Oral immunization of carps with chitosan–alginate microcapsule containing probiotic expressing spring viremia of carp virus (SVCV) G protein provides effective protection against SVCV infection

doi:10.1016/j.fsi.2020.07.052

Fish & Shellfish Immunology

Volume 105, October 2020, Pages 327-329

https://doi.org/10.1016/j.fsi.2020.07.052 Get rights and content

Highlights

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Chitosan-alginate microcapsule probiotic vaccine expressing SVCV G protein was developed.
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The microcapsule probiotic vaccine has good immunogenicity in carps via oral vaccination.
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The microcapsule probiotic vaccine can provide effective anti-SVCV protection for carps.
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The microcapsule oral probiotic vaccine is convenient for mass fish immunization.

Abstract

Spring viremia of carp (SVC) is highly contagious and lethal disease in cyprinid fish, in particular common carps (Cyprinus carpio), causing numerous economic losses to the aquaculture industry. SVC is presently endemic disease in Europe, America, and several countries in Asia and its causative agent is spring viremia of carp virus (SVCV). In this study, a chitosan-alginate microcapsule probiotic vaccine expressing G protein of SVCV was prepared, and the immunogenicity in carps of orally administrated with the microcapsule probiotic vaccine was evaluated. Our results showed that the microcapsule probiotic vaccine can induce potent antigen-specific immune responses in carps via oral vaccination, and provide effective anti-SVCV protection for carps. Significantly, the microcapsule probiotic vaccine is suitable for mass fish immunization, suggesting a promising vaccine strategy for fish.

Section snippets

CRediT authorship contribution statement

Shuo Jia: Data curation, Methodology, Software, Writing - original draft. Kun Zhou: Formal analysis, Investigation, Methodology. Ronghui Pan: Conceptualization, Funding acquisition, Project administration, Resources, Validation. Jing Wei: Investigation, Resources, Validation. Zhongmei Liu: Resources. Yigang Xu: Conceptualization, Funding acquisition, Project administration, Supervision, Writing - review & editing.

Acknowledgements

This work was funded by the National Key R&D Program of China (grant 2017YFD0501105), the National Natural Science Foundation of China (grant number 31672591), and “Academic Backbone” Project of Northeast Agricultural University Scholar Program (grant number 18XG24).

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Modulatory effect of CpG oligodeoxynucleotide on a DNA vaccine against nervous necrosis virus in orange-spotted grouper (Epinephelus coioides)
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There are more references available in the full text version of this article.

Cited by (27)

