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Characterization of a heat shock factor 1 (HSF1) gene and the association of its single nucleotide polymorphisms with susceptibility/resistance of Magallana gigas to Halomonas sp. 7T
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-31 DOI: 10.1016/j.fsi.2025.110168
Tianbao Liu , Qingyu Peng , Bo Wang , Lei Fang , Chuanyan Yang , Ning Kong , Lingling Wang , Linsheng Song
Heat shock transcription factor 1 (HSF1) is an important activator of innate immunity in the response of invertebrates to pathogen invasion. In the present study, a HSF1 was characterized in Pacific oyster Magallana gigas (MgHSF1), and its association of single nucleotide polymorphisms with susceptibility/resistance of oyster to Halomonas sp. 7T were investigated. MgHSF1 shared highly conserved DNA binding and acetylation sites with other organisms. The MgHSF1 mRNA showed high expression in haemocytes, and was significantly induced by lipopolysaccharide stimulation. The single nucleotide polymorphisms (SNPs) within promoter region of MgHSF1 gene from two oyster populations (the bacterial-resistant population and the common population) were investigated to analyze their association with bacterial resistance. Nine out of 14 SNPs including −543 A/G, −494 C/T, −488 T/A, −476 G/A, −336 C/T, −335 T/C, −334 C/T, −307 T/C and −268 T/C were found to be associated with bacterial resistance. Moreover, haplotypes TCTCGA was associated with bacterial resistance. The results threw lights on the molecular mechanisms of different oyster populations' resistance to bacterial diseases which suggested that the increased bacterial resistance of bacterial-resistant population was associated with the higher expression of MgHSF1. Meanwhile, the nine genotypes (−543 G/G, −494 T/T, −488 A/A, −476 A/A, −336 T/T, −335 C/C, −334 T/T, −307 T/T, and −268 C/C) and one haplotype (TCTCGA) could be used as potential markers for oyster selection breeding with higher bacterial resistance.
{"title":"Characterization of a heat shock factor 1 (HSF1) gene and the association of its single nucleotide polymorphisms with susceptibility/resistance of Magallana gigas to Halomonas sp. 7T","authors":"Tianbao Liu ,&nbsp;Qingyu Peng ,&nbsp;Bo Wang ,&nbsp;Lei Fang ,&nbsp;Chuanyan Yang ,&nbsp;Ning Kong ,&nbsp;Lingling Wang ,&nbsp;Linsheng Song","doi":"10.1016/j.fsi.2025.110168","DOIUrl":"10.1016/j.fsi.2025.110168","url":null,"abstract":"<div><div>Heat shock transcription factor 1 (HSF1) is an important activator of innate immunity in the response of invertebrates to pathogen invasion. In the present study, a HSF1 was characterized in Pacific oyster <em>Magallana gigas</em> (<em>Mg</em>HSF1), and its association of single nucleotide polymorphisms with susceptibility/resistance of oyster to <em>Halomonas</em> sp. 7T were investigated. <em>Mg</em>HSF1 shared highly conserved DNA binding and acetylation sites with other organisms. The <em>Mg</em>HSF1 mRNA showed high expression in haemocytes, and was significantly induced by lipopolysaccharide stimulation. The single nucleotide polymorphisms (SNPs) within promoter region of <em>Mg</em>HSF1 gene from two oyster populations (the bacterial-resistant population and the common population) were investigated to analyze their association with bacterial resistance. Nine out of 14 SNPs including −543 A/G, −494 C/T, −488 T/A, −476 G/A, −336 C/T, −335 T/C, −334 C/T, −307 T/C and −268 T/C were found to be associated with bacterial resistance. Moreover, haplotypes TCTCGA was associated with bacterial resistance. The results threw lights on the molecular mechanisms of different oyster populations' resistance to bacterial diseases which suggested that the increased bacterial resistance of bacterial-resistant population was associated with the higher expression of <em>Mg</em>HSF1. Meanwhile, the nine genotypes (−543 G/G, −494 T/T, −488 A/A, −476 A/A, −336 T/T, −335 C/C, −334 T/T, −307 T/T, and −268 C/C) and one haplotype (TCTCGA) could be used as potential markers for oyster selection breeding with higher bacterial resistance.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110168"},"PeriodicalIF":4.1,"publicationDate":"2025-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143079107","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
IPNV Inactive Vaccine Supplemented with GEL 02 PR Adjuvant: Protective Efficacy, Cross-protection, and Stability.
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-29 DOI: 10.1016/j.fsi.2025.110167
Linfang Li, Weitong Liu, Zhen Zhang, Jingzhuang Zhao, Tongyan Lu, Yizhi Shao, Liming Xu

Recently, outbreaks of infectious pancreatic necrosis (IPN) in worldwide rainbow trout farms caused by IPN virus (IPNV) strains belonging to genogroup 1 and genogroup 5 are reported. In this study, formaldehyde-inactivated vaccines supplemented with or without GEL 02 PR adjuvant were developed by using both genogroups IPNV strains and were intraperitoneally injected into rainbow trout. At 30 days post-vaccination, the viral loads of IPNV challenged rainbow trout (Oncorhynchus mykiss) in the vaccine groups were significantly decreased compared with those in the PBS group (P < 0.05), about 2.4 log and 2.5 log in the genogroup 1 and 5 IPNV inactivated vaccine with or without GEL 02 PR adjuvant groups, and the protective effect was not weakened after storage of the adjuvant vaccines at 4 °C for 12 months. Each vaccine could stimulate the expression of CD4, CD8, and IgM, and the adjuvant vaccines induced higher neutralizing antibody titers. In the long-term protection test, both the adjuvant vaccines could still effectively reduce IPNV viral loads in fish at 120 days post-vaccination, and the genogroup 5 IPNV inactivated vaccine showed cross-protection against the genogroup 1 IPNV strain. In the study of cell lines and virus seeds, CHSE-214 was successively passaged to 30 generations, and its growth characteristics and sensitivity to IPNV remained stable. When IPNV was passaged to 10 generations, the viral titers were not affected, but mutations were found in the VP2 protein of both genogroup 1 and 5 IPNV strains. The study is conducive to the improvement of IPNV vaccine development for rainbow trout.

