Neuroepithelial cells (NECs) and mucous cells express a variety of neurotransmitters and neurotransmitter receptors in the gill and respiratory air-sac of the catfish Heteropneustes fossilis (Siluriformes, Heteropneustidae): a possible role in local immune defence

Lauriano, Eugenia Rita; Capillo, Gioele; Icardo, José M.; Fernandes, Jorge M.O.; Kiron, Viswanath; Kuciel, Michał; Żuwała, Krystyna; Guerrera, Maria Cristina; Aragona, Marialuisa; Germanà, Antonino; Zaccone, Giacomo

doi:10.1016/j.zool.2021.125958

Cited by 18 publications

(25 citation statements)

References 45 publications

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“…The communication processes are based on neurotransmitters, neuropeptides, cytokines, hormones and growth factors that establish the relationship between the immune system and the CNS, leading to tissue homeostasis [80]. In agreement with what was highlighted by Das and Salinas [81] regarding the neuroimmune interactions in the fish olfactory organ and those governing the immune responses in the rest of all mucosal tissues of teleosts, we found that the gill, as with the olfactory organ, is also an important route for pathogen entry into fish, based on the immunohistochemical evidence of immunoregulatory substances in the immune cells, sensory nerves and neuroepithelial endocrine cells [8,15,26]. For example, the intraepithelial localization of eosinophils, their interaction with mast cells and the interaction of mast cells with sensory nerves and the occurrence of mast cells in the gill surface layers and their opening in the exterior environment [15,25].…”

Section: Neuroimmune Communication In the Gill-cns Axissupporting

confidence: 89%

“…The consequence of the above reported observations reported in the mammalian literature and the localization of the enkephalins (met and leu enkephalins) and the antimicrobial peptide piscidin 1 in fish gill neuroepithelial endocrine cells [7,8,25] is the overlap between these endocrines and the immune cells and their interaction with the filament nervous system [15,25]. We argue that the neurotransmitters and antimicrobial peptides released by parasympathetic gill nerves bind to their respective receptors, located on the surface of immune cells and chemoreceptor cells and initiate immune-modulatory responses.…”

Section: Fish Mucosal Surfacesmentioning

confidence: 83%

“…Antimicrobial peptides are also produced by the enterocytes and enteroendocrine cells in the digestive system [6]. In this review, we report the presence of the antimicrobial peptide piscidin 1 and enkephalin previously reported in fish gill neuroendocrine epithelial cells [7,8] as potential regulators that may be able to exert an action by signaling to distant organs, such as the brain, as also emphasized for gut neuropeptides by Aresti Sanz and El Aidy [4].…”

Section: Introduction 1neuro-immune Interactions In Host Defensementioning

confidence: 80%

“…In fact, teleost gills are continuously challenged with environmental pollutants/toxins and pathogens, both of which trigger an immune response in teleost gill-associated lymphoid tissue (GIALT) [10,11]. However, several studies have demonstrated that numerous innate and adaptative immune molecules or cells involved in immune-related pathways are present in teleost gills, such as immunoglobulins (Igs), antibody-secreting cells and piscidins [8,[11][12][13][14]. Very recently, the mast cells, the mucous cells and the neuroepithelial endocrine cells (NECs) of the gills of teleosts are reported to generate immunomodulatory substances such as piscidin 1 [8,15] that are thought to have an immunomodulatory activity in fish [16].…”

Section: Interactions Between the Immune Cells And The Nervous System...mentioning

confidence: 99%

“…However, several studies have demonstrated that numerous innate and adaptative immune molecules or cells involved in immune-related pathways are present in teleost gills, such as immunoglobulins (Igs), antibody-secreting cells and piscidins [8,[11][12][13][14]. Very recently, the mast cells, the mucous cells and the neuroepithelial endocrine cells (NECs) of the gills of teleosts are reported to generate immunomodulatory substances such as piscidin 1 [8,15] that are thought to have an immunomodulatory activity in fish [16]. The gill of fish possesses a branchial innervation that is consistent amongst all fish.…”

Section: Interactions Between the Immune Cells And The Nervous System...mentioning

confidence: 99%

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Expression of the Antimicrobial Peptide Piscidin 1 and Neuropeptides in Fish Gill and Skin: A Potential Participation in Neuro-Immune Interaction

et al. 2022

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Antimicrobial peptides (AMPs) are found widespread in nature and possess antimicrobial and immunomodulatory activities. Due to their multifunctional properties, these peptides are a focus of growing body of interest and have been characterized in several fish species. Due to their similarities in amino-acid composition and amphipathic design, it has been suggested that neuropeptides may be directly involved in the innate immune response against pathogen intruders. In this review, we report the molecular characterization of the fish-specific AMP piscidin1, the production of an antibody raised against this peptide and the immunohistochemical identification of this peptide and enkephalins in the neuroepithelial cells (NECs) in the gill of several teleost fish species living in different habitats. In spite of the abundant literature on Piscidin1, the biological role of this peptide in fish visceral organs remains poorly explored, as well as the role of the neuropeptides in neuroimmune interaction in fish. The NECs, by their role as sensors of hypoxia changes in the external environments, in combination with their endocrine nature and secretion of immunomodulatory substances would influence various types of immune cells that contain piscidin, such as mast cells and eosinophils, both showing interaction with the nervous system. The discovery of piscidins in the gill and skin, their diversity and their role in the regulation of immune response will lead to better selection of these immunomodulatory molecules as drug targets to retain antimicrobial barrier function and for aquaculture therapy in the future.

