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• W2029283433 abstract "3,3′-diaminobenzidine TO THE EDITOR Our previous investigations showed that Slug (Snai2), a member of the Snail family of developmental transcription factors, is expressed in unperturbed adult murine epidermis, where it regulates a wide variety of gene targets (Newkirk et al., 2008bNewkirk K.M. MacKenzie D.A. Bakaletz A.P. et al.Microarray analysis demonstrates a role for Slug in epidermal homeostasis.J Invest Dermatol. 2008; 128: 361-369Crossref PubMed Scopus (21) Google Scholar). Slug expression is induced by a number of growth factors and environmental stimuli (Hudson et al., 2007Hudson L.G. Choi C. Newkirk K.M. et al.Ultraviolet radiation stimulates expression of Snail family transcription factors in keratinocytes.Mol Carcinog. 2007; 46: 257-268Crossref PubMed Scopus (51) Google Scholar; Kusewitt et al., 2009Kusewitt D.F. Choi C. Newkirk K.M. et al.Slug/Snai2 is a downstream mediator of epidermal growth factor receptor-stimulated reepithelialization.J Invest Dermatol. 2009; 129: 491-495Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar). Slug enhances cutaneous wound reepithelialization, skin tumor progression, and the sunburn response (Savagner et al., 2005Savagner P. Kusewitt D.F. Carver E.A. et al.Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes.J Cell Physiol. 2005; 202: 858-866Crossref PubMed Scopus (192) Google Scholar; Newkirk et al., 2007Newkirk K.M. Parent A.E. Fossey S.L. et al.Snai2 expression enhances ultraviolet radiation-induced skin carcinogenesis.Am J Pathol. 2007; 171: 1629-1639Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar, Newkirk et al., 2008aNewkirk K.M. Duncan F.J. Brannick E.M. et al.The acute cutaneous inflammatory response is attenuated in Slug-knockout mice.Lab Invest. 2008; 88: 831-841Crossref PubMed Scopus (13) Google Scholar; Hudson et al., 2009Hudson L.G. Newkirk K.M. Chandler H.L. et al.Cutaneous wound reepithelialization is compromised in mice lacking functional Slug (Snai2).J Dermatol Sci. 2009; 56: 19-26Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar). The present studies document Slug expression in embryonic and neonatal epidermis and hair follicles, and significant alterations in hair growth kinetics in Slug knockout mice during the first postnatal hair cycle, indicating a further contribution of Slug to the maintenance of skin homeostasis. Microwave antigen retrieval was performed in citrate buffer on deparaffinized E10–E17 CD1 mouse embryo sections (Zyagen, San Diego, CA). Slides were incubated overnight at 4°C in monoclonal rabbit anti-Slug antibody (#9585, Cell Signaling, Danvers, MA) diluted 1:50, treated with Biocare Rabbit on Rodent HRP-Polymer (Biocare Medical, Concord, CA) and 3,3′-diaminobenzidine chromagen, then counterstained with hematoxylin. Of the many anti-Slug antibodies we have tested, only this antibody consistently gives single bands of appropriate size on protein isolated from HaCaT human epidermal cells (data not shown). Keratin 14 immunostaining was performed similarly, applying first the primary antibody (Covance, Princeton, NJ) at a dilution of 1:500 for 30minutes at room temperature, and then Envision Plus labeled polymer anti-rabbit-HRP (DAKO, Carpinteria, CA) for 30minutes. In embryonic tissues, Slug staining was exclusively nuclear. On E10 and E11, Slug was expressed in scattered cells of the single-layered epidermis and in most of the underlying primitive mesenchymal cells, a time when keratin 14 immunoreactivity was seen in only a few cells (Figure 1). At the beginning of periderm formation at E12, when strong keratin 14 immunoreactivity was first observed, Slug was expressed in essentially all skin epithelial cells and in the underlying mesenchyme. As the epithelium underwent stratification, Slug and keratin 14 expression was progressively confined to basal keratinocytes, with Slug localization occurring earlier. Slug staining was observed in progressively fewer dermal cells as primitive mesenchymal cells matured. However, a substantial number of dermal cells continued to express Slug. In the placode, hair germ, and peg stages of hair follicle development, Slug expression was prominent in the thickened and invaginating epithelium, but was absent from the underlying mesenchymal cells that ultimately form the dermal papillae (Figure 1). In pigmented Slug-lacZ 129 mice, the Slug locus was inactivated by an in-frame insertion of the β-galactosidase gene into the zinc finger coding region of the Slug gene (Jiang et al., 1998Jiang R. Lan Y. Norton C.R. et al.The Slug gene is not essential for mesoderm or neural