Transcriptome analysis reveals the relationship between Spring viremia of carp N protein-induced endoplasmic reticulum stress in Epithelioma papulosum cyprinid (EPC) cells and apoptosis and autophagy
2024, Aquaculture
Spring viremia of carp virus(SVCV) is one of the important pathogens of viral infectious diseases in fish, which brings severe economic losses to the aquaculture industry and is familiar and challenging to control viral disease in aquaculture. Currently, studies have shown that SVCV can induce endoplasmic reticulum stress, whereas the relationship between whether the most abundant protein of SVCV-N, can induce endoplasmic reticulum stress, autophagy and apoptosis has not been reported. In this study, the SVCV-N protein was overexpressed in EPC cells. According to transcriptome analysis of gene changes in EPC cells, there were 2290 differentially expressed genes, 1137 up-regulated and 1153 down-regulated genes compared to controls transfected with the empty vector pCS 2 + 8CmCherry. After gene ontology (GO) analysis, they were classified into three categories: biological processes, molecular functions and cellular components. KEGG enrichment analysis showed that 722 differentially expressed genes were enriched in 190 KEGG pathways, most of them were enriched in endoplasmic reticulum processing. Western blotting showed that GRP78, Beclin1 and Lc3-II/Lc3- I protein expression was increased, and p62 protein expression was decreased. Flow cytometry showed an increased rate of apoptosis. Activation inhibition experiments showed that activation of endoplasmic reticulum stress expression by SVCV-N protein promotes autophagy and apoptosis, and vice versa. The qRT-PCR results are consistent with the RNA-Seq, indicating that the transcriptome sequencing data are reliable. This study provides preliminary insight into the pathogenic mechanism of SVCV-N infection and provides data to reveal the mechanism.
Control of spring viremia of carp in common carp using RNA interference
2022, Aquaculture
Citation Excerpt :
RNAi can be mediated by the generation of siRNAs of 21–23 nucleotides in length from longer dsRNA or micro RNA (miRNAs) by a protein known as dicer (ribonuclease III) (Hannon, 2002; Aliyari and Ding, 2009), results finally in specific degradation of messenger RNA (mRNA) and the expression of its encoded protein cannot proceed (Fire et al., 1998; Elbashir et al., 2001). Despite significant advances that have been made to the control strategies of SVCV (Siwicki et al., 2003; Lorenzen and LaPatra, 2005; Shen et al., 2018, 2019; Liu et al., 2020; Jia et al., 2020) and other viral diseases, the effectiveness of current drugs and vaccines are limited because of many factors such as complexity, toxicity, cost and imposed the of developing drug resistance (Dave and Pomerantz, 2003). Conversely, RNAi based technology has potentials and advantages over the control strategies including the high efficiency of the gene knockdown and the ability to specifically target the gene of interest (Bumcrot et al., 2006).
In this study, the control of Carp sprivivirus, commonly known as spring viremia of carp virus (SVCV), replication in Epithelioma papulosum cyprini (EPC) cells and for the first time in common carp was investigated by using the RNA interference (RNAi) technology targeting the glycoprotein (G), matrix protein (M), and RNA-dependent RNA polymerase (L) genes. Small-interfering RNA sequences (siRNAs) were selected to target three different regions on both the SVCV-G (G-102, G-1070, and G-1456) and SVCV-M gene (M-88, M-271, and M-414). Designed specific siRNAs were investigated individually or in combinations in EPC cells. In vitro results showed that the most effective siRNAs were G-102 and M-271 that significantly reduced the virus titer in EPC cells by 1.6 logs and 1.5 logs respectively. Various combinations of the G-102 and M-271 of this study and siRNA-L-602 (targets the L-gene) from our previous study were investigated in vitro. Results showed that the most effective combination in reducing the virus replication in EPC cells was the siRNA-M-271 + L-602 combination as indicated by the significant reduction in virus titer (2.9 logs). In-vivo investigation of the siRNA-M-271 + L-602 combination by single or two successive doses in common carp challenged by IP injection of SVCV showed a significant reduction in mortality rate by 77.78% and 88.89% respectively. Results were confirmed by measuring the downregulation of SVCV-M and -L gene expression in vivo.
Results of this study proved that SVCV can be controlled in common carp through targeting the SVCV-M and -L genes by using the RNAi technology that results in a significant in-vivo reduction of the SVCV replication.
The functionality of probiotics in aquaculture: An overview
2021, Fish and Shellfish Immunology
Citation Excerpt :
Chitosan-alginate-based microcapsules containing probiotic vaccine, expressing G protein of spring viremia of carp virus (SVCV), have been shown to induce potent immune responses and provide effective anti-SVCV protection in carp. Hence, the use of probiotics in the form of vaccines is also advocated for fish immunization via large-scale oral vaccination [139]. A diet supplemented with L. acidophilus improved gut morphometry (including better length, width, and areas of absorption by villi) and boosted antioxidant potential and the immune response in terms of improved levels of superoxide dismutase, catalase, expression of transforming growth factor-beta (TGFβ), interleukin 8 (IL-8), and tumor necrosis factor-alpha (TNF-alpha) in juveniles of the common carp (Cyprinus carpio) [140].
Probiotics are live beneficial bacteria introduced into the gastrointestinal tract through food or water, promoting good health by enhancing the internal microbial balance. Probiotic microbes produce bacteriocins, siderophores, lysozymes, proteases, and hydrogen peroxides, inhibiting the growth of harmful pathogens. Such beneficial bacteria also produce many enzymes such as amylase enzyme by Aeromonas spp., Bacillus subtilis, Bacteridaceae, Clostridium spp., Lactobacillus plantarum, and Staphylococcus sp., and protease and cellulase enzymes by B. subtilis, L. plantarum, and Staphylococcus sp. In aquaculture, probiotics confer several benefits and play important roles in improving growth performances, disease resistance, immunity, health status, intestinal epithelial barrier integrity, gut microbiome, and water quality. In addition, the practical application of probiotics in aquaculture diets could minimize antibiotic side effects. Promoting these feed additives for fish would help to improve their productive performance and feed utilization and, therefore, boost fish production and safeguard human health. This review provides updated information regarding definitions, sources of bacterial probiotics, probiotic use in fish diets against pathogenic bacteria, mechanisms of action, beneficial aspects, and potential applications of probiotics in fish. It is anticipated that these will be of significant value for nutritionists, agricultural engineers, researchers, pharmacists, scientists, pharmaceutical industries, and veterinarians.
Mucosal immunoglobulins of teleost fish: A decade of advances
2021, Developmental and Comparative Immunology
Citation Excerpt :
In this type of vaccine delivery system, probiotics engineered to express G protein of spring viremia of carp (SVCV) induced high antigen-specific IgM titers in serum after 14, 28, 42 and 56 dpv. The vaccine reduced mortalities by 80% upon challenge with SVCV 42 dpv (Jia et al., 2020). Following a similar strategy, common carp larvae of 18 days post-hatch were orally immunized against cyprinid herpesvirus-3 (CyHV-3) using live Artemia previously fed with Saccharomyces cerevisiae expressing viral PORF65 tagged with GFP.
Immunoglobulins (Igs) are complex glycoproteins that play critical functions in innate and adaptive immunity of all jawed vertebrates. Given the unique characteristics of mucosal barriers, secretory Igs (sIgs) have specialized to maintain homeostasis and keep pathogens at bay at mucosal tissues from fish to mammals. In teleost fish, the three main IgH isotypes, IgM, IgD and IgT/Z can be found in different proportions at the mucosal secretions of the skin, gills, gut, nasal, buccal, and pharyngeal mucosae. Similar to the role of mammalian IgA, IgT plays a predominant role in fish mucosal immunity. Recent studies in IgT have illuminated the primordial role of sIgs in both microbiota homeostasis and pathogen control at mucosal sites. Ten years ago, IgT was discovered to be an immunoglobulin class specialized in mucosal immunity. Aiming at this 10-year anniversary, the goal of this review is to summarize the current status of the field of fish Igs since that discovery, while identifying knowledge gaps and future avenues that will move the field forward in both basic and applied science areas.
Importance of Probiotics in Fish Aquaculture: Towards the Identification and Design of Novel Probiotics
2024, Microorganisms
Physiological and transcriptomic effects of formulated diets including the prebiotics inulin, β-glucan, and chitosan on juveniles of Totoaba macdonaldi
2024, Aquaculture International