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Section: Neuroimmune Communication In the Gill-cns Axissupporting

confidence: 89%

Section: Fish Mucosal Surfacesmentioning

confidence: 83%

Section: Introduction 1neuro-immune Interactions In Host Defensementioning

confidence: 80%

Section: Interactions Between the Immune Cells And The Nervous System...mentioning

confidence: 99%

Section: Interactions Between the Immune Cells And The Nervous System...mentioning

confidence: 99%

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Expression of the Antimicrobial Peptide Piscidin 1 and Neuropeptides in Fish Gill and Skin: A Potential Participation in Neuro-Immune Interaction

et al. 2022

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Immunohistochemical and ultrastructural study of the immune cell system and epithelial surfaces of the respiratory organs in the bimodally breathing African sharptooth catfish (Clarias gariepinus Burchell, 1822)

Maina

Icardo

Zaccone

et al. 2022

The Anatomical Record

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Acetylcholine (Ach) represents the old neurotransmitter in central and peripheral nervous system. Its muscarinic and nicotinic receptors (mAChRs and nAChRs) constitute an independent cholinergic system that is found in immune cells and play a key role in the regulation of the immune function and cytokine production. Gas exchanging surfaces of the gills and air‐breathing organs (ABOs) of the sharptooth catfish Clarias gariepinus were investigated using ultrastructural and confocal immunofluorescence techniques. This study was predominantly focused on the structure of the immune cell types, the expression of their neurotransmitters, including the antimicrobial peptide piscidin 1, and the functional significance of respiratory gas exchange epithelia. A network of immune cells (monocytes, eosinophils, and mast cells) was observed in the gill and the ABO epithelia. Eosinophils containing 5‐hydroxytryptamine (5‐HT) immunoreactivity were seen in close association with mast cells expressing acetylcholine (Ach), 5‐HT, neuronal nitric oxide synthase, and piscidin 1. A rich and dense cholinergic innervation dispersing across the islet capillaries of the gas exchange barrier and the localization of Ach in the squamous pavement cells covering the capillaries were evidenced byVAChT antibodies. We report for the first time that piscidin 1 (Pis 1)‐positive mast cells interact with Pis 1‐positive nerves found in the epithelia of the respiratory organs. Pis 1 immunoreactivity was also observed in the covering respiratory epithelium of the ABOs and associated with a role in local mucosal immune defense. The above results anticipate future studies on the neuro‐immune interactions at mucosal barrier surfaces, like the gill and the skin of fish, areas densely populated by different immune cells and sensory nerves that constantly sense and adapt to tissue‐specific environmental challenges.

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Comparison of vertebrate skin structure at class level: A review

Akat

Yenmiş

Pombal

et al. 2022

The Anatomical Record

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The skin is a barrier between the internal and external environment of an organism. Depending on the species, it participates in multiple functions. The skin is the organ that holds the body together, covers and protects it, and provides communication with its environment. It is also the body's primary line of defense, especially for anamniotes. All vertebrates have multilayered skin composed of three main layers: the epidermis, the dermis, and the hypodermis. The vital mission of the integument in aquatic vertebrates is mucus secretion. Cornification began in apmhibians, improved in reptilians, and endured in avian and mammalian epidermis. The feather, the most ostentatious and functional structure of avian skin, evolved in the Mesozoic period. After the extinction of the dinosaurs, birds continued to diversify, followed by the enlargement, expansion, and diversification of mammals, which brings us to the most complicated skin organization of mammals with differing glands, cells, physiological pathways, and the evolution of hair. Throughout these radical changes, some features were preserved among classes such as basic dermal structure, pigment cell types, basic coloration genetics, and similar sensory features, which enable us to track the evolutionary path. The structural and physiological properties of the skin in all classes of vertebrates are presented. The purpose of this review is to go all the way back to the agnathans and follow the path step by step up to mammals to provide a comparative large and updated survey about vertebrate skin in terms of morphology, physiology, genetics, ecology, and immunology.

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Neuroepithelial cells (NECs) and mucous cells express a variety of neurotransmitters and neurotransmitter receptors in the gill and respiratory air-sac of the catfish Heteropneustes fossilis (Siluriformes, Heteropneustidae): a possible role in local immune defence

Cited by 18 publications

References 45 publications

Expression of the Antimicrobial Peptide Piscidin 1 and Neuropeptides in Fish Gill and Skin: A Potential Participation in Neuro-Immune Interaction

Expression of the Antimicrobial Peptide Piscidin 1 and Neuropeptides in Fish Gill and Skin: A Potential Participation in Neuro-Immune Interaction

Immunohistochemical and ultrastructural study of the immune cell system and epithelial surfaces of the respiratory organs in the bimodally breathing African sharptooth catfish (Clarias gariepinus Burchell, 1822)

Comparison of vertebrate skin structure at class level: A review

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