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Teleost skin, an ancient mucosal surface that elicits gut-like immune responses
Xu, Zhen1; Parra, David1; Gomez, Daniela1; Salinas, Irene2; Zhang, Yong-An3; Jorgensen, Louise von Gersdorff; Heinecke, Rasmus Demuth4; Buchmann, Kurt4; LaPatra, Scott5; Sunyer, J. Oriol1; Sunyer, JO (reprint author), Univ Penn, Sch Vet Med, Dept Pathobiol, Philadelphia, PA 19104 USA.
2013-08-06
Source PublicationPROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
ISSN0027-8424
Volume110Issue:32Pages:13097-13102
AbstractSkin 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.; 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.
SubtypeArticle
KeywordEvolution Mucosal Immunoglobulin Ichthyophthirius Multifiliis Cutaneous
Department[Xu, Zhen ; Parra, David ; Gomez, Daniela ; Sunyer, J. Oriol] Univ Penn, Sch Vet Med, Dept Pathobiol, Philadelphia, PA 19104 USA ; [Salinas, Irene] Univ New Mexico, Dept Biol, Ctr Theoret & Evolutionary Immunol, Albuquerque, NM 87131 USA ; [Zhang, Yong-An] Chinese Acad Sci, Inst Hydrobiol, Wuhan 430072, Peoples R China ; [Heinecke, Rasmus Demuth ; Buchmann, Kurt] Univ Copenhagen, Fac Hlth & Med Sci, Dept Vet Dis Biol, Lab Aquat Pathobiol, DK-1870 Frederiskberg C, Denmark ; [LaPatra, Scott] Clear Springs Foods Inc, Res Div, Buhl, ID 83316 USA
DOI10.1073/pnas.1304319110
WOS HeadingsScience & Technology
Funding OrganizationCenter for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207] ; Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207] ; Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207] ; Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207]
Indexed BySCI
Language英语
WOS Research AreaScience & Technology - Other Topics
WOS SubjectMultidisciplinary Sciences
WOS IDWOS:000322771100061
WOS KeywordIMMUNOGLOBULIN-A ; B-CELLS ; DENDRITIC CELLS ; LYMPHOID-TISSUE ; RAINBOW-TROUT ; FISH ; IDENTIFICATION ; IGA ; DERMATOLOGY ; COLLECTION
Funding OrganizationCenter for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207] ; Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207] ; Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207] ; Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207]
Citation statistics
Cited Times:160[WOS]   [WOS Record]     [Related Records in WOS]
Document Type期刊论文
Identifierhttp://ir.ihb.ac.cn/handle/342005/19610
Collection水生生物分子与细胞生物学研究中心_期刊论文
Corresponding AuthorSunyer, JO (reprint author), Univ Penn, Sch Vet Med, Dept Pathobiol, Philadelphia, PA 19104 USA.
Affiliation1.Univ Penn, Sch Vet Med, Dept Pathobiol, Philadelphia, PA 19104 USA
2.Univ New Mexico, Dept Biol, Ctr Theoret & Evolutionary Immunol, Albuquerque, NM 87131 USA
3.Chinese Acad Sci, Inst Hydrobiol, Wuhan 430072, Peoples R China
4.Univ Copenhagen, Fac Hlth & Med Sci, Dept Vet Dis Biol, Lab Aquat Pathobiol, DK-1870 Frederiskberg C, Denmark
5.Clear Springs Foods Inc, Res Div, Buhl, ID 83316 USA
Recommended Citation
GB/T 7714
Xu, Zhen,Parra, David,Gomez, Daniela,et al. Teleost skin, an ancient mucosal surface that elicits gut-like immune responses[J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA,2013,110(32):13097-13102.
APA Xu, Zhen.,Parra, David.,Gomez, Daniela.,Salinas, Irene.,Zhang, Yong-An.,...&Sunyer, JO .(2013).Teleost skin, an ancient mucosal surface that elicits gut-like immune responses.PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA,110(32),13097-13102.
MLA Xu, Zhen,et al."Teleost skin, an ancient mucosal surface that elicits gut-like immune responses".PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 110.32(2013):13097-13102.
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