{"title":"IPNV Inactive Vaccine Supplemented with GEL 02 PR Adjuvant: Protective Efficacy, Cross-protection, and Stability.","authors":"Linfang Li, Weitong Liu, Zhen Zhang, Jingzhuang Zhao, Tongyan Lu, Yizhi Shao, Liming Xu","doi":"10.1016/j.fsi.2025.110167","DOIUrl":"https://doi.org/10.1016/j.fsi.2025.110167","url":null,"abstract":"<p><p>Recently, outbreaks of infectious pancreatic necrosis (IPN) in worldwide rainbow trout farms caused by IPN virus (IPNV) strains belonging to genogroup 1 and genogroup 5 are reported. In this study, formaldehyde-inactivated vaccines supplemented with or without GEL 02 PR adjuvant were developed by using both genogroups IPNV strains and were intraperitoneally injected into rainbow trout. At 30 days post-vaccination, the viral loads of IPNV challenged rainbow trout (Oncorhynchus mykiss) in the vaccine groups were significantly decreased compared with those in the PBS group (P < 0.05), about 2.4 log and 2.5 log in the genogroup 1 and 5 IPNV inactivated vaccine with or without GEL 02 PR adjuvant groups, and the protective effect was not weakened after storage of the adjuvant vaccines at 4 °C for 12 months. Each vaccine could stimulate the expression of CD4, CD8, and IgM, and the adjuvant vaccines induced higher neutralizing antibody titers. In the long-term protection test, both the adjuvant vaccines could still effectively reduce IPNV viral loads in fish at 120 days post-vaccination, and the genogroup 5 IPNV inactivated vaccine showed cross-protection against the genogroup 1 IPNV strain. In the study of cell lines and virus seeds, CHSE-214 was successively passaged to 30 generations, and its growth characteristics and sensitivity to IPNV remained stable. When IPNV was passaged to 10 generations, the viral titers were not affected, but mutations were found in the VP2 protein of both genogroup 1 and 5 IPNV strains. The study is conducive to the improvement of IPNV vaccine development for rainbow trout.</p>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":" ","pages":"110167"},"PeriodicalIF":4.1,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143073714","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Erythrocytes from gilthead seabream (Sparus aurata) and European sea bass (Dicentrarchus labrax) did not engage in phagocytosis
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-29 DOI: 10.1016/j.fsi.2025.110166
Jose Carlos Campos-Sánchez, Francisco A. Guardiola, José Meseguer, María Ángeles Esteban
Phagocytosis is a fundamental innate immune process primarily executed by vertebrate leucocytes. Fish erythrocytes are involved in immune functions, although their role in phagocytosis remains poorly investigated. Consequently, this study aimed to examine the potential phagocytic mechanisms of fish erythrocytes. To this end, systemic blood erythrocytes were isolated from the teleost gilthead seabream (Sparus aurata) and European sea bass (Dicentrarchus labrax) and incubated for various times (20, 40, 60, 80, 100, and 120 min) with formalin-inactivated bacteria or heat-killed yeasts labelled with fluorescein isothiocyanate. Their putative phagocytic properties and respiratory burst activity were investigated. Our results did not indicate variations in the phagocytic ability or phagocytic capacity of erythrocytes of seabream or sea bass incubated with the bacteria, whereas no activity was detected in the case of incubation with yeast. Additionally, no respiratory burst activity was detected in the erythrocytes of either fish species under any of the experimental conditions tested. Using fluorescence microscopy, it was observed that erythrocytes could bind bacteria to their surface membranes. However, this attachment process was rarely seen with yeast cells. In contrast, examination of the fine structure of erythrocytes using transmission electron microscopy showed distinctive inward and outward folding (pseudopodia formation) and some cytoplasmic vesicles in both species. The results of our study indicate that erythrocytes from gilthead seabream and sea bass did not exhibit phagocytic capabilities when exposed to these specific target particles. Additional studies are necessary to gain more insights into how they contribute to the immune system of fish.
