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Article ; Online: Using Avian Skin Explants to Study Tissue Patterning and Organogenesis.

Jiang, Tingxin / Secor, Maeve / Lansford, Rusty / Widelitz, Randall B / Chuong, Cheng Ming

Journal of visualized experiments : JoVE

2023 , Issue 199

Abstract: The developing avian skin during embryogenesis is a unique model that can provide valuable insights into tissue patterning. Here three variations on skin explant cultures to examine different aspects of skin development are described. First, ex vivo ... ...

Abstract	The developing avian skin during embryogenesis is a unique model that can provide valuable insights into tissue patterning. Here three variations on skin explant cultures to examine different aspects of skin development are described. First, ex vivo organ cultures and manipulations offer researchers opportunities to observe and study the development of feather buds directly. Skin explant culture can grow for 7 days enabling direct analysis of cellular behavior and 4D imaging at intervals during this growth period. This also allows for physical and molecular manipulations of culture conditions to visualize tissue response. For example, growth factor-coated beads can be applied locally to induce changes in feather patterning in a limited area. Alternatively, viral transduction can be delivered globally in the culture media to up or downregulate gene expression. Second, the skin recombination protocol allows researchers to investigate tissue interactions between the epidermis and mesenchyme that are derived from different skin regions, different life stages, or different species. This affords an opportunity to test the time window in which the epithelium is competent to respond to signals and its ability to form different skin appendages in response to signals from different mesenchymal sources. Third, skin reconstitution using dissociated dermal cells overlaid with intact epithelium resets skin development and enables the study of the initial processes of periodic patterning. This approach also enhances our ability to manipulate gene expression among the dissociated cells before creating the reconstituted skin explant. This paper provides the three culture protocols and exemplary experiments to demonstrate their utility.
MeSH term(s)	Animals ; Skin ; Epithelium/metabolism ; Feathers ; Organogenesis
Language	English
Publishing date	2023-09-15
Publishing country	United States
Document type	Journal Article ; Video-Audio Media ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/65580
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Gap junctions in Turing-type periodic feather pattern formation.

Tseng, Chun-Chih / Woolley, Thomas E / Jiang, Ting-Xin / Wu, Ping / Maini, Philip K / Widelitz, Randall B / Cheng-Ming, Chuong

PLoS biology

2024 Volume 22, Issue 5, Page(s) e3002636

Abstract: Periodic patterning requires coordinated cell-cell interactions at the tissue level. Turing showed, using mathematical modeling, how spatial patterns could arise from the reactions of a diffusive activator-inhibitor pair in an initially homogenous 2D ... ...

Abstract	Periodic patterning requires coordinated cell-cell interactions at the tissue level. Turing showed, using mathematical modeling, how spatial patterns could arise from the reactions of a diffusive activator-inhibitor pair in an initially homogenous 2D field. Most activators and inhibitors studied in biological systems are proteins, and the roles of cell-cell interaction, ions, bioelectricity, etc. are only now being identified. Gap junctions (GJs) mediate direct exchanges of ions or small molecules between cells, enabling rapid long-distance communications in a cell collective. They are therefore good candidates for propagating nonprotein-based patterning signals that may act according to the Turing principles. Here, we explore the possible roles of GJs in Turing-type patterning using feather pattern formation as a model. We found 7 of the 12 investigated GJ isoforms are highly dynamically expressed in the developing chicken skin. In ovo functional perturbations of the GJ isoform, connexin 30, by siRNA and the dominant-negative mutant applied before placode development led to disrupted primary feather bud formation. Interestingly, inhibition of gap junctional intercellular communication (GJIC) in the ex vivo skin explant culture allowed the sequential emergence of new feather buds at specific spatial locations relative to the existing primary buds. The results suggest that GJIC may facilitate the propagation of long-distance inhibitory signals. Thus, inhibition of GJs may stimulate Turing-type periodic feather pattern formation during chick skin development, and the removal of GJ activity would enable the emergence of new feather buds if the local environment were competent and the threshold to form buds was reached. We further propose Turing-based computational simulations that can predict the sequential appearance of these ectopic buds. Our models demonstrate how a Turing activator-inhibitor system can continue to generate patterns in the competent morphogenetic field when the level of intercellular communication at the tissue scale is modulated.
Language	English
Publishing date	2024-05-14
Publishing country	United States
Document type	Journal Article
ZDB-ID	2126776-5
ISSN	1545-7885 ; 1544-9173
ISSN (online)	1545-7885
ISSN	1544-9173
DOI	10.1371/journal.pbio.3002636
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Article: Gap junctions in Turing-type periodic feather pattern formation.

