Pub Date : 2022-12-01DOI: 10.1007/s10719-022-10085-5
Wei Dan, Cheng Li, Jun Li, Pengfei Li, Miaomiao Xin, Zexuan Chen, Liuyi Dang, Zihao Yu, Jing Li, Jiechen Shen, Liangshuo Hu, Shisheng Sun
Intrahepatic cholangiocarcinoma (ICC) is the second major subtype of primary liver cancer and has caused more and more attention with increasing incidence and mortality worldwide. Our previous study found that bisecting N-glycans are commonly increased in ICC, while the effects and potential functions of bisecting GlcNAc in ICC are still largely unclear. In this study, we further confirmed that the structures of bisecting GlcNAc were significantly up-regulated in ICC compared with paracancer tissues by glycoproteomic data and lectin histochemistry. The expression of its glycosyltransferase MGAT3 was also up-regulated in ICC tissues at both mRNA and protein levels, and expression of MGAT3 is negatively correlated with overall survival explored by bioinformatic analyses and published datasets from 255 patients. Next, the silencing of MGAT3 could inhibit the growth and invasion of ICC cells, and overexpressing of MGAT3 only promoted ICC cell invasion. Further glycoproteomic analysis showed that the commonly glycoproteins modified by bisecting GlcNAc after MGAT3-overexpression in two ICC cell lines were mainly involved in cell movement-related biological processes, such as cell adhesion, integrin-related and ECM-receptor interaction. This study sheds light on the potential effects of bisecting GlcNAc in ICC cells and suggests that MGAT3 might be used as a potential target in the therapy of ICC.
{"title":"Glycoproteomic analysis reveals the effects of bisecting GlcNAc in intrahepatic cholangiocarcinoma.","authors":"Wei Dan, Cheng Li, Jun Li, Pengfei Li, Miaomiao Xin, Zexuan Chen, Liuyi Dang, Zihao Yu, Jing Li, Jiechen Shen, Liangshuo Hu, Shisheng Sun","doi":"10.1007/s10719-022-10085-5","DOIUrl":"https://doi.org/10.1007/s10719-022-10085-5","url":null,"abstract":"<p><p>Intrahepatic cholangiocarcinoma (ICC) is the second major subtype of primary liver cancer and has caused more and more attention with increasing incidence and mortality worldwide. Our previous study found that bisecting N-glycans are commonly increased in ICC, while the effects and potential functions of bisecting GlcNAc in ICC are still largely unclear. In this study, we further confirmed that the structures of bisecting GlcNAc were significantly up-regulated in ICC compared with paracancer tissues by glycoproteomic data and lectin histochemistry. The expression of its glycosyltransferase MGAT3 was also up-regulated in ICC tissues at both mRNA and protein levels, and expression of MGAT3 is negatively correlated with overall survival explored by bioinformatic analyses and published datasets from 255 patients. Next, the silencing of MGAT3 could inhibit the growth and invasion of ICC cells, and overexpressing of MGAT3 only promoted ICC cell invasion. Further glycoproteomic analysis showed that the commonly glycoproteins modified by bisecting GlcNAc after MGAT3-overexpression in two ICC cell lines were mainly involved in cell movement-related biological processes, such as cell adhesion, integrin-related and ECM-receptor interaction. This study sheds light on the potential effects of bisecting GlcNAc in ICC cells and suggests that MGAT3 might be used as a potential target in the therapy of ICC.</p>","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 6","pages":"737-745"},"PeriodicalIF":3.0,"publicationDate":"2022-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10349626","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}
The pH value was essential for the growth and metabolism of microorganisms. Acidic pH exopolysaccharide (AC-EPS) and alkaline pH exopolysaccharide (AL-EPS) secreted by A. australica QD mediated by pH were studied in this paper. The total carbohydrate content and molecular weight of AC-EPS (79.59% ± 2.24% (w/w), 8.374 × 105 Da) and AL-EPS (82.48% ± 1.46% (w/w), 6.182 × 105 Da) were estimated and compared. In AC-EPS, mannose (3.78%) and galactose (3.24%) content was more, while the proportion of glucuronic acid was less in comparison to AL-EPS. The scanning electron microscopy revealed the structural differences among the AC-EPS and AL-EPS. Thermogravimetric analysis showed degradation temperatures of 272.8 °C and 244.9 °C for AC-EPS and AL-EPS, respectively. AC-EPS was found to exhibit better rheological properties and emulsifying capabilities, while AL-EPS had superior antioxidant activities. Overall, both AC-EPS and AL-EPS have the potential to be used as emulsifiers and biological antioxidants.