{"title":"Erythrocytes from gilthead seabream (Sparus aurata) and European sea bass (Dicentrarchus labrax) did not engage in phagocytosis","authors":"Jose Carlos Campos-Sánchez,&nbsp;Francisco A. Guardiola,&nbsp;José Meseguer,&nbsp;María Ángeles Esteban","doi":"10.1016/j.fsi.2025.110166","DOIUrl":"10.1016/j.fsi.2025.110166","url":null,"abstract":"<div><div>Phagocytosis is a fundamental innate immune process primarily executed by vertebrate leucocytes. Fish erythrocytes are involved in immune functions, although their role in phagocytosis remains poorly investigated. Consequently, this study aimed to examine the potential phagocytic mechanisms of fish erythrocytes. To this end, systemic blood erythrocytes were isolated from the teleost gilthead seabream (<em>Sparus aurata</em>) and European sea bass (<em>Dicentrarchus labrax</em>) and incubated for various times (20, 40, 60, 80, 100, and 120 min) with formalin-inactivated bacteria or heat-killed yeasts labelled with fluorescein isothiocyanate. Their putative phagocytic properties and respiratory burst activity were investigated. Our results did not indicate variations in the phagocytic ability or phagocytic capacity of erythrocytes of seabream or sea bass incubated with the bacteria, whereas no activity was detected in the case of incubation with yeast. Additionally, no respiratory burst activity was detected in the erythrocytes of either fish species under any of the experimental conditions tested. Using fluorescence microscopy, it was observed that erythrocytes could bind bacteria to their surface membranes. However, this attachment process was rarely seen with yeast cells. In contrast, examination of the fine structure of erythrocytes using transmission electron microscopy showed distinctive inward and outward folding (pseudopodia formation) and some cytoplasmic vesicles in both species. The results of our study indicate that erythrocytes from gilthead seabream and sea bass did not exhibit phagocytic capabilities when exposed to these specific target particles. Additional studies are necessary to gain more insights into how they contribute to the immune system of fish.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110166"},"PeriodicalIF":4.1,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143074213","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Expression Profiling and Functional Role of Cyclooxygenase-2 in the Immune and Inflammatory Responses of Red-spotted Grouper (Epinephelus akaara).
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-29 DOI: 10.1016/j.fsi.2025.110158
Yasara Kavindi Kodagoda, H A C R Hanchapola, D C G Rodrigo, Chaehyun Lim, D S Liyanage, W K M Omeka, G A N P Ganepola, M A H Dilshan, Jeongeun Kim, Ji Hun Lee, Taehyug Jeong, Qiang Wan, Gaeun Kim, Jehee Lee

Cyclooxygenase-2 (Cox-2) is a well-studied enzyme and a significant medicinal target associated with various inflammatory disorders. However, its role in pathogen-induced inflammatory responses in fish remains poorly understood. This study characterized the structural and functional properties of a Cox-2 homolog from red-spotted grouper (Epinephelus akaara) (EaCox-2). The three-dimensional structure of EaCox-2 revealed a homodimer with two functional domains: a catalytic domain with two active sites and a membrane-binding domain. EaCox-2 transcripts were ubiquitously expressed in all tested tissues of E. akaara, with the highest expression in the gills, followed by the spleen. Immune stimulation with polyinosinic:polycytidylic acid (poly I:C), lipopolysaccharides (LPS), and nervous necrosis virus (NNV) led to significant upregulation in EaCox-2 transcripts 12 and 24 h post-injection in both gill and spleen tissues. EaCox-2 overexpression in murine macrophages triggered a pro-inflammatory response characterized by M1 macrophage polarization, upregulation of pro-inflammatory mediators such as TNF-α, IL-1β, and IL-6, and iNOS enzyme, enhanced production of reactive nitric oxide (NO), and mitochondrial depolarization. These findings highlight the crucial role of EaCox-2 in regulating immune and inflammatory responses in E. akaara, providing valuable insights into the molecular mechanisms underlying teleost immunity.

{"title":"Expression Profiling and Functional Role of Cyclooxygenase-2 in the Immune and Inflammatory Responses of Red-spotted Grouper (Epinephelus akaara).","authors":"Yasara Kavindi Kodagoda, H A C R Hanchapola, D C G Rodrigo, Chaehyun Lim, D S Liyanage, W K M Omeka, G A N P Ganepola, M A H Dilshan, Jeongeun Kim, Ji Hun Lee, Taehyug Jeong, Qiang Wan, Gaeun Kim, Jehee Lee","doi":"10.1016/j.fsi.2025.110158","DOIUrl":"https://doi.org/10.1016/j.fsi.2025.110158","url":null,"abstract":"<p><p>Cyclooxygenase-2 (Cox-2) is a well-studied enzyme and a significant medicinal target associated with various inflammatory disorders. However, its role in pathogen-induced inflammatory responses in fish remains poorly understood. This study characterized the structural and functional properties of a Cox-2 homolog from red-spotted grouper (Epinephelus akaara) (EaCox-2). The three-dimensional structure of EaCox-2 revealed a homodimer with two functional domains: a catalytic domain with two active sites and a membrane-binding domain. EaCox-2 transcripts were ubiquitously expressed in all tested tissues of E. akaara, with the highest expression in the gills, followed by the spleen. Immune stimulation with polyinosinic:polycytidylic acid (poly I:C), lipopolysaccharides (LPS), and nervous necrosis virus (NNV) led to significant upregulation in EaCox-2 transcripts 12 and 24 h post-injection in both gill and spleen tissues. EaCox-2 overexpression in murine macrophages triggered a pro-inflammatory response characterized by M1 macrophage polarization, upregulation of pro-inflammatory mediators such as TNF-α, IL-1β, and IL-6, and iNOS enzyme, enhanced production of reactive nitric oxide (NO), and mitochondrial depolarization. These findings highlight the crucial role of EaCox-2 in regulating immune and inflammatory responses in E. akaara, providing valuable insights into the molecular mechanisms underlying teleost immunity.</p>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":" ","pages":"110158"},"PeriodicalIF":4.1,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143074400","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Creatine supplementation in largemouth bass (Micropterus salmoides) diets: improving intestinal health and alleviating enteritis.
