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  1. Article ; Online: The "tao" of integuments.

    Lai, Yung Chih / Chuong, Cheng-Ming

    Science (New York, N.Y.)

    2016  Volume 354, Issue 6319, Page(s) 1533–1534

    MeSH term(s) Adaptation, Physiological ; Animals ; Biological Evolution ; Bone Morphogenetic Proteins/metabolism ; Hair Follicle/embryology ; Hair Follicle/metabolism ; Hedgehog Proteins/metabolism ; Morphogenesis ; Mouth/embryology ; Signal Transduction ; Stem Cells/cytology ; Sweat Glands/embryology ; Tooth/embryology ; Whales
    Chemical Substances Bone Morphogenetic Proteins ; Hedgehog Proteins
    Language English
    Publishing date 2016--23
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 128410-1
    ISSN 1095-9203 ; 0036-8075
    ISSN (online) 1095-9203
    ISSN 0036-8075
    DOI 10.1126/science.aal4572
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  2. 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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  3. 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
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  4. Article: Human Fetal Scalp Dermal Papilla Enriched Genes and the Role of R-Spondin-1 in the Restoration of Hair Neogenesis in Adult Mouse Cells.

    Weber, Erin L / Lai, Yung-Chih / Lei, Mingxing / Jiang, Ting-Xin / Chuong, Cheng-Ming

    Frontiers in cell and developmental biology

    2020  Volume 8, Page(s) 583434

    Abstract: Much remains unknown about the regulatory networks which govern the dermal papilla's (DP) ability to induce hair follicle neogenesis, a capacity which decreases greatly with age. To further define the core genes which characterize the DP cell and to ... ...

    Abstract Much remains unknown about the regulatory networks which govern the dermal papilla's (DP) ability to induce hair follicle neogenesis, a capacity which decreases greatly with age. To further define the core genes which characterize the DP cell and to identify pathways prominent in DP cells with greater hair inductive capacity, comparative transcriptome analyses of human fetal and adult dermal follicular cells were performed. 121 genes were significantly upregulated in fetal DP cells in comparison to both fetal dermal sheath cup (DSC) cells and interfollicular dermal (IFD) populations. Comparison of the set of enriched human fetal DP genes with human adult DP, newborn mouse DP, and embryonic mouse dermal condensation (DC) cells revealed differences in the expression of Wnt/β-catenin, Shh, FGF, BMP, and Notch signaling pathways. We chose R-spondin-1, a Wnt agonist, for functional verification and show that exogenous administration restores hair follicle neogenesis from adult mouse cells in skin reconstitution assays. To explore upstream regulators of fetal DP gene expression, we identified twenty-nine transcription factors which are upregulated in human fetal DP cells compared to adult DP cells. Of these, seven transcription factor binding motifs were significantly enriched in the candidate promoter regions of genes differentially expressed between fetal and adult DP cells, suggesting a potential role in the regulatory network which confers the fetal DP phenotype and a possible relationship to the induction of follicle neogenesis.
    Language English
    Publishing date 2020-11-26
    Publishing country Switzerland
    Document type Journal Article
    ZDB-ID 2737824-X
    ISSN 2296-634X
    ISSN 2296-634X
    DOI 10.3389/fcell.2020.583434
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  5. 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
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  6. Article ; Online: Comprehensive molecular and cellular studies suggest avian scutate scales are secondarily derived from feathers, and more distant from reptilian scales.

    Wu, Ping / Lai, Yung-Chih / Widelitz, Randall / Chuong, Cheng-Ming

    Scientific reports

    2018  Volume 8, Issue 1, Page(s) 16766

    Abstract: Amniote skin appendages such as feathers, hairs and scales, provide thermoregulation, physical protection and display different color patterns to attract a mate or frighten an adversary. A long-standing question is whether "reptile scale" and "avian leg ... ...

    Abstract Amniote skin appendages such as feathers, hairs and scales, provide thermoregulation, physical protection and display different color patterns to attract a mate or frighten an adversary. A long-standing question is whether "reptile scale" and "avian leg scales" are of the same origin. Understanding the relation between avian feathers, avian scales and reptilian scales will enhance our understanding of skin appendage evolution. We compared the molecular and cellular profiles in chicken feather, chicken scales and alligator scales and found that chicken scutate scales are similar to chicken feathers in morphogenesis at the early placode stage. When we compared the expression of the recently identified feather-specific genes and scale-specific genes in these skin appendages, we found that at the molecular level alligator scales are significantly different from both chicken feathers and chicken scales. Furthermore, we identified a similarly diffuse putative stem cell niche in morphologically similar chicken and alligator scales. These putative stem cells participate in alligator scale regeneration. In contrast, avian feathers have a more condensed stem cell niche, which may be responsible for cycling. Thus, our results suggest that chicken and alligator scales formed independently through convergent evolution.
    MeSH term(s) Alligators and Crocodiles ; Animals ; Biological Evolution ; Biomarkers/metabolism ; Chick Embryo ; Chickens ; Diffusion ; Feathers/cytology ; Feathers/metabolism ; Gene Expression Regulation ; Sequence Analysis, RNA ; Skin/cytology ; Skin/metabolism ; Species Specificity ; Stem Cells/metabolism
    Chemical Substances Biomarkers
    Language English
    Publishing date 2018-11-13
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 2615211-3
    ISSN 2045-2322 ; 2045-2322
    ISSN (online) 2045-2322
    ISSN 2045-2322
    DOI 10.1038/s41598-018-35176-y
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  7. 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 ... ...

