Skin-Derived TSLP Triggers Progression from Epidermal-Barrier Defects to Asthma
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{"title"=>"Skin-derived TSLP triggers progression from epidermal-barrier defects to asthma", "type"=>"journal", "authors"=>[{"first_name"=>"Shadmehr", "last_name"=>"Demehri", "scopus_author_id"=>"8627354900"}, {"first_name"=>"Mitsuru", "last_name"=>"Morimoto", "scopus_author_id"=>"8607017600"}, {"first_name"=>"Michael J.", "last_name"=>"Holtzman", "scopus_author_id"=>"7005566617"}, {"first_name"=>"Raphael", "last_name"=>"Kopan", "scopus_author_id"=>"7004214252"}], "year"=>2009, "source"=>"PLoS Biology", "identifiers"=>{"pmid"=>"19557146", "sgr"=>"66249095960", "doi"=>"10.1371/journal.pbio.1000067", "scopus"=>"2-s2.0-66249095960", "pui"=>"354663061", "isbn"=>"1545-7885 (Electronic)", "issn"=>"15449173"}, "id"=>"89a4c77a-23df-3d66-a54e-80513409e930", "abstract"=>"Asthma is a common allergic lung disease frequently affecting individuals with a prior history of eczema/atopic dermatitis (AD); however, the mechanism underlying the progression from AD to asthma (the so-called \"atopic march\") is unclear. Here we show that, like humans with AD, mice with skin-barrier defects develop AD-like skin inflammation and are susceptible to allergic asthma. Furthermore, we show that thymic stromal lymphopoietin (TSLP), overexpressed by skin keratinocytes, is the systemic driver of this bronchial hyper-responsiveness. As an AD-like model, we used mice with keratinocyte-specific deletion of RBP-j that sustained high systemic levels of TSLP. Antigen-induced allergic challenge to the lung airways of RBP-j-deficient animals resulted in a severe asthmatic phenotype not seen in similarly treated wild-type littermates. Elimination of TSLP signaling in these animals blocked the atopic march, demonstrating that high serum TSLP levels were required to sensitize the lung to allergic inflammation. Furthermore, we analyzed outbred K14-TSLP(tg) mice that maintained high systemic levels of TSLP without developing any skin pathology. Importantly, epidermal-derived TSLP was sufficient to trigger the atopic march, sensitizing the lung airways to inhaled allergens in the absence of epicutaneous sensitization. Based on these findings, we propose that in addition to early treatment of the primary skin-barrier defects, selective inhibition of systemic TSLP may be the key to blocking the development of asthma in AD patients.", "link"=>"http://www.mendeley.com/research/skinderived-tslp-triggers-progression-epidermalbarrier-defects-asthma", "reader_count"=>91, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>7, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>31, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>6, "Student > Master"=>7, "Other"=>6, "Student > Bachelor"=>9, "Lecturer"=>1, "Professor"=>6, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>7, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>31, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>6, "Student > Master"=>7, "Other"=>6, "Student > Bachelor"=>9, "Lecturer"=>1, "Professor"=>6, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>5, "Materials Science"=>1, "Agricultural and Biological Sciences"=>43, "Medicine and Dentistry"=>24, "Pharmacology, Toxicology and Pharmaceutical Science"=>4, "Veterinary Science and Veterinary Medicine"=>1, "Physics and Astronomy"=>1, "Chemistry"=>1, "Computer Science"=>2, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>24}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>43}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>4}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>1, "South Korea"=>1, "United States"=>5, "Japan"=>1, "Brazil"=>1, "United Kingdom"=>2, "Italy"=>1, "Australia"=>1, "Germany"=>1}, "group_count"=>3}