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-29 DOI: 10.1016/j.fsi.2025.110164
Haodong Yu, Yukang Nie, Boran Zhang, Jiajie Xue, Kun Xue, Xixuan Huang, Xuezhen Zhang

Creatine plays an important role in regulating intestinal epithelial cell energy metabolism, epithelial integrity, and intestinal barrier function. In this study, three feeds with varying creatine concentrations (0%, 0.5%, and 4%, labeled CR0, CR0.5, and CR4, respectively) were formulated and administered to juvenile largemouth bass (Micropterus salmoides) for 8 weeks. Creatine-containing diets significantly improved growth performance and intestinal villus height. Microbiota analysis revealed that creatine-containing diets changed the beta diversity of gut microbes and increased the relative proportion of Cetobacterium. Enteritis was induced for 7 days using the corresponding feeds containing creatine and 2% DSS (labeled CR0, DCR0, DCR0.5, and DCR4). Enteritis resulted in an increase in hif1α expression in the DCR0.5 and DCR4 groups and a significant increase expression of creatine transporter SLC6A8. QPCR and Western blotting of intestinal barrier-related genes (e.g., Claudin1, Claudin4, and ZO1), MUC2 immunohistochemistry, and PAS mucus staining were used to show intestinal barrier status, these results suggest that dietary creatine attenuates the extent of intestinal barrier damage. After TUNEL and KI67 immunofluorescence analyses of the intestine and detection of the expression of relevant genes at the protein and transcript levels, the results showed that dietary addition of creatine significantly alleviated intestinal apoptosis and cellular inflammatory responses due to DSS-induced enteritis. These findings indicate long-term dietary supplementation with creatine modulated the microbial composition of the intestinal lumen of juvenile largemouth bass, promoted intestinal health, and improved anti-inflammatory properties following enteritis induction. This study provides a theoretical foundation for largemouth bass feed formulation optimization and fish enteritis control.

{"title":"Creatine supplementation in largemouth bass (Micropterus salmoides) diets: improving intestinal health and alleviating enteritis.","authors":"Haodong Yu, Yukang Nie, Boran Zhang, Jiajie Xue, Kun Xue, Xixuan Huang, Xuezhen Zhang","doi":"10.1016/j.fsi.2025.110164","DOIUrl":"https://doi.org/10.1016/j.fsi.2025.110164","url":null,"abstract":"<p><p>Creatine plays an important role in regulating intestinal epithelial cell energy metabolism, epithelial integrity, and intestinal barrier function. In this study, three feeds with varying creatine concentrations (0%, 0.5%, and 4%, labeled CR0, CR0.5, and CR4, respectively) were formulated and administered to juvenile largemouth bass (Micropterus salmoides) for 8 weeks. Creatine-containing diets significantly improved growth performance and intestinal villus height. Microbiota analysis revealed that creatine-containing diets changed the beta diversity of gut microbes and increased the relative proportion of Cetobacterium. Enteritis was induced for 7 days using the corresponding feeds containing creatine and 2% DSS (labeled CR0, DCR0, DCR0.5, and DCR4). Enteritis resulted in an increase in hif1α expression in the DCR0.5 and DCR4 groups and a significant increase expression of creatine transporter SLC6A8. QPCR and Western blotting of intestinal barrier-related genes (e.g., Claudin1, Claudin4, and ZO1), MUC2 immunohistochemistry, and PAS mucus staining were used to show intestinal barrier status, these results suggest that dietary creatine attenuates the extent of intestinal barrier damage. After TUNEL and KI67 immunofluorescence analyses of the intestine and detection of the expression of relevant genes at the protein and transcript levels, the results showed that dietary addition of creatine significantly alleviated intestinal apoptosis and cellular inflammatory responses due to DSS-induced enteritis. These findings indicate long-term dietary supplementation with creatine modulated the microbial composition of the intestinal lumen of juvenile largemouth bass, promoted intestinal health, and improved anti-inflammatory properties following enteritis induction. This study provides a theoretical foundation for largemouth bass feed formulation optimization and fish enteritis control.</p>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":" ","pages":"110164"},"PeriodicalIF":4.1,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143079111","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
SQSTM1/p62 from Litopenaeus vannamei is involved in the immune response to Vibrio infection
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-29 DOI: 10.1016/j.fsi.2025.110161
Junliang Luo, Wei Lu, Yanghui Chen, Guojian Li, Jinyuan Feng, Yanru Huang, Yu Yu, Shuanghu Cai, Jichang Jian, Shiping Yang
Sequestosome 1 (SQSTM1 or p62) has multiple functional domains, and it can not only be involved in autophagy process, but also defend against oxidative stress by invoking the Keap1/Nrf2 signaling pathway. However, the role of p62 in the response of Pacific whiteleg shrimp Litopenaeus vannamei to bacterial infection is still unclear. This study successfully identified p62 from L. vannamei (Lv-p62). The length of the open reading frame (ORF) of Lv-p62 is 1908 bp, which encoded 635 amino acids, and had Phox and Bem1p domain (PB1), Zinc-binding and ubiquitin-associated (UBA) domains. The expression level of Lv-p62 in the hepatopancreas of healthy L. vannamei is the highest, and it could be significantly induced under the stimulation of Vibrio harveyi. Besides, knocking down Lv-p62 by using RNA interference technology could reduce the expression levels of Nrf2 (nuclear factor erythroid 2-related factor 2), LC3 (microtubule-associated protein 1 light chain 3) and autophagy-related gene (ATG3, ATG5 and ATG12). Compared with the stimulation with V. harveyi alone, stimulation with V. harveyi after knocking down Lv-p62 could reduce the expression of antioxidant-, autophagy- and apoptosis-related genes in L. vannamei. Moreover, knocking down Lv-p62 could reduce the apoptosis signal of hepatopancreas and the abnormal tissue structure caused by V. harveyi. These results indicated that Lv-p62 is involved in the immune response to Vibrio infection in L. vannamei, which further enriched the regulatory function of p62 and its role in the innate immunity of shrimp.
