Yuan WANG, Dai TSUKIOKA, Shoji ODA, Hiroshi MITANI, Fugaku AOKI
{"title":"DNA repair is efficient in irradiated M phase zygotes","authors":"Yuan WANG, Dai TSUKIOKA, Shoji ODA, Hiroshi MITANI, Fugaku AOKI","doi":"10.1262/jrd.2024-018","DOIUrl":"https://doi.org/10.1262/jrd.2024-018","url":null,"abstract":"</p><p>In somatic cells, DNA repair is attenuated during mitosis to prevent the formation of anaphase bridges and facilitate the proper segregation of sister chromatids. Irradiation-induced γH2AX foci persist for hours in M phase somatic cells. However, we observed that anaphase bridges formed in a significant fraction of mouse zygotes irradiated during mitosis. Additionally, γH2AX signals in M phase zygotes peaked 30 min after irradiation and subsequently reduced with a half-life within 1–2 h. These results suggest that the DNA repair system may operate efficiently in M phase zygotes following irradiation, leading to the frequent formation of anaphase bridges. The absence of H2AX promoted the successful segregation of sister chromatids and enhanced the development of embryos to the blastocyst stage. The DNA repair system may be differentially regulated during the M phase of the first cell cycle to ensure the immediate elimination of damaged zygotes, thereby efficiently preventing transmission of mutations to subsequent generations.</p>\u0000<p></p>\u0000<img alt=\"\" src=\"https://www.jstage.jst.go.jp/pub/jrd/advpub/0/advpub_2024-018/figure/advpub_2024-018.jpg\"/>\u0000Graphical Abstract <span style=\"padding-left:5px;\">Fullsize Image</span>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140623500","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Physiological high temperatures alter the amino acid metabolism of bovine early antral follicles","authors":"Kohei KAWANO, Kenichiro SAKAGUCHI, Nattapong NINPETCH, Yojiro YANAGAWA, Seiji KATAGIRI","doi":"10.1262/jrd.2023-096","DOIUrl":"https://doi.org/10.1262/jrd.2023-096","url":null,"abstract":"</p><p>Heat stress reduces the developmental competence of bovine oocytes during the growth phase; however, the detailed mechanisms remain unclear. Amino acids play various critical roles in follicular development, including protein synthesis and as energy sources. We performed <i>in vitro</i> growth (IVG) culture of oocyte–cumulus–granulosa complexes (OCGCs) to assess the amino acid metabolism of small follicles at high temperatures. We isolated OCGCs from early antral follicles (0.5–1.0 mm) and subjected them to IVG culture for 12 days. OCGCs in the heat shock group were cultured under a temperature cycle of (38.5°C: 5 h, 39.5°C: 5 h, 40.5°C: 5 h, and 39.5°C: 9 h) to reproduce the body temperature of lactating cows under a hot environment. OCGCs in the control group were cultured at a constant temperature of 38.5°C for 24 h. Of the surviving OCGCs, those showing similar morphology and size between the groups were selected for amino acid analysis. We analyzed the free amino acids and their metabolites in the culture medium and calculated the depletion or appearance of molecular species. The depletion of three essential amino acids (isoleucine, leucine, and valine), two non-essential amino acids (aspartic acid and glycine), and ornithine was higher in the heat shock group (P < 0.05). Alanine depletion was lower in the heat shock group (P < 0.05). We concluded that heat exposure alters the amino acid metabolism of OCGCs isolated from early antral follicles, which might be involved with the diminished developmental potential of oocytes during summer. </p>\u0000<p></p>\u0000<img alt=\"\" src=\"https://www.jstage.jst.go.jp/pub/jrd/advpub/0/advpub_2023-096/figure/advpub_2023-096.png\"/>\u0000Graphical Abstract <span style=\"padding-left:5px;\">Fullsize Image</span>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140611406","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Minami W. OKUYAMA, Masaharu MORIYOSHI, Seiji KATAGIRI
{"title":"Changes in interleukin-2, -4, -6 and -8 expression in the postovulatory sow endometrium after artificial insemination based on conceived or failed to conceive","authors":"Minami W. OKUYAMA, Masaharu MORIYOSHI, Seiji KATAGIRI","doi":"10.1262/jrd.2023-094","DOIUrl":"https://doi.org/10.1262/jrd.2023-094","url":null,"abstract":"</p><p>The establishment and maintenance of a pregnancy requires proper interaction between the endocrine and immune systems in the uterus. Therefore, it is crucial to understand how changes in endometrial cytokine levels facilitate reproduction. This study aimed to investigate how representative cytokines sequentially changed in the endometrium and whether conception could be attributed to these changes. In this study, artificial insemination was performed twice in 160 sows and ovulation was examined every 3 h using transrectal ultrasonography. Uterine endometrial tissues were obtained via repeated biopsies at 2, 4, 6, 8, 12, 16, and 20 h after ovulation and interleukin (IL)-2, IL-4, IL-6, and IL-8 expression was examined