{"title":"Effect of fermentation pH on the structure, rheological properties, and antioxidant activities of exopolysaccharides produced by Alteromonas australica QD.","authors":"Fengshu Li, Xin Hu, Xiaojun Sun, Haoshuai Li, Jinren Lu, Yiming Li, Mutai Bao","doi":"10.1007/s10719-022-10087-3","DOIUrl":"https://doi.org/10.1007/s10719-022-10087-3","url":null,"abstract":"<p><p>The pH value was essential for the growth and metabolism of microorganisms. Acidic pH exopolysaccharide (AC-EPS) and alkaline pH exopolysaccharide (AL-EPS) secreted by A. australica QD mediated by pH were studied in this paper. The total carbohydrate content and molecular weight of AC-EPS (79.59% ± 2.24% (w/w), 8.374 × 10<sup>5</sup> Da) and AL-EPS (82.48% ± 1.46% (w/w), 6.182 × 10<sup>5</sup> Da) were estimated and compared. In AC-EPS, mannose (3.78%) and galactose (3.24%) content was more, while the proportion of glucuronic acid was less in comparison to AL-EPS. The scanning electron microscopy revealed the structural differences among the AC-EPS and AL-EPS. Thermogravimetric analysis showed degradation temperatures of 272.8 °C and 244.9 °C for AC-EPS and AL-EPS, respectively. AC-EPS was found to exhibit better rheological properties and emulsifying capabilities, while AL-EPS had superior antioxidant activities. Overall, both AC-EPS and AL-EPS have the potential to be used as emulsifiers and biological antioxidants.</p>","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 6","pages":"773-787"},"PeriodicalIF":3.0,"publicationDate":"2022-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10719413","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}
In this study, a water-soluble polysaccharide from Eucommia folium was extracted by hot water and purified using Sephadex G-200 gel columns. The results showed that the purified fraction (EFP) has a molecular weight of 9.98 × 105 Da and consisted of rhamnose, arabinose, galactose, glucose, mannose, xylose, galacturonic acid, and glucuronic acid (molar ratio: 0.226: 1.739: 2.183: 1: 0.155: 0.321: 0.358: 0.047). The combination of infrared spectroscopy and NMR analysis proved that EFP is an acidic polysaccharide whose main chain consists of α-L-Araf-(1 → , → 3,5)-α-Araf-(1 → , → 3)-β-Galp-(1 → , → 3,6)-β-Glcp-(1 → , → 2)-α-D-Manp-(1 → , → 4)-α-GalpA-(1 → , → 2,4)-α-Rhap-(1 → . In addition, the in vivo antitumoral activity of EFP was studied using a H22 tumor-bearing mice model. EFP effectively inhibited tumor growth in mice following intragastric administration. By Combining with the results of the apoptosis assay and JC-1 staining analysis, we confirmed that EFP induces apoptosis through the mitochondrial pathway. Furthermore, cell cycle analysis demonstrated that EFP blocks the cell cycle at S phase.
