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Article ; Online: Hippo signaling impairs alveolar epithelial regeneration in pulmonary fibrosis.

Warren, Rachel / Lyu, Handeng / Klinkhammer, Kylie / De Langhe, Stijn P

2023 Volume 12

Abstract: Idiopathic pulmonary fibrosis (IPF) consists of fibrotic alveolar remodeling and progressive loss of pulmonary function. Genetic and experimental evidence indicates that chronic alveolar injury and failure to properly repair the respiratory epithelium ... ...

Abstract	Idiopathic pulmonary fibrosis (IPF) consists of fibrotic alveolar remodeling and progressive loss of pulmonary function. Genetic and experimental evidence indicates that chronic alveolar injury and failure to properly repair the respiratory epithelium are intrinsic to IPF pathogenesis. Loss of alveolar type 2 (AT2) stem cells or mutations that either impair their self-renewal and/or impair their differentiation into AT1 cells can serve as a trigger of pulmonary fibrosis. Recent reports indicate increased YAP activity in respiratory epithelial cells in IPF lungs. Individual IPF epithelial cells with aberrant YAP activation in bronchiolized regions frequently co-express AT1, AT2, conducting airway selective markers and even mesenchymal or EMT markers, demonstrating 'indeterminate' states of differentiation and suggesting that aberrant YAP signaling might promote pulmonary fibrosis. Yet, Yap and Taz have recently also been shown to be important for AT1 cell maintenance and alveolar epithelial regeneration after
MeSH term(s)	Humans ; Hippo Signaling Pathway ; Lung/pathology ; Adaptor Proteins, Signal Transducing/genetics ; Adaptor Proteins, Signal Transducing/metabolism ; Idiopathic Pulmonary Fibrosis/metabolism ; Idiopathic Pulmonary Fibrosis/pathology ; Transcription Factors/metabolism ; Intracellular Signaling Peptides and Proteins/metabolism ; Bleomycin/toxicity ; Bleomycin/metabolism
Chemical Substances	Adaptor Proteins, Signal Transducing ; Transcription Factors ; Intracellular Signaling Peptides and Proteins ; Bleomycin (11056-06-7)
Language	English
Publishing date	2023-05-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.85092
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Article ; Online: Niche-mediated repair of airways is directed in an occupant-dependent manner.

Lyu, Handeng / Warren, Rachel / Gao, Shan / Klinkhammer, Kylie / Yuan, Tingting / Zhang, Jin-San / Brownfield, Douglas / Li, Xiaokun / De Langhe, Stijn P

Cell reports

2022 Volume 41, Issue 12, Page(s) 111863

Abstract: In injured airways of the adult lung, epithelial progenitors are called upon to repair by nearby mesenchymal cells via signals transmitted through the niche. Currently, it is unclear whether repair is coordinated by the mesenchymal cells that maintain ... ...

Abstract	In injured airways of the adult lung, epithelial progenitors are called upon to repair by nearby mesenchymal cells via signals transmitted through the niche. Currently, it is unclear whether repair is coordinated by the mesenchymal cells that maintain the niche or by the airway epithelial cells that occupy it. Here, we show that the spatiotemporal expression of Fgf10 by the niche is primarily orchestrated by the niche's epithelial occupants-both those that reside prior to, and following, injury. During homeostasis, differentiated airway epithelial cells secrete Sonic hedgehog (Shh) to inhibit Fgf10 expression by Gli1
MeSH term(s)	Hedgehog Proteins/metabolism ; Lung/metabolism ; Cell Differentiation ; Epithelial Cells/metabolism ; Mesenchymal Stem Cells/metabolism ; Zinc Finger Protein GLI1/metabolism
Chemical Substances	Hedgehog Proteins ; Zinc Finger Protein GLI1
Language	English
Publishing date	2022-11-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2022.111863
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Article: Temporospatial Expression of Fgfr1 and 2 During Lung Development, Homeostasis, and Regeneration.

