title: Teleost skin, an ancient mucosal surface that elicits gut-like immune responses.
abstract: Skin homeostasis is critical to preserve animal integrity. Although the skin of most vertebrates is known to contain a skin-associated lymphoid tissue (SALT), very little is known about skin B-cell responses as well as their evolutionary origins. Teleost fish represent the most ancient bony vertebrates containing a SALT. Due to its lack of keratinization, teleost skin possesses living epithelial cells in direct contact with the water medium. Interestingly, teleost SALT structurally resembles that of the gut-associated lymphoid tissue, and it possesses a diverse microbiota. Thus, we hypothesized that, because teleost SALT and gut-associated lymphoid tissue have probably been subjected to similar evolutionary selective forces, their B-cell responses would be analogous. Confirming this hypothesis, we show that IgT, a teleost immunoglobulin specialized in gut immunity, plays the prevailing role in skin mucosal immunity. We found that IgT(+) B cells represent the major B-cell subset in the skin epidermis and that IgT is mainly present in polymeric form in the skin mucus. Critically, we found that the majority of the skin microbiota are coated with IgT. Moreover, IgT responses against a skin parasite were mainly limited to the skin whereas IgM responses were almost exclusively detected in the serum. Strikingly, we found that the teleost skin mucosa showed key features of mammalian mucosal surfaces exhibiting a mucosa-associated lymphoid tissue. Thus, from an evolutionary viewpoint, our findings suggest that, regardless of their phylogenetic origin and tissue localization, the chief immunoglobulins of all mucosa-associated lymphoid tissue operate under the guidance of primordially conserved principles.
authors.affiliation: Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
authors.forename: Zhen
authors.initials: Z
authors.lastname: Xu
authors.forename: David
authors.initials: D
authors.lastname: Parra
authors.forename: Daniela
authors.initials: D
authors.lastname: Gómez
authors.forename: Irene
authors.initials: I
authors.lastname: Salinas
authors.forename: Yong-An
authors.initials: YA
authors.lastname: Zhang
authors.forename: Louise
authors.initials: L
authors.lastname: von Gersdorff Jørgensen
authors.forename: Rasmus Demuth
authors.initials: RD
authors.lastname: Heinecke
authors.forename: Kurt
authors.initials: K
authors.lastname: Buchmann
authors.forename: Scott
authors.initials: S
authors.lastname: LaPatra
authors.forename: J Oriol
authors.initials: JO
authors.lastname: Sunyer
mesh_terms: D000818:Animals; D016175:B-Lymphocyte Subsets / Q000276:immunology; D001402:B-Lymphocytes / Q000276:immunology; D001419:Bacteria / Q000276:immunology; D015153:Blotting, Western; D004817:Epidermis / Q000276:immunology / Q000382:microbiology / Q000469:parasitology; D005393:Fish Diseases / Q000276:immunology / Q000382:microbiology / Q000469:parasitology; D029941:Fish Proteins; D005434:Flow Cytometry; D041981:Gastrointestinal Tract / Q000276:immunology*; D006790:Host-Parasite Interactions / Q000276:immunology; D054884:Host-Pathogen Interactions / Q000276:immunology; D016803:Hymenostomatida / Q000276:immunology / Q000502:physiology; D018928:Immunity, Mucosal / Q000276:immunology*; D007075:Immunoglobulin M / Q000097:blood / Q000276:immunology; D007136:Immunoglobulins / Q000097:blood / Q000276:immunology; D008221:Lymphoid Tissue / Q000276:immunology; D008856:Microscopy, Fluorescence; D009092:Mucous Membrane / Q000276:immunology* / Q000382:microbiology / Q000469:parasitology; D017686:Oncorhynchus mykiss / Q000276:immunology* / Q000382:microbiology / Q000469:parasitology; D012867:Skin / Q000276:immunology* / Q000382:microbiology / Q000469:parasitology
chemical_list: D029941:Fish Proteins; D007075:Immunoglobulin M; D007136:Immunoglobulins; C569864:immunoglobulin T, teleost
keywords: Ichthyophthirius multifiliis; cutaneous; evolution; mucosal immunoglobulin