{"title":"A water-soluble polysaccharide from Eucommia folium: the structural characterization and anti-tumor activity in vivo.","authors":"Zhi-Qian Yan, Su-Yun Ding, Pei Chen, Hui-Ping Liu, Meng-Li Chang, Shu-Yuan Shi","doi":"10.1007/s10719-022-10086-4","DOIUrl":"https://doi.org/10.1007/s10719-022-10086-4","url":null,"abstract":"<p><p>In this study, a water-soluble polysaccharide from Eucommia folium was extracted by hot water and purified using Sephadex G-200 gel columns. The results showed that the purified fraction (EFP) has a molecular weight of 9.98 × 10<sup>5</sup> Da and consisted of rhamnose, arabinose, galactose, glucose, mannose, xylose, galacturonic acid, and glucuronic acid (molar ratio: 0.226: 1.739: 2.183: 1: 0.155: 0.321: 0.358: 0.047). The combination of infrared spectroscopy and NMR analysis proved that EFP is an acidic polysaccharide whose main chain consists of α-L-Araf-(1 → , → 3,5)-α-Araf-(1 → , → 3)-β-Galp-(1 → , → 3,6)-β-Glcp-(1 → , → 2)-α-D-Manp-(1 → , → 4)-α-GalpA-(1 → , → 2,4)-α-Rhap-(1 → . In addition, the in vivo antitumoral activity of EFP was studied using a H22 tumor-bearing mice model. EFP effectively inhibited tumor growth in mice following intragastric administration. By Combining with the results of the apoptosis assay and JC-1 staining analysis, we confirmed that EFP induces apoptosis through the mitochondrial pathway. Furthermore, cell cycle analysis demonstrated that EFP blocks the cell cycle at S phase.</p>","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 6","pages":"759-772"},"PeriodicalIF":3.0,"publicationDate":"2022-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10351406","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}
A simple method was developed for the separation of glycosphingolipids (GSLs) from lipid mixtures, including phospholipids and cholesterol, using zirconium dioxide (zirconia, ZrO2). Although this procedure does not incorporate a mild alkali treatment, which is commonly used for eliminating glycerophospholipids, it can be used to remove both alkali-resistant sphingomyelin and glycerophospholipids possessing ether bonds. Importantly, when GSLs were dissolved in organic solvent together with cholesterol (Chol) and phospholipids, and loaded onto ZrO2, Chol did not bind to the ZrO2 but both the GSLs and phospholipids did. When eluted with 5 mg/mL of 2,5-dihydroxybenzoic acid in methanol, GSLs but not phospholipids were recovered, leaving the phospholipids bound to the ZrO2 particles. This method is particularly applicable for GSLs such as triglycosylceramides, tetraglycosylceramides and some pentaglycosylceramides, sulfatide and GM3 located in the lower phase of a Folch's partition, where significant amounts of phospholipids, Chol and neutral lipids reside along with GSLs. This method was successfully used to easily isolate GSLs from biological materials for their subsequent analysis by matrix-assisted laser desorption ionization time-of-flight mass spectrometry with high resolution.
{"title":"Simple separation of glycosphingolipids in the lower phase of a Folch's partition from crude lipid fractions using zirconium dioxide.","authors":"Hideharu Nagasawa, Shota Miyazaki, Mamoru Kyogashima","doi":"10.1007/s10719-022-10080-w","DOIUrl":"https://doi.org/10.1007/s10719-022-10080-w","url":null,"abstract":"<p><p>A simple method was developed for the separation of glycosphingolipids (GSLs) from lipid mixtures, including phospholipids and cholesterol, using zirconium dioxide (zirconia, ZrO<sub>2</sub>). Although this procedure does not incorporate a mild alkali treatment, which is commonly used for eliminating glycerophospholipids, it can be used to remove both alkali-resistant sphingomyelin and glycerophospholipids possessing ether bonds. Importantly, when GSLs were dissolved in organic solvent together with cholesterol (Chol) and phospholipids, and loaded onto ZrO<sub>2</sub>, Chol did not bind to the ZrO<sub>2</sub> but both the GSLs and phospholipids did. When eluted with 5 mg/mL of 2,5-dihydroxybenzoic acid in methanol, GSLs but not phospholipids were recovered, leaving the phospholipids bound to the ZrO<sub>2</sub> particles. This method is particularly applicable for GSLs such as triglycosylceramides, tetraglycosylceramides and some pentaglycosylceramides, sulfatide and GM3 located in the lower phase of a Folch's partition, where significant amounts of phospholipids, Chol and neutral lipids reside along with GSLs. This method was successfully used to easily isolate GSLs from biological materials for their subsequent analysis by matrix-assisted laser desorption ionization time-of-flight mass spectrometry with high resolution.</p>","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 6","pages":"789-795"},"PeriodicalIF":3.0,"publicationDate":"2022-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10698951","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}
Pub Date : 2022-12-01DOI: 10.1007/s10719-022-10088-2
Wenfeng Liao, Xiaodong Hu, Zhenyun Du, Peipei Wang, Kan Ding
A homogeneous polysaccharide named as LJW2F2 was extracted and purified from the flowers of Lonicera japonica Thunb. Structural characteristic indicated that LJW2F2 was a homogalacturonan composed of α-1,4-D-galacturonic acid with a molecular weight of 7.2 kDa. Previous investigation suggested that homogalacturonan might impede angiogenesis, however the mechanism is still vague. Here we reported that LJW2F2 significantly disrupted capillary-like tube formation of human microvascular endothelia cells (HMEC-1) on matrigel as well as the cells migration. Mechanism study revealed that LJW2F2 might inactivate phosphorylation of epidermal growth factor receptor (EGFR), subsequently suppress Raf, mitogen-activated protein kinase (MEK) and extracellular-related kinase (ERK) phosphorylation. Moreover, LJW2F2 markedly decreased the expression of Notch1 and Delta-like ligand 4 (Dll4). Therefore, our results suggested that LJW2F2 might be a potential angiogenesis inhibitor via disturbing multiple signaling pathways.