Yuan, Tingting / Klinkhammer, Kylie / Lyu, Handeng / Gao, Shan / Yuan, Jie / Hopkins, Seantel / Zhang, Jin-San / De Langhe, Stijn P

Frontiers in pharmacology

2020 Volume 11, Page(s) 120

Abstract: Fgfr1 (Fibroblast growth factor receptor 1) and Fgfr2 are dynamically expressed during lung development, homeostasis, and regeneration. Our current analysis indicates that Fgfr2 is expressed in distal epithelial progenitors AT2, AT1, club, and basal ... ...

Abstract	Fgfr1 (Fibroblast growth factor receptor 1) and Fgfr2 are dynamically expressed during lung development, homeostasis, and regeneration. Our current analysis indicates that Fgfr2 is expressed in distal epithelial progenitors AT2, AT1, club, and basal cells but not in ciliated or neuroendocrine cells during lung development and homeostasis. However, after injury, Fgfr2 becomes upregulated in neuroendocrine cells and distal club cells. Epithelial Fgfr1 expression is minimal throughout lung development, homeostasis, and regeneration. We further find both Fgfr1 and Fgfr2 strongly expressed in cartilage progenitors and airway smooth muscle cells during lung development, whereas Fgfr1 but not Fgfr2 was expressed in lipofibroblasts and vascular smooth muscle cells. In the adult lung, Fgfr1 and Fgfr2 were mostly downregulated in smooth muscle cells but became upregulated after injury. Fgfr1 remained expressed in mesenchymal alveolar niche cells or lipofibroblasts with lower levels of expression in their descendant (alveolar) myofibroblasts during alveologenesis.
Language	English
Publishing date	2020-03-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587355-6
ISSN	1663-9812
ISSN	1663-9812
DOI	10.3389/fphar.2020.00120
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Article: Fgf10 Signaling in Lung Development, Homeostasis, Disease, and Repair After Injury.

Yuan, Tingting / Volckaert, Thomas / Chanda, Diptiman / Thannickal, Victor J / De Langhe, Stijn P

Frontiers in genetics

2018 Volume 9, Page(s) 418

Abstract: The lung is morphologically structured into a complex tree-like network with branched airways ending distally in a large number of alveoli for efficient oxygen exchange. At the cellular level, the adult lung consists of at least 40-60 different cell ... ...

Abstract	The lung is morphologically structured into a complex tree-like network with branched airways ending distally in a large number of alveoli for efficient oxygen exchange. At the cellular level, the adult lung consists of at least 40-60 different cell types which can be broadly classified into epithelial, endothelial, mesenchymal, and immune cells. Fibroblast growth factor 10 (Fgf10) located in the lung mesenchyme is essential to regulate epithelial proliferation and lineage commitment during embryonic development and post-natal life, and to drive epithelial regeneration after injury. The cells that express
Language	English
Publishing date	2018-09-25
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2606823-0
ISSN	1664-8021
ISSN	1664-8021
DOI	10.3389/fgene.2018.00418
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Article ; Online: Wnt and FGF mediated epithelial-mesenchymal crosstalk during lung development.

Volckaert, Thomas / De Langhe, Stijn P

Developmental dynamics : an official publication of the American Association of Anatomists

2015 Volume 244, Issue 3, Page(s) 342–366

Abstract: Background: The adaptation to terrestrial life required the development of an organ capable of efficient air-blood gas exchange. To meet the metabolic load of cellular respiration, the mammalian respiratory system has evolved from a relatively simple ... ...

