Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.

Epidermal keratinocytes form a highly organized stratified epithelium and sustain a competent barrier function together with dermal and hematopoietic cells. The Notch signaling pathway is a critical regulator of epidermal integrity. Here, we show that keratinocyte-specific deletion of total Notch si...

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Main Authors: Shadmehr Demehri, Zhenyi Liu, Jonghyeob Lee, Meei-Hua Lin, Seth D Crosby, Christopher J Roberts, Perry W Grigsby, Jeffrey H Miner, Andrew G Farr, Raphael Kopan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2008-05-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060123&type=printable
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author Shadmehr Demehri
Zhenyi Liu
Jonghyeob Lee
Meei-Hua Lin
Seth D Crosby
Christopher J Roberts
Perry W Grigsby
Jeffrey H Miner
Andrew G Farr
Raphael Kopan
author_facet Shadmehr Demehri
Zhenyi Liu
Jonghyeob Lee
Meei-Hua Lin
Seth D Crosby
Christopher J Roberts
Perry W Grigsby
Jeffrey H Miner
Andrew G Farr
Raphael Kopan
author_sort Shadmehr Demehri
collection DOAJ
description Epidermal keratinocytes form a highly organized stratified epithelium and sustain a competent barrier function together with dermal and hematopoietic cells. The Notch signaling pathway is a critical regulator of epidermal integrity. Here, we show that keratinocyte-specific deletion of total Notch signaling triggered a severe systemic B-lymphoproliferative disorder, causing death. RBP-j is the DNA binding partner of Notch, but both RBP-j-dependent and independent Notch signaling were necessary for proper epidermal differentiation and lipid deposition. Loss of both pathways caused a persistent defect in skin differentiation/barrier formation. In response, high levels of thymic stromal lymphopoietin (TSLP) were released into systemic circulation by Notch-deficient keratinocytes that failed to differentiate, starting in utero. Exposure to high TSLP levels during neonatal hematopoiesis resulted in drastic expansion of peripheral pre- and immature B-lymphocytes, causing B-lymphoproliferative disorder associated with major organ infiltration and subsequent death, a previously unappreciated systemic effect of TSLP. These observations demonstrate that local skin perturbations can drive a lethal systemic disease and have important implications for a wide range of humoral and autoimmune diseases with skin manifestations.
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spelling doaj-art-4bffeee63891429ba7afc1dd280c7d4c2025-08-20T02:17:29ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852008-05-0165e12310.1371/journal.pbio.0060123Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.Shadmehr DemehriZhenyi LiuJonghyeob LeeMeei-Hua LinSeth D CrosbyChristopher J RobertsPerry W GrigsbyJeffrey H MinerAndrew G FarrRaphael KopanEpidermal keratinocytes form a highly organized stratified epithelium and sustain a competent barrier function together with dermal and hematopoietic cells. The Notch signaling pathway is a critical regulator of epidermal integrity. Here, we show that keratinocyte-specific deletion of total Notch signaling triggered a severe systemic B-lymphoproliferative disorder, causing death. RBP-j is the DNA binding partner of Notch, but both RBP-j-dependent and independent Notch signaling were necessary for proper epidermal differentiation and lipid deposition. Loss of both pathways caused a persistent defect in skin differentiation/barrier formation. In response, high levels of thymic stromal lymphopoietin (TSLP) were released into systemic circulation by Notch-deficient keratinocytes that failed to differentiate, starting in utero. Exposure to high TSLP levels during neonatal hematopoiesis resulted in drastic expansion of peripheral pre- and immature B-lymphocytes, causing B-lymphoproliferative disorder associated with major organ infiltration and subsequent death, a previously unappreciated systemic effect of TSLP. These observations demonstrate that local skin perturbations can drive a lethal systemic disease and have important implications for a wide range of humoral and autoimmune diseases with skin manifestations.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060123&type=printable
spellingShingle Shadmehr Demehri
Zhenyi Liu
Jonghyeob Lee
Meei-Hua Lin
Seth D Crosby
Christopher J Roberts
Perry W Grigsby
Jeffrey H Miner
Andrew G Farr
Raphael Kopan
Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.
PLoS Biology
title Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.
title_full Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.
title_fullStr Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.
title_full_unstemmed Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.
title_short Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity.
title_sort notch deficient skin induces a lethal systemic b lymphoproliferative disorder by secreting tslp a sentinel for epidermal integrity
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060123&type=printable
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