Hypoxia inducible factor −1 regulates WSSV-induced glycolytic genes in the white shrimp Litopenaeus vannamei

Godoy‐Lugo, Jose A.; Miranda-Cruz, Melissa M.; Rosas‐Rodríguez, Jesús A.; Adan-Bante, Norma Patricia; Icedo-García, Ramona; Soñanez‐Organis, José G.

doi:10.1016/j.fsi.2019.05.040

Cited by 22 publications

(19 citation statements)

References 59 publications

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“…Downstream hypoxia was also found, as indicated by the “p53 signaling pathway” and “oxidative phosphorylation”. The hypoxic status could also protect survivors of the non-breeding strain from death since p53 suppresses cell apoptosis ( 70 ), and HIF1A regulates virus-induced glycolytic genes ( 71 ).…”

Section: Discussionmentioning

confidence: 99%

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain

Jia

Jiang

et al. 2021

Front. Immunol.

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Anti-disease breeding is becoming the most promising solution to cyprinid herpesvirus-3 (CyHV-3) infection, the major threat to common carp aquaculture. Virus challenging studies suggested that a breeding strain of common carp developed resistance to CyHV-3 infection. This study illustrates the immune mechanisms involved in both sensitivity and anti-virus ability for CyHV3 infection in fish. An integrative analysis of the protein-coding genes and long non-coding RNAs (lncRNAs) using transcriptomic data was performed. Tissues from the head kidney of common carp were extracted at days 0 (the healthy control) and 7 after CyHV-3 infection (the survivors) and used to analyze the transcriptome through both Illumina and PacBio sequencing. Following analysis of the GO terms and KEGG pathways involved, the immune-related terms and pathways were merged. To dig out details on the immune aspect, the DEGs were filtered using the current common carp immune gene library. Immune gene categories and their corresponding genes in different comparison groups were revealed. Also, the immunological Gene Ontology terms for lncRNA modulation were retained. The weighted gene co-expression network analysis was used to reveal the regulation of immune genes by lncRNA. The results demonstrated that the breeding carp strain develops a marked resistance to CyHV-3 infection through a specific innate immune mechanism. The featured biological processes were autophagy, phagocytosis, cytotoxicity, and virus blockage by lectins and MUC3. Moreover, the immune-suppressive signals, such as suppression of IL21R on STAT3, PI3K mediated inhibition of inflammation by dopamine upon infection, as well as the inhibition of NLRC3 on STING during a steady state. Possible susceptible factors for CyHV-3, such as ITGB1, TLR18, and CCL4, were also revealed from the non-breeding strain. The results of this study also suggested that Nramp and PAI regulated by LncRNA could facilitate virus infection and proliferation for infected cells respectively, while T cell leukemia homeobox 3 (TLX3), as well as galectin 3 function by lncRNA, may play a role in the resistance mechanism. Therefore, immune factors that are immunogenetically insensitive or susceptible to CyHV-3 infection have been revealed.

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Section: Discussionmentioning

confidence: 99%

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain

Jia

Jiang

et al. 2021

Front. Immunol.

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“…HIF‐1 is a critical component in WSSV pathogenesis and it seems to be involved in WSSV‐induced metabolic changes in infected shrimp. Genes for glycolytic enzymes, including HK, PFK and pyruvate kinase (PK), are upregulated after WSSV infection, but this upregulation is blocked in HIF‐1‐silenced shrimp 56 . Although lactate accumulates in WSSV‐infected shrimp, the expression and activity of LDH is blocked in HIF‐1‐silenced shrimp 53 .…”

Section: Signaling Pathways That Regulate Metabolismmentioning

confidence: 99%

The regulation of shrimp metabolism by the white spot syndrome virus (WSSV)