Abstract	Background: The adaptation to terrestrial life required the development of an organ capable of efficient air-blood gas exchange. To meet the metabolic load of cellular respiration, the mammalian respiratory system has evolved from a relatively simple structure, similar to the two-tube amphibian lung, to a highly complex tree-like system of branched epithelial airways connected to a vast network of gas exchanging units called alveoli. The development of such an elaborate organ in a relatively short time window is therefore an extraordinary feat and involves an intimate crosstalk between mesodermal and endodermal cell lineages. Results: This review describes the molecular processes governing lung development with an emphasis on the current knowledge on the role of Wnt and FGF signaling in lung epithelial differentiation. Conclusions: The Wnt and FGF signaling pathways are crucial for the dynamic and reciprocal communication between epithelium and mesenchyme during lung development. In addition, some of this developmental crosstalk is reemployed in the adult lung after injury to drive regeneration, and may, when aberrantly or chronically activated, result in chronic lung diseases. Novel insights into how the Wnt and FGF pathways interact and are integrated into a complex gene regulatory network will not only provide us with essential information about how the lung regenerates itself, but also enhance our understanding of the pathogenesis of chronic lung diseases, as well as improve the controlled differentiation of lung epithelium from pluripotent stem cells.
MeSH term(s)	Animals ; Cell Lineage/physiology ; Epithelial-Mesenchymal Transition/physiology ; Fibroblast Growth Factors/metabolism ; Humans ; Lung/cytology ; Lung/embryology ; Wnt Proteins/metabolism ; Wnt Signaling Pathway/physiology
Chemical Substances	Wnt Proteins ; Fibroblast Growth Factors (62031-54-3)
Language	English
Publishing date	2015-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.24234
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Article ; Online: Developmental pathways in the pathogenesis of lung fibrosis.

Chanda, Diptiman / Otoupalova, Eva / Smith, Samuel R / Volckaert, Thomas / De Langhe, Stijn P / Thannickal, Victor J

Molecular aspects of medicine

2018 Volume 65, Page(s) 56–69

Abstract: Idiopathic pulmonary fibrosis (IPF) is a progressive and terminal lung disease with no known cure. IPF is a disease of aging, with median age of diagnosis over 65 years. Median survival is between 3 and 5 years after diagnosis. IPF is characterized ... ...

Abstract	Idiopathic pulmonary fibrosis (IPF) is a progressive and terminal lung disease with no known cure. IPF is a disease of aging, with median age of diagnosis over 65 years. Median survival is between 3 and 5 years after diagnosis. IPF is characterized primarily by excessive deposition of extracellular matrix (ECM) proteins by activated lung fibroblasts and myofibroblasts, resulting in reduced gas exchange and impaired pulmonary function. Growing evidence supports the concept of a pro-fibrotic environment orchestrated by underlying factors such as genetic predisposition, chronic injury and aging, oxidative stress, and impaired regenerative responses may account for disease development and persistence. Currently, two FDA approved drugs have limited efficacy in the treatment of IPF. Many of the genes and gene networks associated with lung development are induced or activated in IPF. In this review, we analyze current knowledge in the field, gained from both basic and clinical research, to provide new insights into the disease process, and potential approaches to treatment of pulmonary fibrosis.
MeSH term(s)	Animals ; Biomarkers ; Cellular Microenvironment ; Disease Susceptibility ; Homeodomain Proteins/metabolism ; Humans ; Myofibroblasts/metabolism ; Pulmonary Fibrosis/etiology ; Pulmonary Fibrosis/metabolism ; Pulmonary Fibrosis/pathology ; Signal Transduction ; Stromal Cells ; Trans-Activators ; Transforming Growth Factor beta/metabolism
Chemical Substances	Biomarkers ; Homeodomain Proteins ; Trans-Activators ; Transforming Growth Factor beta ; pancreatic and duodenal homeobox 1 protein
Language	English
Publishing date	2018-08-23
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	197640-0
ISSN	1872-9452 ; 0098-2997
ISSN (online)	1872-9452
ISSN	0098-2997
DOI	10.1016/j.mam.2018.08.004
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Article ; Online: Hippo signaling promotes lung epithelial lineage commitment by curbing Fgf10 and β-catenin signaling.

Volckaert, Thomas / Yuan, Tingting / Yuan, Jie / Boateng, Eistine / Hopkins, Seantel / Zhang, Jin-San / Thannickal, Victor J / Fässler, Reinhard / De Langhe, Stijn P

Development (Cambridge, England)

2019 Volume 146, Issue 2

Abstract: Organ growth and tissue homeostasis rely on the proliferation and differentiation of progenitor cell populations. In the developing lung, ... ...