{"title":"SQSTM1/p62 from Litopenaeus vannamei is involved in the immune response to Vibrio infection","authors":"Junliang Luo,&nbsp;Wei Lu,&nbsp;Yanghui Chen,&nbsp;Guojian Li,&nbsp;Jinyuan Feng,&nbsp;Yanru Huang,&nbsp;Yu Yu,&nbsp;Shuanghu Cai,&nbsp;Jichang Jian,&nbsp;Shiping Yang","doi":"10.1016/j.fsi.2025.110161","DOIUrl":"10.1016/j.fsi.2025.110161","url":null,"abstract":"<div><div>Sequestosome 1 (SQSTM1 or p62) has multiple functional domains, and it can not only be involved in autophagy process, but also defend against oxidative stress by invoking the Keap1/Nrf2 signaling pathway. However, the role of <em>p62</em> in the response of Pacific whiteleg shrimp <em>Litopenaeus vannamei</em> to bacterial infection is still unclear. This study successfully identified <em>p62</em> from <em>L. vannamei</em> (Lv-<em>p62</em>). The length of the open reading frame (ORF) of Lv-<em>p62</em> is 1908 bp, which encoded 635 amino acids, and had Phox and Bem1p domain (PB1), Zinc-binding and ubiquitin-associated (UBA) domains. The expression level of Lv-<em>p62</em> in the hepatopancreas of healthy <em>L. vannamei</em> is the highest, and it could be significantly induced under the stimulation of <em>Vibrio harveyi</em>. Besides, knocking down Lv-<em>p6</em>2 by using RNA interference technology could reduce the expression levels of <em>Nrf2</em> (nuclear factor erythroid 2-related factor 2), <em>LC3</em> (microtubule-associated protein 1 light chain 3) and autophagy-related gene (<em>ATG3</em>, <em>ATG5</em> and <em>ATG12</em>). Compared with the stimulation with <em>V. harveyi</em> alone, stimulation with <em>V. harveyi</em> after knocking down Lv-<em>p62</em> could reduce the expression of antioxidant-, autophagy- and apoptosis-related genes in <em>L. vannamei</em>. Moreover, knocking down Lv-<em>p62</em> could reduce the apoptosis signal of hepatopancreas and the abnormal tissue structure caused by <em>V. harveyi</em>. These results indicated that Lv-<em>p62</em> is involved in the immune response to <em>Vibrio</em> infection in <em>L. vannamei,</em> which further enriched the regulatory function of <em>p62</em> and its role in the innate immunity of shrimp.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110161"},"PeriodicalIF":4.1,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143074199","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Ethyl caffeate modulates systemic and mucosal immune responses, growth performance, and disease resistance against Vibrio parahaemolyticus in hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂)
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-28 DOI: 10.1016/j.fsi.2025.110163
Ari Widodo, Huai-Ting Huang, Novi Rosmala Dewi, Yu-Ting Chu, Fan-Hua Nan
Hybrid groupers become one of the important aquatic animals, but gastric pathogen infection causes losses due to Vibrio sp. infections. Ethyl caffeate (EC), a naturally occurring antioxidant and antibacterial derived from medicinal plant. This study investigated the effects of EC on the immune response, growth performance, as well as the systemic and mucosal immunity following Vibrio parahaemolyticus challenge. The hybrid groupers were fed diets containing EC at the concentrations of 0, 0.1, 0.25, and 0.5 g/kg (control, EC0.1, EC0.25, and EC0.5 groups, respectively). This feeding trial was conducted in three-part separate experiments consist of non-specific immune response, growth performance and challenge test experiment. The result demonstrated that the EC0.25 group had the highest total leukocyte count, phagocytic activity, and respiratory burst (O2) and the highest upregulation of genes related to antioxidant activity, inflammation, antimicrobial peptides, and stress. Furthermore, higher growth performance was observed in all EC groups than in the control group with the EC0.25 group exhibited optimum growth performance. According to the challenge test results, the EC0.25 group exhibited strong resistance to V. parahaemolyticus, with a survival rate of 96.7 %. This study elucidated a novel self-defense mechanism after EC modulating against V. parahaemolyticus challenge in hybrid groupers. The EC0.25 group had increased leukocyte subpopulation and the highest upregulation of Toll-like receptor 4, Toll-like receptor 21, MyD88, major histocompatibility complex II, immunoglobulin M, interleukin-1β, and tumor necrosis factor-α in both systemic and mucosal related-organs. Overall, dietary EC0.25 increased the hybrid groupers health status, activated multiple signaling pathways, and synergistically increased the host's systemic and mucosal immunity.