Kumar

Huang

et al. 2021

Reviews in Aquaculture

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For more than three decades, infectious diseases have been one of the major causes of economic losses in the global shrimp industry. One of the deadliest of the shrimp pathogens is white spot syndrome virus (WSSV), which causes mass mortality in farmed shrimp. Various aspects of WSSV pathogenicity have been studied, but in this review, we will focus only on one of them, namely metabolic reprogramming. WSSV’s modulation of host metabolism affects glycolysis, the tricarboxylic acid (TCA) cycle, glutaminolysis and lipid metabolism. Several signaling pathways are involved in this regulation, including JAK‐STAT, PI3K‐AKT‐mTOR, MAPK and Ras‐Raf‐MEK, with the PI3K‐Akt‐mTOR pathway in particular playing a critical role in activating the WSSV‐induced Warburg effect. Taken together, these changes benefit the virus by facilitating WSSV replication. In this review, we summarize current knowledge regarding the metabolism‐related aspects of WSSV pathogenesis, and discuss the mechanisms by which this virus reprograms its host's metabolic pathways. A deeper understanding of these pathways, key metabolic enzymes and signaling mechanisms is potentially important for the development of effective anti‐WSSV strategies.

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“…Downstream hypoxia was also found, as indicated by the "p53 signaling pathway" and "oxidative phosphorylation". The hypoxic status could also protect the fish from death, since p53 suppresses cell apoptosis (47), and HIF1A regulates virus-induced glycolytic genes (48). Furthermore, the advantages of disease-resistant genes were reflected by comparing the survivors from the two strains, which can provide clues for breeding resistance to CyHV-3.…”

Section: Discussionmentioning

confidence: 99%

“…Downstream hypoxia was also found, as indicated by the “p53 signaling pathway” and “oxidative phosphorylation”. The hypoxic status could also protect survivors of the non-breeding strain from death, since p53 suppresses cell apoptosis (58), and HIF1A regulates virus-induced glycolytic genes (59).…”

Section: Discussionmentioning

confidence: 99%

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for A CyHV-3-Resistant Common Carp Strain

Jia

Jiang

et al. 2020

Preprint

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Anti-disease breeding is becoming the most promising solution to cyprinid herpesvirus-3 (CyHV-3) infection, the major threat to common carp aquaculture. Mortality studies suggested that a breeding strain of common carp is resistant to this disease. This study illustrates the immune mechanisms involved in anti-CyHV-3 ability. An integrative analysis of the protein-coding genes and long non-coding RNAs (lncRNAs) using transcriptomic data was also performed. Tissues from the head kidney of common carp were extracted at day 0 (the healthy control) and day 7 after CyHV-3 infection (the survivors), and used to analyze the transcriptome through both Illumina and Pac-bio sequencing. Following analysis of the Kyoto Encyclopedia of Genes and Genomes pathways and Gene Ontology terms involved, the immune-related genes were merged. These genes were filtered using the current common carp immune gene library, and information on the immune process was detailed. Immune gene categories and their corresponding genes in different comparison groups were revealed. Also, the immunological Gene Ontology terms for lncRNA modulation were retained. The weighted gene co-expression network analysis was used for the regulation of immune genes lncRNA. The results demonstrated that the breeding carp strain develops marked resistance to CyHV-3 through a specific innate immune mechanism. The featured biological processes were autophagy, phagocytosis, cytotoxicity, and virus blockage by lectins and mucin 3 (MUC3). Moreover, the immune suppressive signals, such as suppression of interleukin 21 receptor (IL21R) on STAT3, PI3K mediated the inhibition of inflammation by dopamine upon infection, as well as the inhibition of NLR family CARD domain containing 3 (NLRC3) on STING during a steady state. Possible susceptible factors for CyHV-3, such as integrin beta 1 (ITGB1), toll-like receptor 18 (TLR18), and C-C motif chemokine ligand 4 (CCL4), were also revealed from the common strain. The results of this study suggested that the regulation of galectin 3 (LGALS3) and T cell leukemia homeobox 3 (TLX3) by lncRNA may play a role in the resistance mechanism. Therefore, immune factors that are immunogenetically insensitive or susceptible to CyHV-3 infection have been revealed.

show abstract

Hypoxia inducible factor −1 regulates WSSV-induced glycolytic genes in the white shrimp Litopenaeus vannamei

Cited by 22 publications

References 59 publications

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain

The regulation of shrimp metabolism by the white spot syndrome virus (WSSV)

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for A CyHV-3-Resistant Common Carp Strain

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