从金银花中提取纯化了一种均相多糖LJW2F2。结构特征表明LJW2F2为α-1,4- d -半乳糖醛酸组成的均半乳糖醛酸,分子量为7.2 kDa。以往的研究表明,均半乳糖酸可能阻碍血管生成,但其机制尚不清楚。本研究报道LJW2F2显著破坏基质上人微血管内皮细胞(HMEC-1)的毛细血管样管形成和细胞迁移。机制研究表明,LJW2F2可能使表皮生长因子受体(EGFR)磷酸化失活,进而抑制Raf、丝裂原活化蛋白激酶(MEK)和细胞外相关激酶(ERK)磷酸化。LJW2F2显著降低Notch1和δ样配体4 (Dll4)的表达。因此,我们的研究结果表明LJW2F2可能是一种潜在的血管生成抑制剂,通过干扰多种信号通路。
{"title":"A homogalacturonan from Lonicera japonica Thunb. disrupts angiogenesis via epidermal growth factor receptor and Delta-like 4 associated signaling.","authors":"Wenfeng Liao, Xiaodong Hu, Zhenyun Du, Peipei Wang, Kan Ding","doi":"10.1007/s10719-022-10088-2","DOIUrl":"https://doi.org/10.1007/s10719-022-10088-2","url":null,"abstract":"<p><p>A homogeneous polysaccharide named as LJW2F2 was extracted and purified from the flowers of Lonicera japonica Thunb. Structural characteristic indicated that LJW2F2 was a homogalacturonan composed of α-1,4-D-galacturonic acid with a molecular weight of 7.2 kDa. Previous investigation suggested that homogalacturonan might impede angiogenesis, however the mechanism is still vague. Here we reported that LJW2F2 significantly disrupted capillary-like tube formation of human microvascular endothelia cells (HMEC-1) on matrigel as well as the cells migration. Mechanism study revealed that LJW2F2 might inactivate phosphorylation of epidermal growth factor receptor (EGFR), subsequently suppress Raf, mitogen-activated protein kinase (MEK) and extracellular-related kinase (ERK) phosphorylation. Moreover, LJW2F2 markedly decreased the expression of Notch1 and Delta-like ligand 4 (Dll4). Therefore, our results suggested that LJW2F2 might be a potential angiogenesis inhibitor via disturbing multiple signaling pathways.</p>","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 6","pages":"725-735"},"PeriodicalIF":3.0,"publicationDate":"2022-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10496994","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}
C-Mannosylation is a rare type of protein glycosylation and is reportedly critical for the proper folding and secretion of parental proteins. Still, the effects of C-mannosylation on the biological functions of these modified proteins remain to be elucidated. The Trp-x-x-Trp (WxxW) sequences, whose first tryptophan (Trp) can be C-mannosylated, constitute the consensus motifs for this glycosylation modification and are commonly found in thrombospondin type 1 repeats that regulate molecular functions of thrombospondin 1 in binding and activation of transforming growth factor β (TGF-β). TGF-β plays critical roles in the control of the central nervous system including synaptogenesis. Here, we investigated whether C-mannosylation of the synthetic Trp-Ser-Pro-Trp (WSPW) peptide may confer certain functions to this peptide in TGF-β-mediated synaptogenesis. By using primary cultured rat astrocytes and cortical neurons, we found that the C-mannosylated WSPW (C-Man-WSPW) peptide, but not non-mannosylated WSPW peptide, suppressed astrocyte-conditioned medium (ACM)-stimulated synaptogenesis. C-Man-WSPW peptide inhibited both ACM- and recombinant mature TGF-β1-induced activations of Smad 2, an important mediator in TGF-β signaling. Interactions of recombinant mature TGF-β with the C-Man-WSPW peptide were similar to those with non-C-mannosylated WSPW peptide. Taken together, our results reveal a novel function of C-mannosylation of the WxxW motif in signaling and synaptogenesis mediated by TGF-β. Molecular details of how C-mannosylation affects the biological functions of WxxW motifs deserve future study for clarification.