{"title":"Ethyl caffeate modulates systemic and mucosal immune responses, growth performance, and disease resistance against Vibrio parahaemolyticus in hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂)","authors":"Ari Widodo,&nbsp;Huai-Ting Huang,&nbsp;Novi Rosmala Dewi,&nbsp;Yu-Ting Chu,&nbsp;Fan-Hua Nan","doi":"10.1016/j.fsi.2025.110163","DOIUrl":"10.1016/j.fsi.2025.110163","url":null,"abstract":"<div><div>Hybrid groupers become one of the important aquatic animals, but gastric pathogen infection causes losses due to <em>Vibrio</em> sp. infections. Ethyl caffeate (EC), a naturally occurring antioxidant and antibacterial derived from medicinal plant. This study investigated the effects of EC on the immune response, growth performance, as well as the systemic and mucosal immunity following <em>Vibrio parahaemolyticus</em> challenge. The hybrid groupers were fed diets containing EC at the concentrations of 0, 0.1, 0.25, and 0.5 g/kg (control, EC0.1, EC0.25, and EC0.5 groups, respectively). This feeding trial was conducted in three-part separate experiments consist of non-specific immune response, growth performance and challenge test experiment. The result demonstrated that the EC0.25 group had the highest total leukocyte count, phagocytic activity, and respiratory burst (O<sub>2</sub><sup>−</sup>) and the highest upregulation of genes related to antioxidant activity, inflammation, antimicrobial peptides, and stress. Furthermore, higher growth performance was observed in all EC groups than in the control group with the EC0.25 group exhibited optimum growth performance. According to the challenge test results, the EC0.25 group exhibited strong resistance to <em>V</em>. <em>parahaemolyticus</em>, with a survival rate of 96.7 %. This study elucidated a novel self-defense mechanism after EC modulating against <em>V. parahaemolyticus</em> challenge in hybrid groupers. The EC0.25 group had increased leukocyte subpopulation and the highest upregulation of Toll-like receptor 4, Toll-like receptor 21, MyD8<em>8</em>, major histocompatibility complex II, immunoglobulin M, interleukin-1β, and tumor necrosis factor-α in both systemic and mucosal related-organs. Overall, dietary EC0.25 increased the hybrid groupers health status, activated multiple signaling pathways, and synergistically increased the host's systemic and mucosal immunity.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110163"},"PeriodicalIF":4.1,"publicationDate":"2025-01-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143064689","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Non-coding RNAs and regulatory networks involved in the Ameson portunus (Microsporidia)-Portunus trituberculatus interaction
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-28 DOI: 10.1016/j.fsi.2025.110162
Min Zhou, Xintong Zhang, Shuqi Chen, Zhaozhe Xin, Jinyong Zhang
Ameson portunus, the causative agent of “toothpaste disease" in Portunus trituberculatus and “slurry-like syndrome” in Scylla paramamosain, has resulted in considerable economic losses in the marine crab aquaculture industry in China. Practical control strategies are yet unavailable. Non-coding RNAs (ncRNAs) are crucial components of gene regulation of intracellular parasites, however, their roles in regulating the microsporidia-host interaction remain limited. Here we conducted a whole-transcriptome RNA-seq analysis to identify ncRNAs and to establish the interaction regulatory networks to get further insights into the A. portunus-P. trituberculatus interaction. Totally, 2805 mRNAs, 484 lncRNAs, 5 circRNAs, and 496 miRNAs were identified from A. portunus. These ncRNAs are possibly important regulators for its own energy and substrate metabolism, thereby supporting the intracellular survival and proliferation of A. portunus. DNA replication-associated mRNAs were significantly up-regulated after P. trituberculatus infection with A. portunus. It can be hypothesized that up-regulated lncRNAs may be responsible for the up-regulation of these DNA replication-related genes by miRNAs in P. trituberculatus. The downregulation of metabolic pathways is one of possible strategies of P. trituberculatus to respond the infection of A. portunus. Cross-species miRNAs were suggested to play important roles in the cross-talk of P. trituberculatus-A. portunus, e.g. the disruption of the cytoskeletal organization and normal cell function of host by this microsporidian. The results enrich the knowledge of ncRNAs in microsporidia and offer new insights into microsporidia-host interactions.