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  • {"files"=>["https://ndownloader.figshare.com/files/444294", "https://ndownloader.figshare.com/files/444325", "https://ndownloader.figshare.com/files/444360", "https://ndownloader.figshare.com/files/444422", "https://ndownloader.figshare.com/files/444451", "https://ndownloader.figshare.com/files/444479", "https://ndownloader.figshare.com/files/444514", "https://ndownloader.figshare.com/files/444547", "https://ndownloader.figshare.com/files/444570"], "description"=>"<div><p>Asthma is a common allergic lung disease frequently affecting individuals with a prior history of eczema/atopic dermatitis (AD); however, the mechanism underlying the progression from AD to asthma (the so-called “atopic march”) is unclear. Here we show that, like humans with AD, mice with skin-barrier defects develop AD-like skin inflammation and are susceptible to allergic asthma. Furthermore, we show that thymic stromal lymphopoietin (TSLP), overexpressed by skin keratinocytes, is the systemic driver of this bronchial hyper-responsiveness. As an AD-like model, we used mice with keratinocyte-specific deletion of RBP-j that sustained high systemic levels of TSLP. Antigen-induced allergic challenge to the lung airways of RBP-j–deficient animals resulted in a severe asthmatic phenotype not seen in similarly treated wild-type littermates. Elimination of TSLP signaling in these animals blocked the atopic march, demonstrating that high serum TSLP levels were required to sensitize the lung to allergic inflammation. Furthermore, we analyzed outbred <em>K14-TSLP<sup>tg</sup></em> mice that maintained high systemic levels of TSLP without developing any skin pathology. Importantly, epidermal-derived TSLP was sufficient to trigger the atopic march, sensitizing the lung airways to inhaled allergens in the absence of epicutaneous sensitization. Based on these findings, we propose that in addition to early treatment of the primary skin-barrier defects, selective inhibition of systemic TSLP may be the key to blocking the development of asthma in AD patients.</p></div>", "links"=>[], "tags"=>["skin-derived", "tslp", "triggers", "progression", "epidermal-barrier", "defects", "asthma"], "article_id"=>147582, "categories"=>["Medicine", "Cancer", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.s001", "https://dx.doi.org/10.1371/journal.pbio.1000067.s002", "https://dx.doi.org/10.1371/journal.pbio.1000067.s003", "https://dx.doi.org/10.1371/journal.pbio.1000067.s004", "https://dx.doi.org/10.1371/journal.pbio.1000067.s005", "https://dx.doi.org/10.1371/journal.pbio.1000067.s006", "https://dx.doi.org/10.1371/journal.pbio.1000067.s007", "https://dx.doi.org/10.1371/journal.pbio.1000067.s008", "https://dx.doi.org/10.1371/journal.pbio.1000067.s009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Skin_Derived_TSLP_Triggers_Progression_from_Epidermal_Barrier_Defects_to_Asthma/147582", "title"=>"Skin-Derived TSLP Triggers Progression from Epidermal-Barrier Defects to Asthma", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-05-19 02:06:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/896898"], "description"=>"<p>(A) H&E and Toluidine blue staining of the skin documents severe AD-like changes in RBP-j–deficient mice, including epidermal hyperkeratosis, parakeratosis, acanthosis, skin inflammation, and increased number of dermal mast cells (insets) detectable as early as 1 wk after birth, which worsen as RBP-jCKO animals age (6 wk and 10 wk). Note that the keratin cysts formed in the dermis of RBP-jCKO mice are due to the destruction of RBP-j–deficient hair follicles <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000067#pbio.1000067-Yamamoto1\" target=\"_blank\">[42]</a>. (B) The progression of skin inflammation is reflected in RBP-jCKO serum IgE levels, which are dramatically elevated by 10 wk of age (10 wk; <i>n</i> = 4 for each group; *<i>p</i><0.01). (C) Intracellular cytokine staining of CD4<sup>+</sup> T