Extracellular ATP-mediated purinergic immune signaling in teleost fish: A review

Li, Shuo; Zhang, Tongtong; Feng, Yifei; Sun, Jinsheng

doi:10.1016/j.aquaculture.2021.736511

Cited by 11 publications

(7 citation statements)

References 106 publications

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“…Extracellular ATP has been shown to be an effective and conservative signaling molecule to activate natural immunity ( 8 , 16 ). Therefore, it is important to study the molecular mechanisms of inflammation-induced ATP release.…”

Section: Discussionmentioning

confidence: 99%

“…Bacterial infection induced upregulation of Cx32 and Cx43 has also been demonstrated ( 45 ). In fish, Panx1, Cx32, and Cx43 were upregulated by PAMPs stimulation or bacterial infection ( 16 , 31 , 32 ). Similar to these studies, our findings showed that Lm Panx1, Lm Cx32, and Lm Cx43 were upregulated by PAMP [LPS and poly(I:C)] stimulation or E. tarda infection in vivo and in vitro ( Figures 6 , 7A ), suggesting the involvement of Lm Panx1, Lm Cx32, and Lm Cx43 in response to immune challenge in spotted sea bass.…”

Section: Discussionmentioning

confidence: 99%

“…release ( 8 – 11 ) and the activation of the NLRP3/NLRC3 inflammasome ( 12 – 15 ). Therefore, extracellular ATP was considered as an effective signaling molecule to activate the natural immune responses ( 16 ). Apparently, it is extraordinarily important to study the molecular determinants for inflammation-induced ATP release.…”

Section: Introductionmentioning

confidence: 99%

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Characterization of Pannexin1, Connexin32, and Connexin43 in Spotted Sea Bass (Lateolabrax maculatus): They Are Important Neuro-Related Immune Response Genes Involved in Inflammation-Induced ATP Release

et al. 2022

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Many immunological diseases can be treated by regulating neurobehavior, in which extracellular ATP is a vital member of endogenous danger-associated molecular pattern signaling molecule that plays a crucial part in innate neuro-related immunity. It is actively released through pannexin (Panx) and connexin (Cx) hemichannels from activated or stressed cells during inflammation, injury, or apoptosis. In addition to participating in ATP release, Panxs and Cxs also have crucial immune functions. In this study, pannexin1, three connexin32 isoforms and connexin43 were identified and characterized in spotted sea bass (Lateolabrax maculatus), which were named LmPanx1, LmCx32.2, LmCx32.3, LmCx32.7, and LmCx43. Their similar topological structures were discovered by sequence analysis: a relatively unconserved C-terminal region and four highly conserved transmembrane (TM) domains, and so on. Each extracellular (ECL) region of Panx1 has two conserved cysteine residues. Unlike Panx1, each ECL region of Cx32 and Cx43 contains three conserved cysteine residues, forming two conserved motifs: CX6CX3C motif in ECL1 and CX4CX5C motif in ECL2. Furthermore, Panx1 and Cx43 share similar genomic organization and synteny with their counterparts in selected vertebrates. Cx32 and CX43 were located in the same locus in fish, but diverged into two loci from amphibian. Moreover, despite varying expression levels, the identified genes were constitutively expressed in all examined tissues. All genes were upregulated by PAMP [lipopolysaccharide and poly(I:C)] stimulation or bacterial infection in vivo and in vitro, but they were downregulated in the brain at 6 or 12 h after stimulation. Especially, the three LmCx32 isoforms and LmCx43 were upregulated by ATP stimulation in primary head kidney leukocytes; however, downregulation of LmCx32.3 and LmCx43 expression were noted at 12 h. Conversely, ATP treatment inhibited the expression of LmPanx1. Importantly, we showed that the spotted sea bass Panx1, Cx43, and Cx32 were localized on the cellular membrane and involved in inflammation-induced ATP release. Taken together, our results demonstrated that Panx1, Cx32, and Cx43 are important neuro-related immune response genes involved in inflammation-induced ATP release.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Characterization of Pannexin1, Connexin32, and Connexin43 in Spotted Sea Bass (Lateolabrax maculatus): They Are Important Neuro-Related Immune Response Genes Involved in Inflammation-Induced ATP Release

et al. 2022

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“…In addition, as the phosphagen kinases that regulate ATP/ADP homeostasis, the released serum CsCKs might also exert immune effects via ATP. Previous studies reported that there existed conserved extracellular ATP-activated signaling pathways in fish, which activated innate immunity and induced cell apoptosis, whereas the hydrolytic product of extracellular ATP, adenosine, exhibited inhibitory effect on the immunity (55,56). It is possible that serum CsCKs might modulate tongue sole immunity via the regulation of the purinergic signaling pathway.…”

Section: Discussionmentioning

confidence: 99%

Tongue sole creatine kinases function as DAMP and activate antimicrobial immunity via TLR2

Jiang²,

Sun³

2023

Front. Immunol.

