Epidermal club cells and the innate immune system of minnows

Abstract

Thousands of fish species belonging to the Superorder Ostariophysi possess specialized club cells in their epidermis. Damage to the cells, as would occur during a predator attack, releases chemical substances that evoke antipredator responses in nearby shoalmates. These chemical substances have often been referred to as alarm substances and the cells that release them as alarm cells. Understanding the evolution of the cells in an alarm context has been difficult. The fish needs to be captured prior to the chemicals being released, hence the benefit to the receiver is unclear. Recent studies have suggested that the club cells are part of the immune system and are maintained by natural selection owing to the benefits that they confer against pathogens, parasites, and general injury to the epidermis. In the present study, we gave fathead minnows intraperitoneal injections of cortisol, a known immunosuppressant, or injections of a control substance (corn oil). We found that fish exposed to cortisol had suppressed immune systems (as measured by a respiratory burst assay) and that they also reduced their investment in club cells. This is the best evidence to date indicating that the club cells of Ostariophysan fishes are part of the innate immune system and that the alarm function of the cells evolved secondarily. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 891–897.

Alterations of Club Cell Activity in Epidermis of Common Carp, <I>Cyprinus Carpio</I> (Actinopterygii: Cypriniformes: Cyprinidae), due to Infection by <I>Ichthyophthirius Multifiliis</I> (Protista: Ciliophora)

“…It certainly needs clarification whether the above inconsistency is related to the fish skin condition, insufficient acclimatisation time, the influence of selective breeding, parasite specific host life cycle, or invasion intensity. These results are in accord with the hypothesis that club cells of common carp are a part of an integrated response to the parasitic damage of host epidermis (Smith 1992, Chivers et al 2007, Halbgewachs et al 2009). …”

“…The cell-mediated innate mechanisms of epidermal tissues include specialized cells such as macrophages, granulocytes, natural killer cells, and also physical barriers such as mucous layers and skin epithelial tissue lines (Jones 2001, Aoki et al 2008. The epidermal club cells of many fishes in the superorder Ostariophysi have evolved primarily as part of the immune system (Chivers et al 2007, Halbgewachs et al 2009, Ferrari et al 2010 but their functional mechanisms, with non-specific and/or specific immunity, have not been explored in detail. The evolution of club cells of ostariophysan fish remains enigmatic and controversial as it has been historically linked to chemical alarm signalling (von Frisch 1941, Smith1992, James et al 2009).…”

“…In this study an epidermal club cells anti-parasite hypothesis (Smith 1992, Magurran et al 1996, Chivers et al 2007, Halbgewachs et al 2009) was tested. If club cells have anti-parasite attributes it was predicted that injury caused by extended exposure to ciliates should result in an increased number of club cells, and a subsequent reduction in parasite activity in the epidermis.…”

Histology, histochemistry and stereology of the adipose fin of Prochilodus lineatus

“…In the median portion of this epithelium, the presence of club cells is similar to that observed in other species of teleosts, as they are round, with central nuclei and do not react with the routine staining techniques (Bart and Page, 1991;Berra et al, 1989;Flaxman, 1972;Halbgewachs et al, 2009;Koumans and Sire, 1995;McCormick and Larson, 2007;Stabell and Vegusdal, 2010;Strussmann et al, 1994;Zaccone et al, 2001).…”

Effects of two water disinfectants (chloramine T and peracetic acid) on the epidermis and gills of Garra rufa used in human ichthyotherapy

“…In particular, mucous cells are known to be responsive to general irritative insults through hyperplasia and mucous discharge as an adaptive and protective reaction (Ferguson 2006). Halbgewachs et al (2009) found that the number of club cells in fathead minnows (Pimephales promelas) decreased significantly after cortisol injection, suggesting their role in the immune response. Fish taste buds consist of several cellular components and enable the animal to identify food by detecting distinct chemical substances at a short distance (Kasumyan 1997).…”