    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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  8. Article ; Online: Regional specific differentiation of integumentary organs: SATB2 is involved in α- and β-keratin gene cluster switching in the chicken.

    Lin, Gee-Way / Liang, Ya-Chen / Wu, Ping / Chen, Chih-Kuan / Lai, Yung-Chih / Jiang, Ting-Xin / Haung, Yen-Hua / Chuong, Cheng-Ming

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

    2021  Volume 251, Issue 9, Page(s) 1490–1508

    Abstract: Background: Animals develop skin regional specificities to best adapt to their environments. Birds are excellent models in which to study the epigenetic mechanisms that facilitate these adaptions. Patients suffering from SATB2 mutations exhibit multiple ...

    Abstract Background: Animals develop skin regional specificities to best adapt to their environments. Birds are excellent models in which to study the epigenetic mechanisms that facilitate these adaptions. Patients suffering from SATB2 mutations exhibit multiple defects including ectodermal dysplasia-like changes. The preferential expression of SATB2, a chromatin regulator, in feather-forming compared to scale-forming regions, suggests it functions in regional specification of chicken skin appendages by acting on either differentiation or morphogenesis.
    Results: Retrovirus mediated SATB2 misexpression in developing feathers, beaks, and claws causes epidermal differentiation abnormalities (e.g. knobs, plaques) with few organ morphology alterations. Chicken β-keratins are encoded in 5 sub-clusters (Claw, Feather, Feather-like, Scale, and Keratinocyte) on Chromosome 25 and a large Feather keratin cluster on Chromosome 27. Type I and II α-keratin clusters are located on Chromosomes 27 and 33, respectively. Transcriptome analyses showed these keratins (1) are often tuned up or down collectively as a sub-cluster, and (2) these changes occur in a temporo-spatial specific manner.
    Conclusions: These results suggest an organizing role of SATB2 in cluster-level gene co-regulation during skin regional specification.
    MeSH term(s) Animals ; Chickens/genetics ; Feathers/metabolism ; Keratins/genetics ; Keratins/metabolism ; Multigene Family ; beta-Keratins/genetics ; beta-Keratins/metabolism
    Chemical Substances beta-Keratins ; Keratins (68238-35-7)
    Language English
    Publishing date 2021-07-17
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 1102541-4
    ISSN 1097-0177 ; 1058-8388
    ISSN (online) 1097-0177
    ISSN 1058-8388
    DOI 10.1002/dvdy.396
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  9. Article ; Online: Gene Structure and Sequence Polymorphism of the Coat Color Gene,

    Lai, Yung-Chih / Huang, Shiao-Wei / Yu, Hon-Tsen

    Zoological studies

    2016  Volume 55, Page(s) e26

    Abstract: Yung-Chih Lai, Shiao-Wei Huang, and Hon-Tsen Yu (2016) ...

    Abstract Yung-Chih Lai, Shiao-Wei Huang, and Hon-Tsen Yu (2016)
    Language English
    Publishing date 2016-07-12
    Publishing country China (Republic : 1949- )
    Document type Journal Article
    ZDB-ID 2105348-0
    ISSN 1810-522X ; 1021-5506
    ISSN (online) 1810-522X
    ISSN 1021-5506
    DOI 10.6620/ZS.2016.55-26
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  10. Article ; Online: The mechano-chemical circuit drives skin organoid self-organization.

    Lei, Mingxing / Harn, Hans I-Chen / Li, Qiwei / Jiang, Jingwei / Wu, Wang / Zhou, Wei / Jiang, Tin-Xin / Wang, Mengyue / Zhang, Jinwei / Lai, Yung-Chih / Juan, Wen-Tau / Widelitz, Randall Bruce / Yang, Li / Gu, Zhong-Ze / Chuong, Cheng-Ming

    Proceedings of the National Academy of Sciences of the United States of America

    2023  Volume 120, Issue 36, Page(s) e2221982120

    Abstract: Stem cells in organoids self-organize into tissue patterns with unknown mechanisms. Here, we use skin organoids to analyze this process. Cell behavior videos show that the morphological transformation from multiple spheroidal units with morphogenesis ... ...

    Abstract Stem cells in organoids self-organize into tissue patterns with unknown mechanisms. Here, we use skin organoids to analyze this process. Cell behavior videos show that the morphological transformation from multiple spheroidal units with morphogenesis competence (CMU) to planar skin is characterized by two abrupt cell motility-increasing events before calming down. The self-organizing processes are controlled by a morphogenetic module composed of molecular sensors, modulators, and executers. Increasing dermal stiffness provides the initial driving force (driver) which activates Yap1 (sensor) in epidermal cysts. Notch signaling (modulator 1) in epidermal cyst tunes the threshold of Yap1 activation. Activated Yap1 induces Wnts and MMPs (epidermal executers) in basal cells to facilitate cellular flows, allowing epidermal cells to protrude out from the CMU. Dermal cell-expressed Rock (dermal executer) generates a stiff force bridge between two CMU and accelerates tissue mixing via activating Laminin and β1-integrin. Thus, this self-organizing coalescence process is controlled by a mechano-chemical circuit. Beyond skin, self-organization in organoids may use similar mechano-chemical circuit structures.
    MeSH term(s) Skin ; Epidermis ; Personality ; Organoids ; Emotions ; Adaptor Proteins, Signal Transducing
    Chemical Substances Adaptor Proteins, Signal Transducing
    Language English
    Publishing date 2023-08-29
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 209104-5
    ISSN 1091-6490 ; 0027-8424
    ISSN (online) 1091-6490
    ISSN 0027-8424
    DOI 10.1073/pnas.2221982120
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