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Creatine kinase (CK) is an enzyme that regulates adenosine triphosphate (ATP) metabolism to maintain energy homeostasis. Although CK has been reported to be involved in pathogen infection, the immune function of CK remains elusive. In this study, we identified two muscle-type CK from the teleost tongue sole Cynoglossus semilaevis (designated CsCKM-1 and CsCKM-2). Bacterial infection modulated CsCKM-1/2 expression in tongue sole tissues and induced the release of CsCKM-1/2 into serum. Recombinant CsCKM-1/2 (rCsCKM-1/2) exhibited robust kinase activity and bound to bacterial pathogens and pathogen-associated molecular patterns. rCsCKM-1/2 also bound to tongue sole peripheral blood leukocytes (PBLs) and promoted PBLs to uptake bacterial pathogens, inhibit bacterial proliferation, and express proinflammatory cytokines. When co-expressed in HEK293T cells, CsCKM-1/2 were found to interact with the leucine rich domain of toll-like receptor 2 (TLR2). The presence of TLR2 antagonist significantly reduced CsCKM-1/2-induced immune response and antibacterial effect. Taken together, these results indicated that tongue sole creatine kinases function as damage-associated molecular pattern (DAMP) molecules and play an important role in antimicrobial immunity via TLR2.

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“…In the second mechanism, IAP regulates the ATP-adenosine-A 2A receptor (A 2A R)– cyclic AMP (cAMP)–protein kinase A (PKA)–NF-κB pathway (Figure ). During the initial inflammatory phase, large quantities of extracellular purines (adenosine monophosphate [AMP], adenosine diphosphate [ADP], and ATP) and pyrimidines (UDP and uridine triphosphate) are released via multiple pathways to induce autocrine and paracrine stimulation of purinergic receptors. , Extracellular ATP (eATP), which is released through secretion, degranulation, semichannel dependence, or cell death, is subsequently rapidly dephosphorylated by IAP into ADP, AMP, and adenosine . Previous studies found that the intestinal ATP levels in IAP-KO mice were significantly higher than those of WT mice .…”

Section: Iap and Its Involvement In Signal Transductionmentioning

confidence: 99%

Protective Properties of Intestinal Alkaline Phosphatase Supplementation on the Intestinal Barrier: Interactions and Effects

Gao,

Koko,

Hong

et al. 2023

J. Agric. Food Chem.

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The intestinal barrier is critical for maintaining intestinal homeostasis, and its dysfunction is associated with various diseases. Recent findings have revealed the multifunctional role of intestinal alkaline phosphatase (IAP) in diverse biological processes, including gut health maintenance and function. This review summarizes the protective effects of IAP on intestinal barrier integrity, encompassing the physical, chemical, microbial, and immune barriers. We discuss the results and insights from in vitro, animal model, and clinical studies as well as the available evidence regarding the impact of diet on IAP activity and expression. IAP can also be used as an indicator to assess intestinal-barrier-related diseases. Further research into the mechanisms of action and long-term health effects of IAP in maintaining overall intestinal health is essential for its future use as a dietary supplement or functional component in medical foods.

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Extracellular ATP-mediated purinergic immune signaling in teleost fish: A review

Cited by 11 publications

References 106 publications

Characterization of Pannexin1, Connexin32, and Connexin43 in Spotted Sea Bass (Lateolabrax maculatus): They Are Important Neuro-Related Immune Response Genes Involved in Inflammation-Induced ATP Release

Characterization of Pannexin1, Connexin32, and Connexin43 in Spotted Sea Bass (Lateolabrax maculatus): They Are Important Neuro-Related Immune Response Genes Involved in Inflammation-Induced ATP Release

Tongue sole creatine kinases function as DAMP and activate antimicrobial immunity via TLR2

Protective Properties of Intestinal Alkaline Phosphatase Supplementation on the Intestinal Barrier: Interactions and Effects

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