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      Schwann Cells in the Ventral Dermis Do Not Derive from Myf5-Expressing Precursors

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          Summary

          The embryonic origin of lineage precursors of the trunk dermis is somewhat controversial. Precursor cells traced by Myf5 and Twist2 ( Dermo1) promoter activation (i.e., cells of presumed dermomyotomal lineage) have been reported to generate Schwann cells. On the other hand, abundant data demonstrate that dermal Schwann cells derive from the neural crest. This is relevant because dermal precursors give rise to neural lineages, and multilineage differentiation potential qualifies them as adult stem cells. However, it is currently unclear whether neural lineages arise from dedifferentiated Schwann cells instead of mesodermally derived dermal precursor cells. To clarify these discrepancies, we traced SOX2 + adult dermal precursor cells by two independent Myf5 lineage tracing strains. We demonstrate that dermal Schwann cells do not belong to the Myf5 + cell lineage, indicating that previous tracing data reflected aberrant cre recombinase expression and that bona fide Myf5 + dermal precursors cannot transdifferentiate to neural lineages in physiological conditions.

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          Highlights

          • Adult Myf5-cre Sor mice aberrantly trace dermal Schwann cells (dSCs)

          • Dedifferentiated, SOX2 + dSCs are the neural-competent precursors in the dermis

          • These findings cast doubt on the multipotency of adult skin-derived precursors

          Abstract

          In this article, Izeta, Gutiérrez-Rivera and colleagues solve a controversy regarding how non-neural crest-derived adult dermal precursors are able to commit to peripheral glial fate. Through Myf5 + cell lineage tracing (with two independent strains), in situ localization, and sorting experiments, they demonstrate that aberrant lineage tracing unexpectedly traces dermal Schwann cells. Thus, instead of resident stem/precursor cells, neural-competent cells of adult ventral dermis may just be dedifferentiated Schwann cells.

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          SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells.

          Despite the remarkable regenerative capacity of mammalian skin, an adult dermal stem cell has not yet been identified. Here, we investigated whether skin-derived precursors (SKPs) might fulfill such a role. We show that SKPs derive from Sox2(+) hair follicle dermal cells and that these two cell populations are similar with regard to their transcriptome and functional properties. Both clonal SKPs and endogenous Sox2(+) cells induce hair morphogenesis, differentiate into dermal cell types, and home to a hair follicle niche upon transplantation. Moreover, hair follicle-derived SKPs self-renew, maintain their multipotency, and serially reconstitute hair follicles. Finally, grafting experiments show that follicle-associated dermal cells move out of their niche to contribute cells for dermal maintenance and wound-healing. Thus, SKPs derive from Sox2(+) follicle-associated dermal precursors and display functional properties predicted of a dermal stem cell, contributing to dermal maintenance, wound-healing, and hair follicle morphogenesis.
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            The basement membrane of hair follicle stem cells is a muscle cell niche.

            The hair follicle bulge in the epidermis associates with the arrector pili muscle (APM) that is responsible for piloerection ("goosebumps"). We show that stem cells in the bulge deposit nephronectin into the underlying basement membrane, thus regulating the adhesion of mesenchymal cells expressing the nephronectin receptor, α8β1 integrin, to the bulge. Nephronectin induces α8 integrin-positive mesenchymal cells to upregulate smooth muscle markers. In nephronectin knockout mice, fewer arrector pili muscles form in the skin, and they attach to the follicle above the bulge, where there is compensatory upregulation of the nephronectin family member EGFL6. Deletion of α8 integrin also abolishes selective APM anchorage to the bulge. Nephronectin is a Wnt target; epidermal β-catenin activation upregulates epidermal nephronectin and dermal α8 integrin expression. Thus, bulge stem cells, via nephronectin expression, create a smooth muscle cell niche and act as tendon cells for the APM. Our results reveal a functional role for basement membrane heterogeneity in tissue patterning. PAPERCLIP: Copyright © 2011 Elsevier Inc. All rights reserved.
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              Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis.

              The dermal papilla comprises the specialised mesenchymal cells at the base of the hair follicle. Communication between dermal papilla cells and the overlying epithelium is essential for differentiation of the hair follicle lineages. We report that Sox2 is expressed in all dermal papillae at E16.5, but from E18.5 onwards expression is confined to a subset of dermal papillae. In postnatal skin, Sox2 is only expressed in the dermal papillae of guard/awl/auchene follicles, whereas CD133 is expressed both in guard/awl/auchene and in zigzag dermal papillae. Using transgenic mice that express GFP under the control of the Sox2 promoter, we isolated Sox2(+) (GFP(+)) CD133(+) cells and compared them with Sox2(-) (GFP(-)) CD133(+) dermal papilla cells. In addition to the 'core' dermal papilla gene signature, each subpopulation expressed distinct sets of genes. GFP(+) CD133(+) cells had upregulated Wnt, FGF and BMP pathways and expressed neural crest markers. In GFP(-) CD133(+) cells, the hedgehog, IGF, Notch and integrin pathways were prominent. In skin reconstitution assays, hair follicles failed to form when dermis was depleted of both GFP(+) CD133(+) and GFP(-) CD133(+) cells. In the absence of GFP(+) CD133(+) cells, awl/auchene hairs failed to form and only zigzag hairs were found. We have thus demonstrated a previously unrecognised heterogeneity in dermal papilla cells and shown that Sox2-positive cells specify particular hair follicle types.
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                Author and article information

                Contributors
                Journal
                Stem Cell Reports
                Stem Cell Reports
                Stem Cell Reports
                Elsevier
                2213-6711
                12 October 2017
                14 November 2017
                12 October 2017
                : 9
                : 5
                : 1477-1487
                Affiliations
                [1 ]Tissue Engineering Laboratory, Bioengineering Area, Instituto Biodonostia, San Sebastian 20014, Spain
                [2 ]Department of Biomedical Engineering, School of Engineering, Tecnun-University of Navarra, San Sebastian 20009, Spain
                Author notes
                []Corresponding author araika.gutierrez@ 123456biodonostia.org
                [∗∗ ]Corresponding author ander.izeta@ 123456biodonostia.org
                Article
                S2213-6711(17)30417-4
                10.1016/j.stemcr.2017.09.010
                5830985
                29033303
                23fbcb95-28bd-422a-8c37-38d70c85a9c5
                © 2017 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 11 November 2016
                : 12 September 2017
                : 13 September 2017
                Categories
                Article

                dermal stem cell,developmental origin,neural crest,mesoderm,lineage tracing,skin-derived precursors,dedifferentiation,peripheral glia,multilineage differentiation potential,cell fate

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