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

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          Abstract

          The neuroendocrine-immune (NEI) regulatory network is a complex system, which plays an indispensable role in the immunity of host. In this study, a neuroendocrine immunomodulatory axis (NIA)-like pathway mediated by the nervous system and haemocytes was characterized in the oyster Crassostrea gigas. Once invaded pathogen was recognized by the host, the nervous system would temporally release neurotransmitters to modulate the immune response. Instead of acting passively, oyster haemocytes were able to mediate neuronal immunomodulation promptly by controlling the expression of specific neurotransmitter receptors on cell surface and modulating their binding sensitivities, thus regulating intracellular concentration of Ca 2+. This neural immunomodulation mediated by the nervous system and haemocytes could influence cellular immunity in oyster by affecting mRNA expression level of TNF genes, and humoral immunity by affecting the activities of key immune-related enzymes. In summary, though simple in structure, the ‘nervous-haemocyte’ NIA-like pathway regulates both cellular and humoral immunity in oyster, meaning a world to the effective immune regulation of the NEI network.

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          Most cited references44

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          Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens.

          The central nervous system (CNS) regulates innate immune responses through hormonal and neuronal routes. The neuroendocrine stress response and the sympathetic and parasympathetic nervous systems generally inhibit innate immune responses at systemic and regional levels, whereas the peripheral nervous system tends to amplify local innate immune responses. These systems work together to first activate and amplify local inflammatory responses that contain or eliminate invading pathogens, and subsequently to terminate inflammation and restore host homeostasis. Here, I review these regulatory mechanisms and discuss the evidence indicating that the CNS can be considered as integral to acute-phase inflammatory responses to pathogens as the innate immune system.
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            Phagocyte-derived catecholamines enhance acute inflammatory injury.

            It is becoming increasingly clear that the autonomic nervous system and the immune system demonstrate cross-talk during inflammation by means of sympathetic and parasympathetic pathways. We investigated whether phagocytes are capable of de novo production of catecholamines, suggesting an autocrine/paracrine self-regulatory mechanism by catecholamines during inflammation, as has been described for lymphocytes. Here we show that exposure of phagocytes to lipopolysaccharide led to a release of catecholamines and an induction of catecholamine-generating and degrading enzymes, indicating the presence of the complete intracellular machinery for the generation, release and inactivation of catecholamines. To assess the importance of these findings in vivo, we chose two models of acute lung injury. Blockade of alpha2-adrenoreceptors or catecholamine-generating enzymes greatly suppressed lung inflammation, whereas the opposite was the case either for an alpha2-adrenoreceptor agonist or for inhibition of catecholamine-degrading enzymes. We were able to exclude T cells or sympathetic nerve endings as sources of the injury-modulating catecholamines. Our studies identify phagocytes as a new source of catecholamines, which enhance the inflammatory response.
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              Elaborate interactions between the immune and nervous systems.

              The immune system and the nervous system maintain extensive communication, including 'hardwiring' of sympathetic and parasympathetic nerves to lymphoid organs. Neurotransmitters such as acetylcholine, norepinephrine, vasoactive intestinal peptide, substance P and histamine modulate immune activity. Neuroendocrine hormones such as corticotropin-releasing factor, leptin and alpha-melanocyte stimulating hormone regulate cytokine balance. The immune system modulates brain activity, including body temperature, sleep and feeding behavior. Molecules such as the major histocompatibility complex not only direct T cells to immunogenic molecules held in its cleft but also modulate development of neuronal connections. Neurobiologists and immunologists are exploring common ideas like the synapse to understand properties such as memory that are shared in these two systems.
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                Author and article information

                Journal
                Open Biol
                Open Biol
                RSOB
                royopenbio
                Open Biology
                The Royal Society
                2046-2441
                January 2017
                11 January 2017
                11 January 2017
                : 7
                : 1
                : 160289
                Affiliations
                [1 ]Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences , Qingdao 266071, People's Republic of China
                [2 ]Key Laboratory of Mariculture and Stock Enhancement in North China's Sea, Ministry of Agriculture, Dalian Ocean University , Dalian 116023, People's Republic of China
                [3 ]University of Chinese Academy of Sciences , Beijing 100049, People's Republic of China
                Author notes
                Author information
                http://orcid.org/0000-0002-1049-9170
                Article
                rsob160289
                10.1098/rsob.160289
                5303279
                28077596
                c9bc5b45-6dbe-4f45-be1e-c9b0813e37cf
                © 2017 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 15 October 2016
                : 6 December 2016
                Funding
                Funded by: the Research Foundation for Talented Scholars in Dalian Ocean University;
                Funded by: Grants from National Science Foundation of China;
                Award ID: Nos. 41276169, 31530069
                Funded by: earmarked fund from Modern Agro-industry Technology Research System;
                Award ID: CARS-48
                Categories
                1001
                199
                133
                Research
                Research Article
                Custom metadata
                January 2017

                Life sciences
                crassostrea gigas,neuroendocrine immunomodulatory axis,circulating haemocyte,membrane receptor,immune regulation

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