The neuroendocrine immunomodulatory axis-like pathway mediated by circulating haemocytes in pacific oyster<i>Crassostrea gigas</i>

Liu, Zhaoqun; Zhou, Zhi; Wang, Lingling; Yi, Qingfeng; Qiu, Limei; Song, Linsheng

doi:10.1098/rsob.160289

Cited by 47 publications

(19 citation statements)

References 52 publications

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“…5S ), suggesting the involvement of neuromodulation in the response process. Recently, neural-immune regulation in hemocytes was identified in mollusks; this regulation was conducted by neurotransmitters via a “nervous-hemocyte”-mediated neuroendocrine immunomodulatory axis (NIA)-like pathway 57 , 58 . In the present study, GO terms associated with neurotransmitter activity were significantly enriched in the mantle and hemocytes.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional changes in the Japanese scallop (Mizuhopecten yessoensis) shellinfested by Polydora provide insights into the molecular mechanism of shell formation and immunomodulation

Mao

Zhang

et al. 2018

Sci Rep

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The Japanese scallop (Mizuhopecten yessoensis) is one of the most important aquaculture species in Asian countries; however, it has suffered severe infection by Polydora in northern China in recent years, causing great economic losses. The Polydora parasitizes the shell of scallops, badly destroying the shell’s structure. To investigate the molecular response mechanism of M. yessoensis to Polydora infestion, a comprehensive and niche-targeted cDNA sequence database for diseased scallops was constructed. Additionally, the transcriptional changes in the edge mantle, central mantle and hemocytes, tissues directly related to the disease, were first described in this study. The results showed that genes involved in shell formation and immunomodulation were significantly differentially expressed due to the infestation. Different transcriptional changes existed between the two mantle regions, indicating the different molecular functions likely responsible for the formation of different shell layers. The differential expression of genes for immune recognition, signal transduction and pathogen elimination presented an integrated immune response process in scallops. Moreover, neuromodulation and glycometabolism involved in the regulation process with relevant function significantly enriched. The study provides valuable information for mechanism study of shell formation and immunomodulation in scallops.

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Section: Discussionmentioning

confidence: 99%

Transcriptional changes in the Japanese scallop (Mizuhopecten yessoensis) shellinfested by Polydora provide insights into the molecular mechanism of shell formation and immunomodulation

Mao

Zhang

et al. 2018

Sci Rep

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“…Mollusks rely on an innate immune system to protect themselves from invading environmental microbes. Hemocytes comprise an important aspect of their innate immune system, especially granular cells [ 27 ], which are involved in both cellular and humoral immunity, and serve as an immune modulator through a neuroendocrine-immune (NEI) regulatory network [ 16 ]. However, hemocytes carry a high level of OsHV-1 load in infected mollusks, which might directly disturb the whole innate immune system of mollusks and lead to death.…”

Section: Discussionmentioning

confidence: 99%

“…This would imply that apoptosis is a key part of antiviral response and under complex or antagonistic control [ 11 ]. As the major executors of cellular immune defense [ 16 , 17 ], hemocytes are attacked by OsHV-1, and an increased level of OsHV-1 DNA has been detected in mollusk hemocytes post infection [ 18 , 19 ]. Similar to crustaceans, at least three types of mollusk hemocytes have been isolated according to their size and granularity, including agranulocytes (hyaline cells), semi-granular and granular cells [ 20 , 21 ].…”

Section: Introductionmentioning

confidence: 99%

Ostreid Herpesvirus-1 Infects Specific Hemocytes in Ark Clam, Scapharca broughtonii

Xin

Bai

et al. 2018

Viruses

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High levels of ostreid herpesvirus 1 (OsHV-1) were detected in hemocytes of OsHV-1 infected mollusks. Mollusk hemocytes are comprised of different cell types with morphological and functional heterogeneity. Granular cells are considered the main immunocompetent hemocytes. This study aimed to ascertain if OsHV-1 infects specific types of hemocytes in ark clams. Types of hemocytes were first characterized through microexamination and flow cytometry. In addition to a large group of red cells, there were three types of recognizable granular cells in ark clams. Type II granular cells were mostly found with OsHV-1 infection by transmission electron microscope (TEM) examination, and represented the hemocyte type that was susceptible to OsHV-1 infection. The subcellular location of OsHV-1 particles in apoptotic type II granular cells was further analyzed. Some OsHV-1 particles were free inside the apoptotic cells, which may contribute to OsHV-1 transmission among cells in the host, some particles were also found enclosed inside apoptotic bodies. Apoptosis is an important part of the host defense system, but might also be hijacked by OsHV-1 as a strategy to escape host immune attack. Following this investigation, a primary culture of type II granular cells with OsHV-1 infection would facilitate the research on the interaction between OsHV-1 and mollusk hosts.