using real-time polymerase chain reaction. The conception rate was 91.9%. The IL-2 levels showed no differences in conception or time. The expression peaks of IL-4 and IL-6 were delayed in sows that failed to conceive within 4–6 h and 2 h, respectively, compared to those that did conceive. In sows that conceived, IL-8 was highest after 2 h, and no difference was observed at other time point, regardless of conception. In sows that failed to conceive, the increase in IL-8 levels might have been cancelled or terminated before the first sampling time. These results highlight the importance of timely increases and subsequent declines in the levels of some cytokines for the establishment of pregnancy. Differences in uterine capacity start just after ovulation; detection and correction of these deviations can improve the reproductive efficiency of sows.</p>\u0000<p></p>\u0000<img alt=\"\" src=\"https://www.jstage.jst.go.jp/pub/jrd/advpub/0/advpub_2023-094/figure/advpub_2023-094.png\"/>\u0000Graphical Abstract <span style=\"padding-left:5px;\">Fullsize Image</span>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140588986","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Progesterone and estradiol regulate sperm hyperactivation and in vitro fertilization success in mice.","authors":"Miyu Fujikura, Masakatsu Fujinoki","doi":"10.1262/jrd.2023-080","DOIUrl":"10.1262/jrd.2023-080","url":null,"abstract":"<p><p>Progesterone (P) and 17β-estradiol (Eβ) form the well-known hormone pair that regulates sperm capacitation. Here, we examined the regulatory effects of P and Eβ on sperm hyperactivation in mice and evaluated the in vitro fertilization (IVF) success. Although P enhanced hyperactivation, Eβ dose-dependently suppressed the P-enhanced hyperactivation. Moreover, P increased IVF success, whereas Eβ suppressed the P-induced increase in IVF success in a dose-dependent manner. Thus, P and Eβ competitively regulate hyperactivation and IVF success in mice. Since P and Eβ concentrations generally change during the estrous cycle, sperm are speculated to capacitate in response to the oviductal environment and fertilize the oocyte.</p>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11017098/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139723087","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nao Aburada, Jun Ito, Yuki Inoue, Taiyo Yamamoto, Masamune Hayashi, Noko Teramoto, Yuri Okada, Yuichi Koshiishi, Koumei Shirasuna, Hisataka Iwata
{"title":"Effect of paternal aging and vitrification on mitochondrial DNA copy number and telomere length of mouse blastocysts.","authors":"Nao Aburada, Jun Ito, Yuki Inoue, Taiyo Yamamoto, Masamune Hayashi, Noko Teramoto, Yuri Okada, Yuichi Koshiishi, Koumei Shirasuna, Hisataka Iwata","doi":"10.1262/jrd.2023-079","DOIUrl":"10.1262/jrd.2023-079","url":null,"abstract":"<p><p>In this study, we examined the effects of paternal aging on the mitochondrial DNA copy number (mt-cn), telomere length (TL), and gene expression in mouse embryos. The effects of vitrification on the mt-cn and TL of the embryos derived from young and aged male parents (YF and AF, respectively) were examined. C57BL/6N male mice were used for embryo production at 13-23 and 50-55 weeks of age. Two-cell stage embryos were collected from the oviducts of superovulated female mice (8-15 weeks old) and cultured for 24 h until the 8-cell stage, followed by embryo vitrification. Fresh and vitrified-warmed embryos were incubated for 2 days until the blastocyst stage, and mt-cn and TL were investigated. The cell-free mitochondrial DNA copy number (cf-mt-cn) in the spent culture medium (SCM) of the embryos was then investigated. RNA sequencing of blastocysts revealed that metabolic pathways, including oxidative phosphorylation and mTOR pathways, were enriched in differentially expressed genes. The mt-cn and TL of AF-derived blastocysts were lower and shorter, respectively, than those of YF-derived blastocysts. Paternal aging did not affect the blastocyst rate after vitrification. Vitrification of the 8-cell stage embryos did not affect the mt-cn of the blastocysts. However, it increased the cf-mt-cn (cell-free mt-cn) in the SCM of both YF- and AF-derived embryos. Vitrification did not affect the TL of either YF- or AF-derived embryos. Thus, paternal aging affected the mt-cn and TL of the embryos, but vitrification did not affect these parameters in either age groups.