Development and Maintenance of Epidermal Stem Cells in Skin Adnexa

. 2020 Dec 20 ; 21 (24) : . [epub] 20201220

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33419358

Grantová podpora
Progres Q40/06 Charles University

The skin surface is modified by numerous appendages. These structures arise from epithelial stem cells (SCs) through the induction of epidermal placodes as a result of local signalling interplay with mesenchymal cells based on the Wnt-(Dkk4)-Eda-Shh cascade. Slight modifications of the cascade, with the participation of antagonistic signalling, decide whether multipotent epidermal SCs develop in interfollicular epidermis, scales, hair/feather follicles, nails or skin glands. This review describes the roles of epidermal SCs in the development of skin adnexa and interfollicular epidermis, as well as their maintenance. Each skin structure arises from distinct pools of epidermal SCs that are harboured in specific but different niches that control SC behaviour. Such relationships explain differences in marker and gene expression patterns between particular SC subsets. The activity of well-compartmentalized epidermal SCs is orchestrated with that of other skin cells not only along the hair cycle but also in the course of skin regeneration following injury. This review highlights several membrane markers, cytoplasmic proteins and transcription factors associated with epidermal SCs.

Zobrazit více v PubMed

Byrne C., Tainsky M., Fuchs E. Programming gene expression in developing epidermis. [(accessed on 18 December 2020)];Development. 1994 120:2369–2383. Available online: https://www.ncbi.nlm.nih.gov/pubmed/7525178. PubMed

Blanpain C., Lowry W.E., Pasolli H.A., Fuchs E. Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev. 2006;20:3022–3035. doi: 10.1101/gad.1477606. PubMed DOI PMC

Asare A., Levorse J., Fuchs E. Coupling organelle inheritance with mitosis to balance growth and differentiation. Science. 2017;355:eaah4701. doi: 10.1126/science.aah4701. PubMed DOI PMC

Ellis S.J., Gomez N.C., Levorse J., Mertz A.F., Ge Y., Fuchs E. Distinct modes of cell competition shape mammalian tissue morphogenesis. Nature. 2019;569:497–502. doi: 10.1038/s41586-019-1199-y. PubMed DOI PMC

Smart I.H. Variation in the plane of cell cleavage during the process of stratification in the mouse epidermis. Br. J. Dermatol. 1970;82:276–282. doi: 10.1111/j.1365-2133.1970.tb12437.x. PubMed DOI

Matos I., Asare A., Levorse J., Ouspenskaia T., de la Cruz-Racelis J., Schuhmacher L.N., Fuchs E. Progenitors oppositely polarize WNT activators and inhibitors to orchestrate tissue development. Elife. 2020;9:e54304. doi: 10.7554/eLife.54304. PubMed DOI PMC

Ouspenskaia T., Matos I., Mertz A.F., Fiore V.F., Fuchs E. WNT-SHH antagonism specifies and expands stem cells prior to niche formation. Cell. 2016;164:156–169. doi: 10.1016/j.cell.2015.11.058. PubMed DOI PMC

Mok K.W., Saxena N., Heitman N., Grisanti L., Srivastava D., Muraro M.J., Jacob T., Sennett R., Wang Z., Su Y., et al. Dermal condensate niche fate specification occurs prior to formation and is placode progenitor dependent. Dev. Cell. 2019;48:32–48. doi: 10.1016/j.devcel.2018.11.034. PubMed DOI PMC

Sick S., Reinker S., Timmer J., Schlake T. WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science. 2006;314:1447–1450. doi: 10.1126/science.1130088. PubMed DOI

Schlake T., Sick S. Canonical WNT signalling controls hair follicle spacing. Cell Adh. Migr. 2007;1:149–151. doi: 10.4161/cam.1.3.5073. PubMed DOI PMC

Dhouailly D., Godefroit P., Martin T., Nonchev S., Caraguel F., Oftedal O. Getting to the root of scales, feather and hair: As deep as odontodes? Exp. Dermatol. 2019;4:503–508. doi: 10.1111/exd.13391. PubMed DOI