{"title":"Thrombospondin type 1 repeat-derived C-mannosylated peptide attenuates synaptogenesis of cortical neurons induced by primary astrocytes via TGF-β.","authors":"Kazuchika Nishitsuji, Midori Ikezaki, Shino Manabe, Kenji Uchimura, Yukishige Ito, Yoshito Ihara","doi":"10.1007/s10719-021-10030-y","DOIUrl":"https://doi.org/10.1007/s10719-021-10030-y","url":null,"abstract":"<p><p>C-Mannosylation is a rare type of protein glycosylation and is reportedly critical for the proper folding and secretion of parental proteins. Still, the effects of C-mannosylation on the biological functions of these modified proteins remain to be elucidated. The Trp-x-x-Trp (WxxW) sequences, whose first tryptophan (Trp) can be C-mannosylated, constitute the consensus motifs for this glycosylation modification and are commonly found in thrombospondin type 1 repeats that regulate molecular functions of thrombospondin 1 in binding and activation of transforming growth factor β (TGF-β). TGF-β plays critical roles in the control of the central nervous system including synaptogenesis. Here, we investigated whether C-mannosylation of the synthetic Trp-Ser-Pro-Trp (WSPW) peptide may confer certain functions to this peptide in TGF-β-mediated synaptogenesis. By using primary cultured rat astrocytes and cortical neurons, we found that the C-mannosylated WSPW (C-Man-WSPW) peptide, but not non-mannosylated WSPW peptide, suppressed astrocyte-conditioned medium (ACM)-stimulated synaptogenesis. C-Man-WSPW peptide inhibited both ACM- and recombinant mature TGF-β1-induced activations of Smad 2, an important mediator in TGF-β signaling. Interactions of recombinant mature TGF-β with the C-Man-WSPW peptide were similar to those with non-C-mannosylated WSPW peptide. Taken together, our results reveal a novel function of C-mannosylation of the WxxW motif in signaling and synaptogenesis mediated by TGF-β. Molecular details of how C-mannosylation affects the biological functions of WxxW motifs deserve future study for clarification.</p>","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 5","pages":"701-710"},"PeriodicalIF":3.0,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39634371","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}
Pub Date : 2022-06-08DOI: 10.1007/s10719-022-10067-7
T. Miyagi, Koji Yamamoto
{"title":"Sialidase NEU3 and its pathological significance","authors":"T. Miyagi, Koji Yamamoto","doi":"10.1007/s10719-022-10067-7","DOIUrl":"https://doi.org/10.1007/s10719-022-10067-7","url":null,"abstract":"","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 1","pages":"677 - 683"},"PeriodicalIF":3.0,"publicationDate":"2022-06-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"45100838","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}
Pub Date : 2022-06-08DOI: 10.1007/s10719-022-10065-9
Jiao Zhou, Jinhua Gong, Yangyang Chai, D. Li, Cong Zhou, Chuansheng Sun, J. Regenstein
{"title":"Structural analysis and in vitro antitumor effect of polysaccharides from Pholiota adiposa","authors":"Jiao Zhou, Jinhua Gong, Yangyang Chai, D. Li, Cong Zhou, Chuansheng Sun, J. Regenstein","doi":"10.1007/s10719-022-10065-9","DOIUrl":"https://doi.org/10.1007/s10719-022-10065-9","url":null,"abstract":"","PeriodicalId":12762,"journal":{"name":"Glycoconjugate Journal","volume":"39 1","pages":"513 - 523"},"PeriodicalIF":3.0,"publicationDate":"2022-06-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49410030","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}