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题名: Teleost skin, an ancient mucosal surface that elicits gut-like immune responses
作者: 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
通讯作者: Sunyer, JO (reprint author), Univ Penn, Sch Vet Med, Dept Pathobiol, Philadelphia, PA 19104 USA.
关键词: evolution ; mucosal immunoglobulin ; Ichthyophthirius multifiliis ; cutaneous
刊名: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
发表日期: 2013-08-06
DOI: 10.1073/pnas.1304319110
卷: 110, 期:32, 页:13097-13102
收录类别: SCI
文章类型: Article
部门归属: [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
WOS标题词: Science & Technology
资助者: Center for Molecular Studies in Digestive and Liver Diseases [NIH P30 DK050306]; National Science Foundation [NSF-MCB-0719599]; National Institutes of Health [R01GM085207]
类目[WOS]: Multidisciplinary Sciences
研究领域[WOS]: Science & Technology - Other Topics
摘要: 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.
英文摘要: 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.
关键词[WOS]: IMMUNOGLOBULIN-A ; B-CELLS ; DENDRITIC CELLS ; LYMPHOID-TISSUE ; RAINBOW-TROUT ; FISH ; IDENTIFICATION ; IGA ; DERMATOLOGY ; COLLECTION
语种: 英语
项目资助者: Center for Molecular Studies in Digestive and Liver Diseases(NIH P30 DK050306) ; National Science Foundation(NSF-MCB-0719599) ; National Institutes of Health(R01GM085207)
WOS记录号: WOS:000322771100061
ISSN号: 0027-8424
Citation statistics:
内容类型: 期刊论文
URI标识: http://ir.ihb.ac.cn/handle/342005/19610
Appears in Collections:水生生物分子与细胞生物学研究中心_期刊论文

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作者单位: 1.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:
Xu, Zhen; Parra, David; Gomez, Daniela; Salinas, Irene; Zhang, Yong-An; Jorgensen, Louise von Gersdorff; Heinecke, Rasmus Demuth; Buchmann, Kurt; LaPatra, Scott; Sunyer, J. Oriol.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,2013,110(32):13097-13102
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