Lai Y.C., Chuong C.M. The “tao” of integuments. Science. 2016;354:1533–1534. doi: 10.1126/science.aal4572. PubMed DOI PMC

Lu C.P., Polak L., Keyes B.E., Fuchs E. Spatiotemporal antagonism in mesenchymal-epithelial signaling in sweat versus hair fate decision. Science. 2016;354:aah6102. doi: 10.1126/science.aah6102. PubMed DOI PMC

Woo W.M., Zhen H.H., Oro A.E. Shh maintains dermal papilla identity and hair morphogenesis via a Noggin-Shh regulatory loop. Genes Dev. 2012;26:1235–1246. doi: 10.1101/gad.187401.112. PubMed DOI PMC

Törnqvist G., Sandberg A., Hägglund A.C., Carlsson L. Cyclic expression of Lhx2 regulates hair formation. PLoS Genet. 2010;6:e1000904. doi: 10.1371/journal.pgen.1000904. PubMed DOI PMC

Frances D., Niemann C. Stem cell dynamics in sebaceous gland morphogenesis in mouse skin. Dev. Biol. 2012;363:138–146. doi: 10.1016/j.ydbio.2011.12.028. PubMed DOI

Jensen K.B., Collins C.A., Nascimento E., Tan D.W., Frye M., Itami S., Watt F.M. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell. 2009;4:427–439. doi: 10.1016/j.stem.2009.04.014. PubMed DOI PMC

Kos R., Reedy M.V., Johnson R.L., Erickson C.A. The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. [(accessed on 18 December 2020)];Development. 2001 128:1467–1479. Available online: https://pubmed.ncbi.nlm.nih.gov/11262245/ PubMed

Lee H.O., Levorse J.M., Shin M.K. The endothelin receptor-B is required for the migration of neural crest-derived melanocyte and enteric neuron precursors. Dev. Biol. 2003;259:162–175. doi: 10.1016/S0012-1606(03)00160-X. PubMed DOI

Qiu W., Chuong C.M., Lei M. Regulation of melanocyte stem cells in the pigmentation of skin and its appendages: Biological patterning and therapeutic potentials. Exp. Dermatol. 2019;28:395–405. doi: 10.1111/exd.13856. PubMed DOI PMC

Donati G., Rognoni E., Hiratsuka T., Liakath-Ali K., Hoste E., Kar G., Kayikci M., Russell R., Kretzschmar K., Mulder K.W., et al. Wounding induces dedifferentiation of epidermal Gata6+ cells and acquisition of stem cell properties. Nat. Cell Biol. 2017;19:603–613. doi: 10.1038/ncb3532. PubMed DOI PMC

Oulès B., Rognoni E., Hoste E., Goss G., Fiehler R., Natsuga K., Quist S., Mentink R., Donati G., Watt F.M. Mutant Lef1 controls Gata6 in sebaceous gland development and cancer. EMBO J. 2019;38:e100526. doi: 10.15252/embj.2018100526. PubMed DOI PMC

Panteleyev A.A., Rosenbach T., Paus R., Christiano A.M. The bulge is the source of cellular renewal in the sebaceous gland of mouse skin. Arch. Dermatol. Res. 2000;292:573–576. doi: 10.1007/s004030000182. PubMed DOI

Nijhof J.G., Braun K.M., Giangreco A., van Pelt C., Kawamoto H., Boyd R.L., Willemze R., Mullenders L.H., Watt F.M., de Gruijl F.R., et al. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development. 2006;133:3027–3037. doi: 10.1242/dev.02443. PubMed DOI

Snippert H.J., Haegebarth A., Kasper M., Jaks V., van Es J.H., Barker N., van de Wetering M., van den Born M., Begthel H., Vries R.G., et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science. 2010;327:1385–1389. doi: 10.1126/science.1184733. PubMed DOI

Mack J.A., Anand S., Maytin E.V. Proliferation and cornification during development of the mammalian epidermis. Birth Defects Res. C Embryo Today. 2005;75:314–329. doi: 10.1002/bdrc.20055. PubMed DOI

Fuchs E. Skin stem cells: Rising to the surface. J. Cell Biol. 2008;180:273–284. doi: 10.1083/jcb.200708185. PubMed DOI PMC

