Skin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells

Abstract

Cyprinid herpesvirus 3 (CyHV-3) is the aetiological agent of a mortal and highly contagious disease in common and koi carp. The skin is the major portal of entry of CyHV-3 in carp after immersion in water containing the virus. In the present study, we used in vivo bioluminescence imaging to investigate the effect of skin mucus removal and skin epidermis lesion on CyHV-3 entry. Physical treatments inducing removal of the mucus up to complete erosion of the epidermis were applied on a defined area of carp skin just before inoculation by immersion in infectious water. CyHV-3 entry in carp was drastically enhanced on the area of the skin where the mucus was removed with or without associated epidermal lesion. To investigate whether skin mucus inhibits CyHV-3 binding to epidermal cells, tail fins with an intact mucus layer or without mucus were inoculated ex vivo. While electron microscopy examination revealed numerous viral particles bound on the fins inoculated after mucus removal, no particle could be detected after infection of mucus-covered fins. Finally, anti-CyHV-3 neutralising activity of mucus extract was tested in vitro. Incubation of CyHV-3 with mucus extract reduced its infectivity in a dose dependent manner. The present study demonstrates that skin mucus removal and epidermal lesions enhance CyHV-3 entry in carp. It highlights the role of fish skin mucus as an innate immune protection against viral epidermal entry.

Antimicrobial Action of Epidermal Mucus Extract of Clarias gariepinus (Burchell, 1822) Juveniles-Fed Ginger Inclusion in Diet

“…The composition and rate of mucus secretion has been observed to change in response to microbial exposure or to environmental fluctuations (Ellis, 2001). Raj et al (2011) reported that skin mucus removal and epidermal lesions in Cyprinus carpio in invitro experiments enhanced the entry of CyHV-3 virus while the presence of skin mucus of Cyprinus carpio conferred protection against the entry of the virus. Numerous studies on innate immunity in fish have shown that fish epidermal mucus can inhibit the growth of some bacteria and therefore may have a potential source of novel antimicrobial components in it (Wei, Xavier, & Marimuthu, 2010).…”

An Overview of the Immunological Defenses in Fish Skin

“…Concomitantly, mucus plays a critical role in the defence mechanism of the fishes by also acting as a biological barrier [79][80][81]. Skin mucus has evolved to have robust mechanisms that can trap and immobilize pathogens before they can contact epithelial surfaces, because it is impermeant to most bacteria and many pathogens [82].…”

Presence of herpesvírus in diseased fishes

“…The resin embedding technique has also been applied to study ultrastructural aspects of herpesvirus into cells infected by CyHV-3 [17,25,26,27,28], of the Koi herpesvirus (KHV) infecting carp (Cyprinus carpio) [29] and of the CCV (channel catfish virus) in a kind of catfish (Ictalurus nebulosus). 4 From this technique herpesvirus particles were visualized in all stages of development in the nucleus, granular bodies containing virus particles, lamellar structures and altered nuclear membrane, and numerous viral particles in the cytoplasm [24].…”