{"title":"Non-coding RNAs and regulatory networks involved in the Ameson portunus (Microsporidia)-Portunus trituberculatus interaction","authors":"Min Zhou,&nbsp;Xintong Zhang,&nbsp;Shuqi Chen,&nbsp;Zhaozhe Xin,&nbsp;Jinyong Zhang","doi":"10.1016/j.fsi.2025.110162","DOIUrl":"10.1016/j.fsi.2025.110162","url":null,"abstract":"<div><div><em>Ameson portunus</em>, the causative agent of “toothpaste disease\" in <em>Portunus trituberculatus</em> and “slurry-like syndrome” in <em>Scylla paramamosain</em>, has resulted in considerable economic losses in the marine crab aquaculture industry in China. Practical control strategies are yet unavailable. Non-coding RNAs (ncRNAs) are crucial components of gene regulation of intracellular parasites, however, their roles in regulating the microsporidia-host interaction remain limited. Here we conducted a whole-transcriptome RNA-seq analysis to identify ncRNAs and to establish the interaction regulatory networks to get further insights into the <em>A. portunus</em>-<em>P. trituberculatus</em> interaction. Totally, 2805 mRNAs, 484 lncRNAs, 5 circRNAs, and 496 miRNAs were identified from <em>A. portunus</em>. These ncRNAs are possibly important regulators for its own energy and substrate metabolism, thereby supporting the intracellular survival and proliferation of <em>A. portunus</em>. DNA replication-associated mRNAs were significantly up-regulated after <em>P. trituberculatus</em> infection with <em>A. portunus</em>. It can be hypothesized that up-regulated lncRNAs may be responsible for the up-regulation of these DNA replication-related genes by miRNAs in <em>P. trituberculatus</em>. The downregulation of metabolic pathways is one of possible strategies of <em>P. trituberculatus</em> to respond the infection of <em>A. portunus</em>. Cross-species miRNAs were suggested to play important roles in the cross-talk of <em>P. trituberculatus</em>-<em>A. portunus</em>, e.g. the disruption of the cytoskeletal organization and normal cell function of host by this microsporidian. The results enrich the knowledge of ncRNAs in microsporidia and offer new insights into microsporidia-host interactions.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110162"},"PeriodicalIF":4.1,"publicationDate":"2025-01-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143064705","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
G-CSF modulates innate and adaptive immunity via the ligand-receptor pathway of binding GCSFR in flounder (Paralichthys olivaceus)
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-27 DOI: 10.1016/j.fsi.2025.110160
Panqiu Geng , Xianghu Meng , Xiaokai Hao , Xiaoqian Tang , Jing Xing , Xiuzhen Sheng , Wenbin Zhan , Roy Ambli Dalmo , Heng Chi
Granulocyte colony stimulating factor (G-CSF) has been shown in mammalia to activate a series of signal transduction systems and exert various biological effects, such as controlling the differentiation, proliferation, and survival of granulocytes, promoting the movement of hematopoietic stem cells from the bone marrow to the bloodstream, and triggering the development of T cells, dendritic cells, and immune tolerance in transplants. In this study, the mRNA of flounder G-CSF (PoG-CSF) and its receptor (PoGCSFR) were detected and widely expressed in all examined tissues with the highest expression in peritoneal cells. G-CSF+ and GCSFR+ cells were observed to be abundantly distributed in the leukocytes from the peritoneal cavity, followed by head kidney. PoG-CSF was detected in IgM+, CD4+, MHCII+ and CD83+ cells which indicated that flounder lymphocytes, dendritic cells and other MHCII positive cells may produce G-CSF protein. PoGCSFR was expressed in the MPO+ cells, suggesting that PoGCSFR is mainly expressed in flounder granulocytes. In addition, rPoG-CSF demonstrated a capacity to enhance the phagocytosis of peritoneal cells and HK leukocytes in vitro. In vivo, the percentage of IgM+, CD4+, MHCII+, CD83+ and GCSFR+ cells in the peritoneal cavity increased after rPoG-CSF i.p. stimulation. It seemed that rPoG-CSF promoted the migration of innate cells from the head kidney into the peritoneal cavity. Meanwhile, administration of rPoG-CSF increased the expression levels of the inflammatory cytokines. Finally, drawing of the interfaces of G-CSF and GCSFR showed the principal hydrogen-bonding linkages. This study suggests that G-CSF as a pleiotropic growth factor binding to GCSFR may be involved in the regulation of innate and adaptive responses.
{"title":"G-CSF modulates innate and adaptive immunity via the ligand-receptor pathway of binding GCSFR in flounder (Paralichthys olivaceus)","authors":"Panqiu Geng ,&nbsp;Xianghu Meng ,&nbsp;Xiaokai Hao ,&nbsp;Xiaoqian Tang ,&nbsp;Jing Xing ,&nbsp;Xiuzhen Sheng ,&nbsp;Wenbin Zhan ,&nbsp;Roy Ambli Dalmo ,&nbsp;Heng Chi","doi":"10.1016/j.fsi.2025.110160","DOIUrl":"10.1016/j.fsi.2025.110160","url":null,"abstract":"<div><div>Granulocyte colony stimulating factor (G-CSF) has been shown in mammalia to activate a series of signal transduction systems and exert various biological effects, such as controlling the differentiation, proliferation, and survival of granulocytes, promoting the movement of hematopoietic stem cells from the bone marrow to the bloodstream, and triggering the development of T cells, dendritic cells, and immune tolerance in transplants. In this study, the mRNA of flounder G-CSF (<em>Po</em>G-CSF) and its receptor (<em>Po</em>GCSFR) were detected and widely expressed in all examined tissues with the highest expression in peritoneal cells. G-CSF<sup>+</sup> and GCSFR<sup>+</sup> cells were observed to be abundantly distributed in the leukocytes from the peritoneal cavity, followed by head kidney. <em>Po</em>G-CSF was detected in IgM<sup>+</sup>, CD4<sup>+</sup>, MHCII<sup>+</sup> and CD83<sup>+</sup> cells which indicated that flounder lymphocytes, dendritic cells and other MHCII positive cells may produce G-CSF protein. <em>Po</em>GCSFR was expressed in the MPO<sup>+</sup> cells, suggesting that <em>Po</em>GCSFR is mainly expressed in flounder granulocytes. In addition, r<em>Po</em>G-CSF demonstrated a capacity to enhance the phagocytosis of peritoneal cells and HK leukocytes <em>in vitro</em>. <em>In vivo</em>, the percentage of IgM<sup>+</sup>, CD4<sup>+</sup>, MHCII<sup>+</sup>, CD83<sup>+</sup> and GCSFR<sup>+</sup> cells in the peritoneal cavity increased after r<em>Po</em>G-CSF i.p. stimulation. It seemed that r<em>Po</em>G-CSF promoted the migration of innate cells from the head kidney into the peritoneal cavity. Meanwhile, administration of r<em>Po</em>G-CSF increased the expression levels of the inflammatory cytokines. Finally, drawing of the interfaces of G-CSF and GCSFR showed the principal hydrogen-bonding linkages. This study suggests that G-CSF as a pleiotropic growth factor binding to GCSFR may be involved in the regulation of innate and adaptive responses.