cells isolated from lymph nodes (mixture of inguinal and axillary) or spleen shows a robust interleukin (IL)-4-positive and interferon (IFN)-γ-negative Th2 cell presence in 10-wk-old RBP-jCKO animals, indicating the development of a full-blown AD-like allergic inflammation. Percentage of cells in each quadrant is included (representative data are presented). (D) H&E and periodic acid-Schiff (PAS) staining of the lung do not show any signs of inflammation in 10-wk-old RBP-jCKO animals; however, at 52 wk (1 y), the mutant mice develop lung inflammation. The pathology of RBP-jCKO lung includes immune cell infiltration around the airways and blood vessels (arrowheads), goblet cell hyperplasia in the airways (arrow; insets), and airway remodeling (representative pictures are presented; scale bar: 50 µm).</p>", "links"=>[], "tags"=>["mice", "lacking", "rbp-j", "notch", "keratinocytes", "ad-like", "culminating", "aged", "animals"], "article_id"=>567342, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RBP_jCKO_mice_lacking_RBP_j_and_thus_notch_signaling_in_skin_keratinocytes_develop_a_progressive_AD_like_disease_culminating_in_aged_animals_with_lung_inflammation_/567342", "title"=>"RBP-jCKO mice lacking RBP-j (and thus, notch signaling) in skin keratinocytes develop a progressive, AD-like disease culminating in aged animals with lung inflammation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-19 02:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/897035"], "description"=>"<p>(A and B) There are more leukocytes (A) and a higher percentage of eosinophils (B) present in BAL fluid collected from OVA-treated RBP-jCKO mice in comparison to their wild-type littermates (<i>Msx2-Cre/+;RBP-j<sup>flox/+</sup></i>, <i>RBP-j<sup>flox/flox</sup></i>, <i>RBP-j<sup>flox/+</sup></i>), indicating a severe airway inflammation in these mutant animals (M, macrophages; E, eosinophils; L, lymphocytes; N, neutrophils). (C) IgE reaches detectable levels only in BAL fluid from RBP-j–deficient mice, further indicating the high intensity of OVA-induced allergic inflammation in the RBP-jCKO lung. (D) Comparing lung histology of RBP-jCKO with wild-type littermates sensitized and challenged with OVA shows a significantly more intense lung inflammation in RBP-jCKO mice. H&E and PAS staining shows greater immune cell infiltration around the airways and blood vessels (arrowheads), increased airway remodeling, goblet cell hyperplasia (insets), and mucus overproduction in the mutant lung (representative pictures are presented; scale bar: 50 µm). “Controls” refers to RBP-jCKO and wild-type animals treated with PBS instead of OVA (<i>n</i> = 4 for each group; *<i>p</i><0.05, comparing the adjacent groups). These data are confirmed in additional independent experiments.</p>", "links"=>[], "tags"=>["seven-wk-old", "rbp-jcko", "mice", "allergic", "inflammation", "ova-induced", "murine"], "article_id"=>567486, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Five_to_seven_wk_old_RBP_jCKO_mice_develop_a_severe_allergic_lung_inflammation_in_an_OVA_induced_murine_model_of_asthma_/567486", "title"=>"Five- to seven-wk-old RBP-jCKO mice develop a severe allergic lung inflammation in an OVA-induced murine model of asthma.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-19 02:04:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/897200"], "description"=>"<p>(A) H&E and Toluidine blue staining of the skin shows the persistence of epidermal hyperplasia, hyperkeratosis, parakeratosis, and acanthosis in 10-wk-old RBP-jCKO;IL7rα-/- skin. However, the local skin inflammation and number of dermal mast cells (insets) are markedly reduced in RBP-jCKO;IL7rα-/- skin (representative pictures are presented; scale bar: 50 µm <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000067#pbio.1000067-He1\" target=\"_blank\">[28]</a>). (B) The quantitative analysis of mast