</p>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11017102/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139546785","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Busulfan administration replicated the characteristics of the epididymal initial segment observed in mice lacking testis-epididymis lumicrine signaling.","authors":"Daiji Kiyozumi","doi":"10.1262/jrd.2023-102","DOIUrl":"10.1262/jrd.2023-102","url":null,"abstract":"<p><p>The physiological functions of the mammalian epididymis are typically regulated by the testes. In addition to sex steroids secreted by testicular Leydig cells, which act on the epididymis in an endocrine manner, there is a non-sex-steroidal signaling pathway known as the lumicrine pathway. This lumicrine signaling pathway involves ligand proteins secreted from germ cells within the testicular seminiferous tubules traversing the male reproductive tract, which induce epithelial differentiation in the epididymis. These findings prompted an inquiry into whether treatments influencing testis physiology can disrupt epididymal function by interfering with testis-epididymis communication. Busulfan, an alkylating agent commonly used to deplete testicular germ cells in reproductive biology, has not been sufficiently explored because of its effects on the epididymis. This study investigated the effects of busulfan administration on the proximal epididymis using histological and transcriptomic analyses. Notably, busulfan, as opposed to the vehicle dimethyl sulfoxide (DMSO), altered the morphology of the initial segment of the epididymis, leading to a reduction in the cell height of the luminal epithelium. RNA sequencing identified 185 significantly downregulated genes in the proximal epididymis of busulfan-administered mice compared to DMSO-administered mice. Comparative transcriptome analyses revealed similarities between the epididymal transcriptome of busulfan-administered mice and lumicrine-deficient mice, such as efferent-duct-ligated W/Wv and Nell2<sup>-/-</sup> mice. However, this differed from that of bilaterally orchidectomized mice, in which both the endocrine and lumicrine signaling pathways were simultaneously ablated. Collectively, these results suggested that the harmful effects of busulfan on the proximal epididymis are secondary consequences of the ablation of testis-epididymis lumicrine signaling.</p>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11017096/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139723085","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Efficient derivation of embryonic stem cells and primordial germ cell-like cells in cattle.","authors":"Atsushi Shirasawa, Masafumi Hayashi, Mayumi Shono, Atsushi Ideta, Takashi Yoshino, Katsuhiko Hayashi","doi":"10.1262/jrd.2023-087","DOIUrl":"10.1262/jrd.2023-087","url":null,"abstract":"<p><p>The induction of the germ cell lineage from pluripotent stem cells (in vitro gametogenesis) will help understand the mechanisms underlying germ cell differentiation and provide an alternative source of gametes for reproduction. This technology is especially important for cattle, which are among the most important livestock species for milk and meat production. Here, we developed a new method for robust induction of primordial germ cell-like cells (PGCLCs) from newly established bovine embryonic stem (bES) cells. First, we refined the pluripotent culture conditions for pre-implantation embryos and ES cells. Inhibition of RHO increased the number of epiblast cells in the pre-implantation embryos and dramatically improved the efficiency of ES cell establishment. We then determined suitable culture conditions for PGCLC differentiation using bES cells harboring BLIMP1-tdTomato and TFAP2C-mNeonGreen (BTTN) reporter constructs. After a 24-h culture with bone morphogenetic protein 4 (BMP4), followed by three-dimensional culture with BMP4 and a chemical agonist and WNT signaling chemical antagonist, bES cells became positive for the reporters. A set of primordial germ cells (PGC) marker genes, including PRDM1/BLIMP1, TFAP2C, SOX17, and NANOS3, were expressed in BTTN-positive cells. These bovine PGCLCs (bPGCLCs) were isolated as KIT/CD117-positive and CD44-negative cell populations. We anticipate that this method for the efficient establishment of bES cells and induction of PGCLCs will be useful for stem cell-based reproductive technologies in cattle.</p>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11017101/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139735395","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Parallel expression patterns of NR4A nuclear receptor family genes in the pituitary gland of proestrus rats.","authors":"Ryota Terashima, Daiki Nagao, Masato Ikeo, Keisuke Morioka, Titaree Laoharatchatathanin, Shiro Kurusu, Mitsumori Kawaminami","doi":"10.1262/jrd.2023-090","DOIUrl":"10.1262/jrd.2023-090","url":null,"abstract":"<p><p>The NR4A nuclear receptor family (NR4As), encompassing NR4A1, NR4A2, and NR4A3, exerts pivotal roles in cellular processes through intricate expression patterns and interactions. Despite the influence of some NR4As on anterior pituitary functions regulated by the hypothalamus, their physiological expression patterns remain unclear. In our prior work, we demonstrated the specific upregulation of NR4A3 in the rat anterior pituitary gland during the proestrus afternoon, coinciding with a gonadotropin surge. In this study, we investigated changes in pituitary Nr4a gene expression throughout the estrous cycle in rats and a