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110160"},"PeriodicalIF":4.1,"publicationDate":"2025-01-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143064691","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Mitigating LPS-induced stress in Chinese mitten crab (Eriocheir sinensis) with P4’ peptide-bearing Bacillus subtilis
IF 4.1 2区 农林科学 Q1 FISHERIES Pub Date : 2025-01-26 DOI: 10.1016/j.fsi.2025.110156
Chao-Fan He , Ye Yang , Yong Liu , Xiang Liu , Xiang-Fei Li , Guang-Zhen Jiang , Wen-Bin Liu
The Chinese mitten crab (Eriocheir sinensis) is an important component in Chinese aquaculture. Due to its lacking adaptive immune system as a crustacean, it exhibits poor tolerance to environmental stresses, particularly the deleterious impact of lipopolysaccharide (LPS) from pathogenic bacteria during E. sinensis culture. In a previous study, we isolated LGSPDVIVIR (cmP4) peptide from cottonseed meal hydrolysate, having excellent antioxidant and immune-enhancing properties in vitro. Expressing this peptide abundantly as a tandem (a tandem of five cmP4 peptides, cmP4’) using the Bacillus subtilis expression system, we aimed to investigate the effects of incorporating recombinant B. subtilis into diets on growth performance, acute oxidative stress, and hepatopancreatic injury induced by LPS injection in E. sinensis. Crabs were cultured for a period of 12 weeks on three diets: basal diet, basal diet supplemented with 109 CFU/kg of unmodified B. subtilis, and recombinant B. subtilis, respectively. Results indicated that both B. subtilis species improved the growth performance of E. sinensis. Subsequent challenge with LPS at 400 μg/kg body weight for 6 h revealed that both B. subtilis groups exhibited improved antioxidant capacity, decreased oxidative stress indexes in hemolymph, enhanced mitochondrial membrane potential, and reduced hepatopancreatic damage compared to the single LPS-treated group. Notably, the recombinant B. subtilis had better performance, demonstrating superior effects. Specifically, compared with the single LPS-treated group, the oxidative stress indexes, mitochondrial membrane potential, and apoptosis-related gene expression in both B. subtilis groups followed a similar trend. However, the recombinant B. subtilis group displayed greater absolute changes in these indexes, a finding further supported by histopathological observations of the hepatopancreas. In conclusion, this study provides useful information for promoting the application of plant protein by-products in aquafeeds, promoting antimicrobial-free aquaculture practices for E. sinensis.
{"title":"Mitigating LPS-induced stress in Chinese mitten crab (Eriocheir sinensis) with P4’ peptide-bearing Bacillus subtilis","authors":"Chao-Fan He ,&nbsp;Ye Yang ,&nbsp;Yong Liu ,&nbsp;Xiang Liu ,&nbsp;Xiang-Fei Li ,&nbsp;Guang-Zhen Jiang ,&nbsp;Wen-Bin Liu","doi":"10.1016/j.fsi.2025.110156","DOIUrl":"10.1016/j.fsi.2025.110156","url":null,"abstract":"<div><div>The Chinese mitten crab (<em>Eriocheir sinensis</em>) is an important component in Chinese aquaculture. Due to its lacking adaptive immune system as a crustacean, it exhibits poor tolerance to environmental stresses, particularly the deleterious impact of lipopolysaccharide (LPS) from pathogenic bacteria during <em>E. sinensis</em> culture. In a previous study, we isolated LGSPDVIVIR (cmP4) peptide from cottonseed meal hydrolysate, having excellent antioxidant and immune-enhancing properties in vitro. Expressing this peptide abundantly as a tandem (a tandem of five cmP4 peptides, cmP4’) using the <em>Bacillus subtilis</em> expression system, we aimed to investigate the effects of incorporating recombinant <em>B. subtilis</em> into diets on growth performance, acute oxidative stress, and hepatopancreatic injury induced by LPS injection in <em>E. sinensis</em>. Crabs were cultured for a period of 12 weeks on three diets: basal diet, basal diet supplemented with 10<sup>9</sup> CFU/kg of unmodified <em>B. subtilis</em>, and recombinant <em>B. subtilis</em>, respectively. Results indicated that both <em>B. subtilis</em> species improved the growth performance of <em>E. sinensis</em>. Subsequent challenge with LPS at 400 μg/kg body weight for 6 h revealed that both <em>B. subtilis</em> groups exhibited improved antioxidant capacity, decreased oxidative stress indexes in hemolymph, enhanced mitochondrial membrane potential, and reduced hepatopancreatic damage compared to the single LPS-treated group. Notably, the recombinant <em>B. subtilis</em> had better performance, demonstrating superior effects. Specifically, compared with the single LPS-treated group, the oxidative stress indexes, mitochondrial membrane potential, and apoptosis-related gene expression in both <em>B. subtilis</em> groups followed a similar trend. However, the recombinant <em>B. subtilis</em> group displayed greater absolute changes in these indexes, a finding further supported by histopathological observations of the hepatopancreas. In conclusion, this study provides useful information for promoting the application of plant protein by-products in aquafeeds, promoting antimicrobial-free aquaculture practices for <em>E. sinensis</em>.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"158 ","pages":"Article 110156"},"PeriodicalIF":4.1,"publicationDate":"2025-01-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143046144","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
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Fish & shellfish immunology
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