Abstract	Organ growth and tissue homeostasis rely on the proliferation and differentiation of progenitor cell populations. In the developing lung, localized
MeSH term(s)	Adaptor Proteins, Signal Transducing/metabolism ; Animals ; Cell Cycle Proteins ; Cell Differentiation ; Cell Lineage ; Cytoplasm/metabolism ; Epithelial Cells/cytology ; Epithelial Cells/metabolism ; Female ; Fibroblast Growth Factor 10/metabolism ; Lung/cytology ; Lung/embryology ; Male ; Mice ; Models, Biological ; Organogenesis ; Phenotype ; Phosphoproteins/metabolism ; Protein-Serine-Threonine Kinases/metabolism ; Pulmonary Alveoli/embryology ; Signal Transduction ; Trans-Activators ; beta Catenin/metabolism
Chemical Substances	Adaptor Proteins, Signal Transducing ; Cell Cycle Proteins ; Fgf10 protein, mouse ; Fibroblast Growth Factor 10 ; Phosphoproteins ; Trans-Activators ; Wwtr1 protein, mouse ; Yap1 protein, mouse ; beta Catenin ; integrin-linked kinase (EC 2.7.1.-) ; Hippo protein, mouse (EC 2.7.11.1) ; Protein-Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2019-01-16
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.166454
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Article: Wnt signaling in lung organogenesis.

De Langhe, Stijn P / Reynolds, Susan D

Organogenesis

2009 Volume 4, Issue 2, Page(s) 100–108

Abstract: Reporter transgene, knockout, and misexpression studies support the notion that Wnt/beta-catenin signaling regulates aspects of branching morphogenesis, regional specialization of the epithelium and mesenchyme, and establishment of progenitor cell pools. ...

Abstract	Reporter transgene, knockout, and misexpression studies support the notion that Wnt/beta-catenin signaling regulates aspects of branching morphogenesis, regional specialization of the epithelium and mesenchyme, and establishment of progenitor cell pools. As demonstrated for other foregut endoderm-derived organs, beta-catenin and the Wnt/beta-catenin signaling pathway contribute to control of cellular proliferation, differentiation and migration. However, the contribution of Wnt/beta-catenin signaling to these processes is shaped by other signals impinging on target tissues. In this review, we will concentrate on roles for Wnt/beta-catenin in respiratory system development, including segregation of the conducting airway and alveolar compartments, specialization of the mesenchyme, and establishment of tracheal asymmetries and tracheal glands.
Language	English
Publishing date	2009-03-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	2159583-5
ISSN	1555-8592 ; 1547-6278
ISSN (online)	1555-8592
ISSN	1547-6278
DOI	10.4161/org.4.2.5856
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Article ; Online: FGF10-FGFR2B Signaling Generates Basal Cells and Drives Alveolar Epithelial Regeneration by Bronchial Epithelial Stem Cells after Lung Injury.

Yuan, Tingting / Volckaert, Thomas / Redente, Elizabeth F / Hopkins, Seantel / Klinkhammer, Kylie / Wasnick, Roxana / Chao, Cho-Ming / Yuan, Jie / Zhang, Jin-San / Yao, Changfu / Majka, Susan / Stripp, Barry R / Günther, Andreas / Riches, David W H / Bellusci, Saverio / Thannickal, Victor J / De Langhe, Stijn P

Stem cell reports

2019 Volume 12, Issue 5, Page(s) 1041–1055

Abstract: Idiopathic pulmonary fibrosis is a common form of interstitial lung disease resulting in alveolar remodeling and progressive loss of pulmonary function because of chronic alveolar injury and failure to regenerate the respiratory epithelium. ... ...