Tseng, Chun-Chih / Woolley, Thomas E / Jiang, Ting-Xin / Wu, Ping / Maini, Philip K / Widelitz, Randall B / Chuong, Cheng-Ming

bioRxiv : the preprint server for biology

2023

Abstract	Periodic patterning requires coordinated cell-cell interactions at the tissue level. Turing showed, using mathematical modeling, how spatial patterns could arise from the reactions of a diffusive activator-inhibitor pair in an initially homogenous two-dimensional field. Most activators and inhibitors studied in biological systems are proteins, and the roles of cell-cell interaction, ions, bioelectricity, etc. are only now being identified. Gap junctions (GJs) mediate direct exchanges of ions or small molecules between cells, enabling rapid long-distance communications in a cell collective. They are therefore good candidates for propagating non-protein-based patterning signals that may act according to the Turing principles. Here, we explore the possible roles of GJs in Turing-type patterning using feather pattern formation as a model. We found seven of the twelve investigated GJ isoforms are highly dynamically expressed in the developing chicken skin.
Language	English
Publishing date	2023-04-16
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.04.15.537019
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Article ; Online: Adaptive patterning of vascular network during avian skin development: Mesenchymal plasticity and dermal vasculogenesis.

Ou, Kuang-Ling / Chen, Chih-Kuan / Huang, Junxiang J / Chang, William Weijen / Hsieh Li, Shu-Man / Jiang, Ting-Xin / Widelitz, Randall B / Lansford, Rusty / Chuong, Cheng-Ming

Cells & development

2024 , Page(s) 203922

Abstract: A vasculature network supplies blood to feather buds in the developing skin. Does the vasculature network during early skin development form by sequential sprouting from the central vasculature or does local vasculogenesis occur first that then connect ... ...

Abstract	A vasculature network supplies blood to feather buds in the developing skin. Does the vasculature network during early skin development form by sequential sprouting from the central vasculature or does local vasculogenesis occur first that then connect with the central vascular tree? Using transgenic Japanese quail Tg(TIE1p.H2B-eYFP), we observe that vascular progenitor cells appear after feather primordia formation. The vasculature then radiates out from each bud and connects with primordial vessels from neighboring buds. Later they connect with the central vasculature. Epithelial-mesenchymal recombination shows local vasculature is patterned by the epithelium, which expresses FGF2 and VEGF. Perturbing noggin expression leads to abnormal vascularization. To study endothelial origin, we compare transcriptomes of TIE1p.H2B-eYFP
Language	English
Publishing date	2024-04-28
Publishing country	Netherlands
Document type	Journal Article
ISSN	2667-2901
ISSN (online)	2667-2901
DOI	10.1016/j.cdev.2024.203922
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Article: Regional Specific Differentiation of Integumentary Organs: Regulation of Gene Clusters within the Avian Epidermal Differentiation Complex and Impacts of SATB2 Overexpression

Lin, Gee-Way / Lai, Yung-Chih / Liang, Ya-Chen / Widelitz, Randall B. / Wu, Ping / Chuong, Cheng-Ming

Genes. 2021 Aug. 23, v. 12, no. 8

2021

Abstract: The epidermal differentiation complex (EDC) encodes a group of unique proteins expressed in late epidermal differentiation. The EDC gave integuments new physicochemical properties and is critical in evolution. Recently, we showed β-keratins, members of ... ...

Abstract	The epidermal differentiation complex (EDC) encodes a group of unique proteins expressed in late epidermal differentiation. The EDC gave integuments new physicochemical properties and is critical in evolution. Recently, we showed β-keratins, members of the EDC, undergo gene cluster switching with overexpression of SATB2 (Special AT-rich binding protein-2), considered a chromatin regulator. We wondered whether this unique regulatory mechanism is specific to β-keratins or may be derived from and common to EDC members. Here we explore (1) the systematic expression patterns of non-β-keratin EDC genes and their preferential expression in different skin appendages during development, (2) whether the expression of non-β-keratin EDC sub-clusters are also regulated in clusters by SATB2. We analyzed bulk RNA-seq and ChIP-seq data and also evaluated the disrupted expression patterns caused by overexpressing SATB2. The results show that the expression of whole EDDA and EDQM sub-clusters are possibly mediated by enhancers in E14-feathers. Overexpressing SATB2 down-regulates the enriched EDCRP sub-cluster in feathers and the EDCH sub-cluster in beaks. These results reveal the potential of complex epigenetic regulation activities within the avian EDC, implying transcriptional regulation of EDC members acting at the gene and/or gene cluster level in a temporal and skin regional-specific fashion, which may contribute to the evolution of diverse avian integuments.
Keywords	birds ; chromatin ; chromatin immunoprecipitation ; epigenetics ; evolution ; multigene family ; sequence analysis ; transcription (genetics)
Language	English
Dates of publication	2021-0823
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2527218-4
ISSN	2073-4425
ISSN	2073-4425
DOI	10.3390/genes12081291
Database	NAL-Catalogue (AGRICOLA)

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Article: Wnt signaling in skin organogenesis.