Dekoninck S., Hannezo E., Sifrim A., Miroshnikova Y.A., Aragona M., Malfait M., Gargouri S., de Neunheuser C., Dubois C., Voet T., et al. Defining the design principles of skin epidermis postnatal growth. Cell. 2020;181:604–620. doi: 10.1016/j.cell.2020.03.015. PubMed DOI PMC

Lu C.P., Polak L., Rocha A.S., Pasolli H.A., Chen S.C., Sharma N., Blanpain C., Fuchs E. Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell. 2012;150:136–150. doi: 10.1016/j.cell.2012.04.045. PubMed DOI PMC

Headon D.J. Ectodysplasin signaling in cutaneous appendage development: Dose, duration, and diversity. J. Investig. Dermatol. 2009;129:817–819. doi: 10.1038/jid.2008.426. PubMed DOI

Cui C.Y., Yin M., Sima J., Childress V., Michel M., Piao Y., Schlessinger D. Involvement of Wnt, Eda and Shh at defined stages of sweat gland development. Development. 2014;141:3752–3760. doi: 10.1242/dev.109231. PubMed DOI PMC

Haneke E. Anatomy of the nail unit and the nail biopsy. Semin. Cutan. Med. Surg. 2015;34:95–100. doi: 10.12788/j.sder.2015.0143. PubMed DOI

Lehoczky J.A., Tabin C.J. Lgr6 marks nail stem cells and is required for digit tip regeneration. Proc. Natl. Acad. Sci. USA. 2015;112:13249–13254. doi: 10.1073/pnas.1518874112. PubMed DOI PMC

Jaks V., Barker N., Kasper M., van Es J.H., Snippert H.J., Clevers H., Toftgård R. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 2008;40:1291–1299. doi: 10.1038/ng.239. PubMed DOI

Brownell I., Guevara E., Bai C.B., Loomis C.A., Joyner A.L. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell. 2011;8:552–565. doi: 10.1016/j.stem.2011.02.021. PubMed DOI PMC

Trempus C.S., Morris R.J., Bortner C.D., Cotsarelis G., Faircloth R.S., Reece J.M., Tennant R.W. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Investig. Dermatol. 2003;120:501–511. doi: 10.1046/j.1523-1747.2003.12088.x. PubMed DOI

Liu Y., Lyle S., Yang Z., Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J. Investig. Dermatol. 2003;121:963–968. doi: 10.1046/j.1523-1747.2003.12600.x. PubMed DOI

Youssef K.K., Van Keymeulen A., Lapouge G., Beck B., Michaux C., Achouri Y., Sotiropoulou P.A., Blanpain C. Identification of the cell lineage at the origin of basal cell carcinoma. Nat. Cell Biol. 2010;12:299–305. doi: 10.1038/ncb2031. PubMed DOI

Joost S., Zeisel A., Jacob T., Sun X., La Manno G., Lönnerberg P., Linnarsson S., Kasper M. Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity. Cell Syst. 2016;3:221–237. doi: 10.1016/j.cels.2016.08.010. PubMed DOI PMC

Yang H., Adam R.C., Ge Y., Hua Z.L., Fuchs E. Epithelial-mesenchymal micro-niches govern stem cell lineage choices. Cell. 2017;169:483–496. doi: 10.1016/j.cell.2017.03.038. PubMed DOI PMC

Füllgrabe A., Joost S., Are A., Jacob T., Sivan U., Haegebarth A., Linnarsson S., Simons B.D., Clevers H., Toftgård R., et al. Dynamics of Lgr6+ progenitor cells in the hair follicle, sebaceous gland, and interfollicular epidermis. Stem Cell Rep. 2015;5:843–855. doi: 10.1016/j.stemcr.2015.09.013. PubMed DOI PMC

Gonzales K.A.U., Fuchs E. Skin and its regenerative powers: An alliance between stem cells and their niche. Dev. Cell. 2017;43:387–401. doi: 10.1016/j.devcel.2017.10.001. PubMed DOI PMC