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Fish & Shellfish Immunology

Highlights

Abstract

Section snippets

CRediT authorship contribution statement

Acknowledgements

References (10)

Determination of the complete genomic sequence and analysis of the gene products of the virus of spring viremia of carp, a fish rhabdovirus

Virus Res.

Modulatory effect of CpG oligodeoxynucleotide on a DNA vaccine against nervous necrosis virus in orange-spotted grouper (Epinephelus coioides)

Fish Shellfish Immunol.

DNA vaccines as a tool for analysing the protective immune response against rhabdoviruses in rainbowtrout

Fish Shellfish Immunol.

Dendritic cell targeting of bovine viral diarrhea virus E2 protein expressed by Lactobacillus casei effectively induces antigen-specific immune responses via oral vaccination

Viruses

Recombinant lactobacillus expressing G protein of spring viremia of carp virus (SVCV) combined with ORF81 protein of koi herpesvirus (KHV): a promising way to induce protective immunity against SVCV and KHV infection in cyprinid fish via oral vaccination

Vaccine

Cited by (27)

Transcriptome analysis reveals the relationship between Spring viremia of carp N protein-induced endoplasmic reticulum stress in Epithelioma papulosum cyprinid (EPC) cells and apoptosis and autophagy

Control of spring viremia of carp in common carp using RNA interference

The functionality of probiotics in aquaculture: An overview

Mucosal immunoglobulins of teleost fish: A decade of advances

Importance of Probiotics in Fish Aquaculture: Towards the Identification and Design of Novel Probiotics

Physiological and transcriptomic effects of formulated diets including the prebiotics inulin, β-glucan, and chitosan on juveniles of Totoaba macdonaldi

Short communicationOral immunization of carps with chitosan–alginate microcapsule containing probiotic expressing spring viremia of carp virus (SVCV) G protein provides effective protection against SVCV infection

Highlights

Abstract

Section snippets

CRediT authorship contribution statement

Acknowledgements

Virus Res.

Fish Shellfish Immunol.

Fish Shellfish Immunol.

Viruses

Vaccine

Short communication
Oral immunization of carps with chitosan–alginate microcapsule containing probiotic expressing spring viremia of carp virus (SVCV) G protein provides effective protection against SVCV infection