Widelitz, Randall B

Organogenesis

2009 Volume 4, Issue 2, Page(s) 123–133

Abstract: While serving as the interface between an organism and its environment, the skin also can elaborate a wide range of skin appendages to service specific purposes in a region-specific fashion. As in other organs, Wnt signaling plays a key role in ... ...

Abstract	While serving as the interface between an organism and its environment, the skin also can elaborate a wide range of skin appendages to service specific purposes in a region-specific fashion. As in other organs, Wnt signaling plays a key role in regulating the proliferation, differentiation and motility of skin cells during their morphogenesis. Here I will review some of the recent work that has been done on skin organogenesis. I will cover dermis formation, the development of skin appendages, cycling of appendages in the adult, stem cell regulation, patterning, orientation, regional specificity and modulation by sex hormone nuclear receptors. I will also cover their roles in wound healing, hair regeneration and skin related diseases. It appears that Wnt signaling plays essential but distinct roles in different hierarchical levels of morphogenesis and organogenesis. Many of these areas have not yet been fully explored but are certainly promising areas of future research.
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.4.2.5859
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Epidermal-dermal coupled spheroids are important for tissue pattern regeneration in reconstituted skin explant cultures.

Lei, Mingxing / Jiang, Jingwei / Wang, Mengyue / Wu, Wang / Zhang, Jinwei / Liu, Wanqian / Zhou, Wei / Lai, Yung-Chih / Jiang, Ting-Xin / Widelitz, Randall B / Harn, Hans I-Chen / Yang, Li / Chuong, Cheng-Ming

NPJ Regenerative medicine

2023 Volume 8, Issue 1, Page(s) 65

Abstract: Tissue patterning is critical for the development and regeneration of organs. To advance the use of engineered reconstituted skin organs, we study cardinal features important for tissue patterning and hair regeneration. We find they spontaneously form ... ...

Abstract	Tissue patterning is critical for the development and regeneration of organs. To advance the use of engineered reconstituted skin organs, we study cardinal features important for tissue patterning and hair regeneration. We find they spontaneously form spheroid configurations, with polarized epidermal cells coupled with dermal cells through a newly formed basement membrane. Functionally, the spheroid becomes competent morphogenetic units (CMU) that promote regeneration of tissue patterns. The emergence of new cell types and molecular interactions during CMU formation was analyzed using scRNA-sequencing. Surprisingly, in newborn skin explants, IFNr signaling can induce apical-basal polarity in epidermal cell aggregates. Dermal-Tgfb induces basement membrane formation. Meanwhile, VEGF signaling mediates dermal cell attachment to the epidermal cyst shell, thus forming a CMU. Adult mouse and human fetal scalp cells fail to form a CMU but can be restored by adding IFNr or VEGF to achieve hair regeneration. We find different multi-cellular configurations and molecular pathways are used to achieve morphogenetic competence in developing skin, wound-induced hair neogenesis, and reconstituted explant cultures. Thus, multiple paths can be used to achieve tissue patterning. These insights encourage more studies of "in vitro morphogenesis" which may provide novel strategies to enhance regeneration.
Language	English
Publishing date	2023-11-23
Publishing country	United States
Document type	Journal Article
ISSN	2057-3995
ISSN (online)	2057-3995
DOI	10.1038/s41536-023-00340-0
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Systems Biology Analyses in Chicken: Workflow for Transcriptome and ChIP-Seq Analyses Using the Chicken Skin Paradigm.

Lai, Yung-Chih / Widelitz, Randall B / Chuong, Cheng-Ming

Methods in molecular biology (Clifton, N.J.)

2017 Volume 1650, Page(s) 87–100

Abstract: With advances in molecular biology, various biological phenomena can now be explored at higher resolution using mRNA sequencing (RNA-Seq) and chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-Seq), two powerful high-throughput ... ...