gonadotropin surge-induced model. Nr4a1 and Nr4a2 gene expression significantly increased during proestrus, aligning with previous observations for Nr4a3. Furthermore, prolactin gene expression increased sequentially with rising Nr4a gene expression, while thyroid-stimulating hormone beta gene expression remained stable. Immunohistochemistry revealed a widespread and differential distribution of NR4A proteins in the anterior pituitary, with NR4A1 and NR4A3 being particularly abundant in thyrotrophs, and NR4A2 in gonadotrophs. In estrogen-treated ovariectomized rats, elevated luteinizing hormone secretion corresponded to markedly upregulated expression of Nr4a1, Nr4a2, and Nr4a3. In gonadotroph and somatomammotroph cell lines, gonadotropin- and thyrotropin-releasing hormones transiently and dose-dependently increased the expression of Nr4a genes. These findings suggest that hypothalamic hormone secretion during proestrus may induce the parallel expression of pituitary Nr4a genes, potentially influencing the pituitary gene expression program related to endocrine functions before and after ovulation.</p>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11017097/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139723086","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Effect of globin peptide on female fertility in aging granulosa cell-specific Nrg1 knockout mice","authors":"Takashi UMEHARA, Marino OGASAHARA, D.M.V. Supun PREMARATHNE, Yuka SASAKAWA, Yasuo SUMIDA, Masayuki SHIMADA","doi":"10.1262/jrd.2023-076","DOIUrl":"https://doi.org/10.1262/jrd.2023-076","url":null,"abstract":"</p><p>Ovarian fibrosis contributes to age-related ovarian dysfunction. In our previous study, we observed ovarian fibrosis in both obese and aging mice with intracellular lipid droplets in the fibrotic ovaries. Although the importance of mitochondria in ovarian fibrosis has been recognized in pharmacological studies, their role in lipid metabolism remains unclear. Globin peptide (GP), derived from hemoglobin, enhances lipid metabolism in obese mice. This study aimed to elucidate the importance of lipid metabolism in ovarian fibrosis by using GP. Treatment of ovarian stromal cells with GP increased mitochondrial oxygen consumption during β-oxidation. Lipid accumulation was also observed in the ovaries of granulosa cell-specific <i>Nrg1</i> knockout mice (gc<i>Nrg1</i>KO), and the administration of GP to gc<i>Nrg1</i>KO mice for two months reduced ovarian lipid accumulation and fibrosis in addition to restoring the estrous cycle. GP holds promise for mitigating lipid-related ovarian issues and provides a novel approach to safeguarding ovarian health by regulating fibrosis via lipid pathways.</p>\u0000<p></p>\u0000<img alt=\"\" src=\"https://www.jstage.jst.go.jp/pub/jrd/advpub/0/advpub_2023-076/figure/advpub_2023-076.jpg\"/>\u0000Graphical Abstract <span style=\"padding-left:5px;\">Fullsize Image</span>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-03-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140105679","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Chromatin structure in totipotent mouse early preimplantation embryos","authors":"Masatoshi OOGA","doi":"10.1262/jrd.2023-106","DOIUrl":"https://doi.org/10.1262/jrd.2023-106","url":null,"abstract":"</p><p>Totipotency refers to the ability of a single cell to give rise to all the different cell types in the body. Terminally differentiated germ cells (spermatozoa and oocytes) undergo reprogramming, which results in the acquisition of totipotency in zygotes. Since the 1990s, numerous studies have focused on the mechanisms of totipotency. With the emergence of the concept of epigenetic reprogramming, which is important for the undifferentiated and differentiated states of cells, the epigenomes of germ cells and fertilized eggs have been thoroughly analyzed. However, in early immunostaining studies, detailed epigenomic information was difficult to obtain. In recent years, the explosive development of next-generation sequencing has made it possible to acquire genome-wide information and the rise of genome editing has facilitated the analysis of knockout mice, which was previously difficult. In addition, live imaging can effectively analyze zygotes and 2-cell embryos, for which the number of samples is limited, and provides biological insights that cannot be obtained by other methods. In this review, the progress of our research using these advanced techniques is traced back from the present to its earliest years.</p>\u0000<p></p>\u0000<img alt=\"\" src=\"https://www.jstage.jst.go.jp/pub/jrd/advpub/0/advpub_2023-106/figure/advpub_2023-106.png\"/>\u0000Graphical Abstract <span style=\"padding-left:5px;\">Fullsize Image</span>","PeriodicalId":16942,"journal":{"name":"Journal of Reproduction and Development","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2024-03-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140056941","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}