crest development in mice.Dev Biol. 1998; 198: 277-285Crossref PubMed Google Scholar). Mice homozygous for the Slug-lacZ allele are functional Slug knockout animals, but heterozygous Slug knockout mice are phenotypically normal. Daily examination of newborn mice (Figure 2a) revealed that darkening of the skin occurred in all wild-type and heterozygous Slug knockout mice by postnatal days 2–3; however, darkening of the skin of Slug knockout neonates was not seen until postnatal days 4–7. In wild-type and heterozygous knockout mice, hair emergence occurred on postnatal days 5–7, but in knockout mice the emergence was delayed until days 8–10. Differences between knockout and wild-type/heterozygous mice were highly significant for both skin darkening and hair emergence (P<10−7 using the log-rank statistic). Skin darkening in pigmented neonatal mice occurs during early hair follicle growth and hair shafts emerge from follicles during mid to late follicle maturation (Muller-Rover et al., 2001Muller-Rover S. Handjiski B. van der Veen C. et al.A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages.J Invest Dermatol. 2001; 117: 3-15Crossref PubMed Google Scholar). Thus, our findings suggest delayed hair follicle development in neonatal Slug knockout mice. Immunohistochemical analysis for Slug in 129 wild-type mice showed that Slug was expressed in many, but not all, basal keratinocytes at birth. As previously reported for adult epidermis (Parent et al., 2004Parent A.E. Choi C. Caudy K. et al.The developmental transcription factor slug is widely expressed in tissues of adult mice.J Histochem Cytochem. 2004; 52: 959-965Crossref PubMed Scopus (32) Google Scholar), Slug-expressing keratinocytes were clustered around hair follicles. In developing follicles, Slug was stably expressed in the developing external root sheath, hair matrix cells, and some mesenchymal cells of the dermal papilla (Figure 2b). Most interfollicular epidermal cells were Slug-positive at 3 days after birth, but staining progressively declined. At 18 days after birth, follicles in catagen expressed little or no Slug, and Slug expression was also absent from the interfollicular epidermis. Early telogen follicles and interfollicular epidermis showed no Slug immunoreactivity. Localization of Slug was confirmed by immunohistochemical analysis for Slug in tissues of mice expressing the Slug–β-galactosidase fusion protein (Figure 2b, inset). Staining was performed on frozen sections using an affinity-purified rabbit anti-β-galactosidase (#RGAL-45, Immunology Consultants Laboratory, Newberg, OR) as recommended by the supplier. Immunohistochemical and in situ hybridization studies by Jamora et al., 2005Jamora C. Lee P. Kocieniewski P. et al.A signaling pathway involving TGF-beta2 and snail in hair follicle morphogenesis.PLoS Biol. 2005; 3: e11Crossref PubMed Scopus (117) Google Scholar indicated that expression of the closely related Snail family transcription factor Snail (Snai1) in the epidermis is limited to hair bud cells during the period E15.5 days to birth. No staining of mesodermal skin cells was reported by these investigators. In contrast, Franci et al., 2006Franci C. Takkunen M. Dave N. et al.Expression of Snail protein in tumor-stroma interface.Oncogene. 2006; 25: 5134-5144PubMed Google Scholar detected Snail expression only in mesenchymal cells of the skin, particularly in the mesenchymal cells clustered below the hair buds of embryonic skin and in the dermal papillae of adult hair follicles. The discrepancy between the two studies has not been resolved; however, it does appear that the patterns of expression of Slug and Snail in the epidermis differ substantially. The pelage of adult Slug knockout animals appeared normal; thus, Slug was not required for hair follicle development and maintenance. However, Slug knockout mice showed significantly delayed onset of postnatal hair growth, and Slug expression was modulated temporally and spatially in embryonic and postnatal hair follicles. These findings indicate a modest but distinct role for Slug in the hair cycle. This work was supported by the following National Institutes of Health awards: R01 CA089216 (DK), P30 CA16672, and P30 ES007784. We thank the members of the histology laboratory at the Science Park Research Division of the University of Texas MD Anderson Cancer Center for their outstanding histology support and Dr Kevin Lin for statistical assistance." @default.
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• W2029283433 title "Slug (Snai2) Expression during Skin and Hair Follicle Development" @default.
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