework for understanding how diverse biochemical processes in granulosa cells and thecal layer cells are coordinated at the cellular level during follicular growth in laying birds.</p>","PeriodicalId":8965,"journal":{"name":"Biology of Reproduction","volume":" ","pages":"675-691"},"PeriodicalIF":3.1,"publicationDate":"2025-04-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143187997","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}