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“…For instance, catecholamines (CAs), ACh, 5-HT, γ-aminobutyric acid (GABA), histamine, enkephaline (ENK), glutamic acid (GA), neuropeptide Y (NPY), and nitric oxide (NO) have been identified from the nervous and endocrine tissues in mollusks ( 13 , 14 ). These neurotransmitters conduct neural immune regulation through a nervous-hemocyte neuroendocrine immunomodulatory axis (NIA)-like pathway, modulating both cellular and humoral immune activities in mollusk ( 15 ). Astonishingly, recent studies have illustrated that molluskan immune system can also synthesize neurotransmitters and may conduct autocrine/paracrine immune regulation.…”

Section: Introductionmentioning

confidence: 99%

The Cholinergic and Adrenergic Autocrine Signaling Pathway Mediates Immunomodulation in Oyster Crassostrea gigas

Liu

Wang

et al. 2018

Front. Immunol.

Self Cite

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It is becoming increasingly clear that neurotransmitters impose direct influence on regulation of the immune process. Recently, a simple but sophisticated neuroendocrine–immune (NEI) system was identified in oyster, which modulated neural immune response via a “nervous-hemocyte”-mediated neuroendocrine immunomodulatory axis (NIA)-like pathway. In the present study, the de novo synthesis of neurotransmitters and their immunomodulation in the hemocytes of oyster Crassostrea gigas were investigated to understand the autocrine/paracrine pathway independent of the nervous system. After hemocytes were exposed to lipopolysaccharide (LPS) stimulation, acetylcholine (ACh), and norepinephrine (NE) in the cell supernatants, both increased to a significantly higher level (2.71- and 2.40-fold, p < 0.05) comparing with that in the control group. The mRNA expression levels and protein activities of choline O-acetyltransferase and dopamine β-hydroxylase in hemocytes which were involved in the synthesis of ACh and NE were significantly elevated at 1 h after LPS stimulation, while the activities of acetylcholinesterase and monoamine oxidase, two enzymes essential in the metabolic inactivation of ACh and NE, were inhibited. These results demonstrated the existence of the sophisticated intracellular machinery for the generation, release and inactivation of ACh and NE in oyster hemocytes. Moreover, the hemocyte-derived neurotransmitters could in turn regulate the mRNA expressions of tumor necrosis factor (TNF) genes, the activities of superoxide dismutase, catalase and lysosome, and hemocyte phagocytosis. The phagocytic activities of hemocytes, the mRNA expressions of TNF and the activities of key immune-related enzymes were significantly changed after the block of ACh and NE receptors with different kinds of antagonists, suggesting that autocrine/paracrine self-regulation was mediated by transmembrane receptors on hemocyte. The present study proved that oyster hemocyte could de novo synthesize and release cholinergic and adrenergic neurotransmitters, and the hemocyte-derived ACh/NE could then execute a negative regulation on hemocyte phagocytosis and synthesis of immune effectors with similar autocrine/paracrine signaling pathway identified in vertebrate macrophages. Findings in the present study demonstrated that the immune and neuroendocrine system evolved from a common origin and enriched our knowledge on the evolution of NEI system.

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The neuroendocrine immunomodulatory axis-like pathway mediated by circulating haemocytes in pacific oysterCrassostrea gigas

Cited by 47 publications

References 52 publications

Transcriptional changes in the Japanese scallop (Mizuhopecten yessoensis) shellinfested by Polydora provide insights into the molecular mechanism of shell formation and immunomodulation

Transcriptional changes in the Japanese scallop (Mizuhopecten yessoensis) shellinfested by Polydora provide insights into the molecular mechanism of shell formation and immunomodulation

Ostreid Herpesvirus-1 Infects Specific Hemocytes in Ark Clam, Scapharca broughtonii

The Cholinergic and Adrenergic Autocrine Signaling Pathway Mediates Immunomodulation in Oyster Crassostrea gigas

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