cell infiltration in the dermis of RBP-jCKO;IL7rα-/- (R;I) shows that there is still more mast cell accumulation in RBP-jCKO;IL7rα-/- compared to wild-type (Wt) and IL7rα-/- (I) skin. The bar graphs show the average number of mast cells in ten random 100× microscope fields (*<i>p</i><0.001). (C) Serum IgE levels of 10-wk-old RBP-jCKO;IL7rα-/- mice are highly elevated and are comparable to those of RBP-jCKO (<i>Msx2-Cre/+;RBP-j<sup>flox/flox</sup>;IL7r</i>α<i>+/-</i>, R) littermates (*<i>p</i><0.01). (D) Intracellular cytokine staining shows a significant population of IL-4-producing Th2 cells in inguinal/axillary lymph nodes and spleen of 10-wk-old RBP-jCKO;IL7rα-/- animals (representative data are presented). (E) Comparing lung histology of 5- to 7-wk-old RBP-jCKO;IL7rα-/-, RBP-jCKO, IL7rα-/-, and wild-type littermates sensitized and challenged with OVA shows a complete reversal of the intense RBP-jCKO lung inflammation in RBP-jCKO;IL7rα-/- mice. H&E and PAS staining shows the muted inflammatory response around the airways and blood vessels (arrowheads), and lack of airway remodeling or goblet cell hyperplasia (insets) in RBP-jCKO;IL7rα-/- lung (representative pictures are presented; scale bar: 50 µm). (F and G) The average number of leukocytes (F) and percentage of eosinophils (G) in BAL fluid from OVA-treated RBP-jCKO;IL7rα-/- lung is lower than that of wild-type lung treated similarly, indicating that deletion of <i>IL7R</i>α rescues the allergic lung inflammation in RBP-jCKO mice (M, macrophages; E, eosinophils; L, lymphocytes; N, neutrophils). (H) IgE remains below detection levels in BAL fluid from OVA-treated RBP-jCKO;IL7rα-/- mice, further confirming that the intense OVA-induced allergic inflammation in RBP-jCKO lung is absent in RBP-jCKO;IL7rα-/- lung. To avoid death among RBP-jCKO cohort, all the animals in this study are challenged intranasally with OVA twice. Although the asthmatic response among RBP-jCKO;IL7rα-/-, IL7rα-/-, and wild-type groups is minimal, a severe response is seen in RBP-jCKO mice. “Controls” refers to RBP-jCKO;IL7rα-/-, RBP-jCKO, IL7rα-/-, and wild-type animals treated with PBS instead of OVA (<i>n</i> = 4 for each group; *<i>p</i><0.01, compared to wild-type cohort). These data are confirmed in additional independent experiments.</p>", "links"=>[], "tags"=>["signaling", "blockade", "rescues", "asthmatic", "phenotype", "rbp-jcko"], "article_id"=>567654, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TSLP_signaling_blockade_rescues_asthmatic_phenotype_of_RBP_jCKO_mice_/567654", "title"=>"TSLP signaling blockade rescues asthmatic phenotype of RBP-jCKO mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-19 02:07:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/897358"], "description"=>"<p>Age- and sex-matched RBP-jCKO;IL7rα-/-, RBP-jCKO, IL7rα-/-, and wild-type littermates are sensitized and challenged with OVA as in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000067#pbio-1000067-g003\" target=\"_blank\">Figure 3</a>. Airway reactivity at the basal state (vehicle alone; V) and in response to increasing doses of methacholine (2.5, 5, 10, 20, 40, and 80 mg/ml) is monitored in OVA-treated animals using total lung resistance (R<sub>L</sub>; <i>n</i> = 4 for each group). OVA-treated RBP-jCKO animals mount a severe airway hyper-responsiveness at 5 mg/ml of methacholine and do not tolerate methacholine doses less than or equal to 10 mg/ml, developing fatal labored breathing. OVA-treated RBP-jCKO;IL7rα-/-, IL7rα-/-, and wild-type mice, on the other hand, show moderate response only to the highest dose of methacholine (*<i>p</i><0.01). Data are presented as mean + standard deviation of percent increase in total lung resistance compared to basal state (vehicle alone; V) in each group. These measurements are confirmed in another independent set of experiments.