Abstract	Idiopathic pulmonary fibrosis is a common form of interstitial lung disease resulting in alveolar remodeling and progressive loss of pulmonary function because of chronic alveolar injury and failure to regenerate the respiratory epithelium. Histologically, fibrotic lesions and honeycomb structures expressing atypical proximal airway epithelial markers replace alveolar structures, the latter normally lined by alveolar type 1 (AT1) and AT2 cells. Bronchial epithelial stem cells (BESCs) can give rise to AT2 and AT1 cells or honeycomb cysts following bleomycin-mediated lung injury. However, little is known about what controls this binary decision or whether this decision can be reversed. Here we report that inactivation of Fgfr2b in BESCs impairs their contribution to both alveolar epithelial regeneration and honeycomb cysts after bleomycin injury. By contrast overexpression of Fgf10 in BESCs enhances fibrosis resolution by favoring the more desirable outcome of alveolar epithelial regeneration over the development of pathologic honeycomb cysts.
MeSH term(s)	Alveolar Epithelial Cells/cytology ; Alveolar Epithelial Cells/metabolism ; Animals ; Bleomycin ; Cell Line ; Female ; Fibroblast Growth Factor 10/genetics ; Fibroblast Growth Factor 10/metabolism ; Humans ; Lung Injury/chemically induced ; Lung Injury/genetics ; Lung Injury/metabolism ; Male ; Mice, Knockout ; Mice, Transgenic ; Receptor, Fibroblast Growth Factor, Type 2/genetics ; Receptor, Fibroblast Growth Factor, Type 2/metabolism ; Regeneration/genetics ; Respiratory Mucosa/cytology ; Respiratory Mucosa/metabolism ; Respiratory Mucosa/physiology ; Signal Transduction/genetics ; Stem Cells/cytology ; Stem Cells/metabolism
Chemical Substances	Fgf10 protein, mouse ; Fibroblast Growth Factor 10 ; Bleomycin (11056-06-7) ; Receptor, Fibroblast Growth Factor, Type 2 (EC 2.7.10.1)
Language	English
Publishing date	2019-05-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2019.04.003
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Article ; Online: Fgf10-Hippo Epithelial-Mesenchymal Crosstalk Maintains and Recruits Lung Basal Stem Cells.

Volckaert, Thomas / Yuan, Tingting / Chao, Cho-Ming / Bell, Harold / Sitaula, Alina / Szimmtenings, Luisa / El Agha, Elie / Chanda, Diptiman / Majka, Susan / Bellusci, Saverio / Thannickal, Victor J / Fässler, Reinhard / De Langhe, Stijn P

Developmental cell

2017 Volume 43, Issue 1, Page(s) 48–59.e5

Abstract: The lung harbors its basal stem/progenitor cells (BSCs) in the protected environment of the cartilaginous airways. After major lung injuries, BSCs are activated and recruited to sites of injury. Here, we show that during homeostasis, BSCs in ... ...

Abstract	The lung harbors its basal stem/progenitor cells (BSCs) in the protected environment of the cartilaginous airways. After major lung injuries, BSCs are activated and recruited to sites of injury. Here, we show that during homeostasis, BSCs in cartilaginous airways maintain their stem cell state by downregulating the Hippo pathway (resulting in increased nuclear Yap), which generates a localized Fgf10-expressing stromal niche; in contrast, differentiated epithelial cells in non-cartilaginous airways maintain quiescence by activating the Hippo pathway and inhibiting Fgf10 expression in airway smooth muscle cells (ASMCs). However, upon injury, surviving differentiated epithelial cells spread to maintain barrier function and recruit integrin-linked kinase to adhesion sites, which leads to Merlin degradation, downregulation of the Hippo pathway, nuclear Yap translocation, and expression and secretion of Wnt7b. Epithelial-derived Wnt7b, then in turn, induces Fgf10 expression in ASMCs, which extends the BSC niche to promote regeneration.
MeSH term(s)	Adaptor Proteins, Signal Transducing/metabolism ; Animals ; Cell Differentiation/physiology ; Epithelial Cells/cytology ; Fibroblast Growth Factor 10/metabolism ; Lung/metabolism ; Mice, Transgenic ; Myocytes, Smooth Muscle/cytology ; Phosphoproteins/metabolism ; Protein-Serine-Threonine Kinases/metabolism ; Regeneration/physiology ; Stem Cells/cytology
Chemical Substances	Adaptor Proteins, Signal Transducing ; Fgf10 protein, mouse ; Fibroblast Growth Factor 10 ; Phosphoproteins ; integrin-linked kinase (EC 2.7.1.-) ; Hippo protein, mouse (EC 2.7.11.1) ; Protein-Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2017-10-18
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2017.09.003
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