Abstract	With advances in molecular biology, various biological phenomena can now be explored at higher resolution using mRNA sequencing (RNA-Seq) and chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-Seq), two powerful high-throughput next-generation sequencing (NGS) technologies. While methods are used widely in mouse, human, etc., less information is available in other animals, such as the chicken. Here we assemble a workflow of the RNA-Seq and ChIP-Seq analyses for the chicken studies using chicken skin appendage tissue as an example. We present guidelines for RNA-Seq quality control, alignment, quantification, normalization, and differentially expressed gene analysis. In the meantime, we outline a bioinformatics pipeline for ChIP-Seq quality control, alignment, peak calling, super-enhancer identification, and differential enrichment analysis.
MeSH term(s)	Animals ; Chickens ; Chromatin Immunoprecipitation/methods ; High-Throughput Nucleotide Sequencing/methods ; Quality Control ; Regulatory Sequences, Nucleic Acid ; Sequence Analysis, DNA/methods ; Sequence Analysis, RNA/methods ; Skin/metabolism ; Software ; Systems Biology/methods ; Transcriptome ; Workflow
Language	English
Publishing date	2017-07-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-7216-6_5
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Integrating Bioelectrical Currents and Ca

Li, Ang / Zhou, Jingsong / Widelitz, Randall B / Chow, Robert H / Chuong, Cheng-Ming

Bioelectricity

2020 Volume 2, Issue 3, Page(s) 210–220

Abstract: Roles of bioelectrical signals are increasingly recognized in excitable and nonexcitable non-neural tissues. Diverse ion-selective channels, pumps, and gap junctions participate in bioelectrical signaling, including those transporting calcium ions ( ... ...

Abstract	Roles of bioelectrical signals are increasingly recognized in excitable and nonexcitable non-neural tissues. Diverse ion-selective channels, pumps, and gap junctions participate in bioelectrical signaling, including those transporting calcium ions (Ca
Language	English
Publishing date	2020-09-16
Publishing country	United States
Document type	Journal Article ; Review
ISSN	2576-3113
ISSN (online)	2576-3113
DOI	10.1089/bioe.2020.0001
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Regional Specific Differentiation of Integumentary Organs: Regulation of Gene Clusters within the Avian Epidermal Differentiation Complex and Impacts of SATB2 Overexpression.

Lin, Gee-Way / Lai, Yung-Chih / Liang, Ya-Chen / Widelitz, Randall B / Wu, Ping / Chuong, Cheng-Ming

Genes

2021 Volume 12, Issue 8

Abstract	The epidermal differentiation complex (EDC) encodes a group of unique proteins expressed in late epidermal differentiation. The EDC gave integuments new physicochemical properties and is critical in evolution. Recently, we showed β-keratins, members of the EDC, undergo gene cluster switching with overexpression of SATB2 (Special AT-rich binding protein-2), considered a chromatin regulator. We wondered whether this unique regulatory mechanism is specific to β-keratins or may be derived from and common to EDC members. Here we explore (1) the systematic expression patterns of non-β-keratin EDC genes and their preferential expression in different skin appendages during development, (2) whether the expression of non-β-keratin EDC sub-clusters are also regulated in clusters by SATB2. We analyzed bulk RNA-seq and ChIP-seq data and also evaluated the disrupted expression patterns caused by overexpressing SATB2. The results show that the expression of whole EDDA and EDQM sub-clusters are possibly mediated by enhancers in E14-feathers. Overexpressing SATB2 down-regulates the enriched EDCRP sub-cluster in feathers and the EDCH sub-cluster in beaks. These results reveal the potential of complex epigenetic regulation activities within the avian EDC, implying transcriptional regulation of EDC members acting at the gene and/or gene cluster level in a temporal and skin regional-specific fashion, which may contribute to the evolution of diverse avian integuments.
MeSH term(s)	Animals ; Avian Proteins/genetics ; Birds/genetics ; Birds/growth & development ; Cell Differentiation/genetics ; Chromosomes/genetics ; Epidermis/growth & development ; Epidermis/metabolism ; Epigenesis, Genetic/genetics ; Evolution, Molecular ; Feathers/growth & development ; Gene Expression Regulation, Developmental/genetics ; Humans ; Integumentary System/growth & development ; Matrix Attachment Region Binding Proteins/genetics ; Skin/growth & development ; Skin/metabolism ; Transcription Factors/genetics ; beta-Keratins/genetics
Chemical Substances	Avian Proteins ; Matrix Attachment Region Binding Proteins ; SATB2 protein, human ; Transcription Factors ; beta-Keratins
Language	English
Publishing date	2021-08-23
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes12081291
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