</p>", "links"=>[], "tags"=>["airway", "hyper-responsiveness", "ova-treated", "rbp-jcko", "mice", "tslp"], "article_id"=>567809, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Severe_airway_hyper_responsiveness_among_OVA_treated_RBP_jCKO_mice_is_dependent_on_TSLP_signaling_/567809", "title"=>"Severe airway hyper-responsiveness among OVA-treated RBP-jCKO mice is dependent on TSLP signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-19 02:10:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/897450"], "description"=>"<p>(A) Skin-derived TSLP overexpression leads to high systemic TSLP levels in the serum of <i>K14-TSLP<sup>tg</sup></i> mice (<i>n</i> = 10 for each group; *<i>p</i><0.01). (B–D) Under normal conditions, skin TSLP overproduction on an outbred C57BL/6-CD1 background does not elicit any allergic inflammation in <i>K14-TSLP<sup>tg</sup></i> mice. Note the normal skin histology (B), normal serum IgE levels (<i>n</i> = 10 in each group)(C), and normal number of peripheral IL-4-producing Th2 cells (D) in <i>K14-TSLP<sup>tg</sup></i> mice at postnatal day 120 (P120). (E) H&E and PAS stained lung sections of <i>K14-TSLP<sup>tg</sup></i> animals confirm that no inflammation or airway remodeling occurred at P120 (scale bar: 50 µm).</p>", "links"=>[], "tags"=>["mice", "allergic", "inflammation"], "article_id"=>567903, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_K14_TSLP_tg_mice_exhibit_no_sign_of_skin_or_lung_allergic_inflammation_under_normal_conditions_/567903", "title"=>"<i>K14-TSLP<sup>tg</sup></i> mice exhibit no sign of skin or lung allergic inflammation under normal conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-19 02:11:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/897573"], "description"=>"<p>(A) Histological analysis shows severe inflammatory cell infiltrates (arrowheads), airway remodeling, and goblet cell hyperplasia (arrow; insets) in the lung airways of 5- to 7-wk-old <i>K14-TSLP<sup>tg</sup></i> animals that are sensitized and challenged with OVA, but not in similarly treated wild-type littermates (scale bar: 50 µm). (B–D) BAL fluid analysis shows more leukocytes (B), a higher percentage of eosinophils (C), and specific appearance of IgE in lung airways of OVA-treated <i>K14-TSLP<sup>tg</sup></i> mice (D), confirming the higher intensity of the asthmatic phenotype conferred by the TSLP overexpression in the morphologically normal skin (M, macrophages; E, eosinophils; L, lymphocytes; N, neutrophils). (E) The severe allergic inflammation in OVA-treated <i>K14-TSLP<sup>tg</sup></i> lungs leads to drastic elevation of serum IgE in the animals. “Controls” refers to <i>K14-TSLP<sup>tg</sup></i> and wild-type mice treated with PBS alone (<i>n</i> = 4 for each group; *<i>p</i><0.05, comparing the adjacent groups). (F) Total lung resistance (R<sub>L</sub>) measurements show that OVA-treated <i>K14-TSLP<sup>tg</sup></i> lung airways are hyper-responsive to increasing doses of nebulized methacholine as compared to OVA-treated wild types (V: vehicle-only basal measurement; <i>n</i> = 4 for each group; *<i>p</i><0.05). These findings are confirmed in additional independent experiments.</p>", "links"=>[], "tags"=>["reveals", "mice", "prone", "asthmatic"], "article_id"=>568033, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Shadmehr Demehri", "Mitsuru Morimoto", "Michael J. Holtzman", "Raphael Kopan"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000067.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_OVA_treatment_reveals_that_K14_TSLP_tg_mice_are_prone_to_asthmatic_phenotype_/568033", "title"=>"OVA treatment reveals that <i>K14-TSLP<sup>tg</sup></i> mice are prone to asthmatic phenotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-19 02:13:53"}

PMC Usage Stats | Further Information

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Relative Metric

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