Liu S., Zhang H., Duan E. Epidermal development in mammals: Key regulators, signals from beneath, and stem cells. Int. J. Mol. Sci. 2013;14:10869–10895. doi: 10.3390/ijms140610869. PubMed DOI PMC

Welle M.M., Wiener D.J. The hair follicle: A comparative review of canine hair follicle anatomy and physiology. Toxicol. Pathol. 2016;44:564–574. doi: 10.1177/0192623316631843. PubMed DOI

Fujiwara H., Ferreira M., Donati G., Marciano D.K., Linton J.M., Sato Y., Hartner A., Sekiguchi K., Reichardt L.F., Watt F.M. The basement membrane of hair follicle stem cells is a muscle cell niche. Cell. 2011;144:577–589. doi: 10.1016/j.cell.2011.01.014. PubMed DOI PMC

Fujiwara H., Tsutsui K., Morita R. Multi-tasking epidermal stem cells: Beyond epidermal maintenance. Dev. Growth Differ. 2018;60:531–541. doi: 10.1111/dgd.12577. PubMed DOI

Matsumura H., Mohri Y., Binh N.T., Morinaga H., Fukuda M., Ito M., Kurata S., Hoeijmakers J., Nishimura E.K. Hair follicle aging is driven by transepidermal elimination of stem cells via COL17A1 proteolysis. Science. 2016;351:aad4395. doi: 10.1126/science.aad4395. PubMed DOI

Miyachi K., Yamada T., Kawagishi-Hotta M., Hasebe Y., Date Y., Hasegawa S., Arima M., Iwata Y., Kobayashi T., Numata S., et al. Extracellular proteoglycan decorin maintains human hair follicle stem cells. J. Dermatol. 2018;45:1403–1410. doi: 10.1111/1346-8138.14678. PubMed DOI

Hsu Y.C., Pasolli H.A., Fuchs E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell. 2011;144:92–105. doi: 10.1016/j.cell.2010.11.049. PubMed DOI PMC

Li K.N., Jain P., He C.H., Eun F.C., Kang S., Tumbar T. Skin vasculature and hair follicle cross-talking associated with stem cell activation and tissue homeostasis. Elife. 2019;8:e45977. doi: 10.7554/eLife.45977. PubMed DOI PMC

Di-Poï N., Milinkovitch M.C. The anatomical placode in reptile scale morphogenesis indicates shared ancestry among skin appendages in amniotes. Sci. Adv. 2016;2:e1600708. doi: 10.1126/sciadv.1600708. PubMed DOI PMC

Xu Y.L., Sun J.G., Wu F.B., Xi Y.M. Investigation of characteristics of feather follicle stem cells and their regeneration potential. J. Stem Cells Regen. Med. 2011;7:69–74. PubMed PMC

Wu P., Lai Y.C., Widelitz R., Chuong C.M. Comprehensive molecular and cellular studies suggest avian scutate scales are secondarily derived from feathers, and more distant from reptilian scales. Sci. Rep. 2018;8:16766. doi: 10.1038/s41598-018-35176-y. PubMed DOI PMC

Li H., Hou L. Regulation of melanocyte stem cell behavior by the niche microenvironment. Pigment Cell Melanoma Res. 2018;5:556–569. doi: 10.1111/pcmr.12701. PubMed DOI

Tanimura S., Tadokoro Y., Inomata K., Binh N.T., Nishie W., Yamazaki S., Nakauchi H., Tanaka Y., McMillan J.R., Sawamura D., et al. Hair follicle stem cells provide a functional niche for melanocyte stem cells. Cell Stem Cell. 2011;8:177–187. doi: 10.1016/j.stem.2010.11.029. PubMed DOI

Liu N., Matsumura H., Kato T., Ichinose S., Takada A., Namiki T., Asakawa K., Morinaga H., Mohri Y., De Arcangelis A., et al. Stem cell competition orchestrates skin homeostasis and ageing. Nature. 2019;568:344–350. doi: 10.1038/s41586-019-1085-7. PubMed DOI

Nishimura E.K. Melanocyte stem cells: A melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell Melanoma Res. 2011;24:401–410. doi: 10.1111/j.1755-148X.2011.00855.x. PubMed DOI

Barsh G., Gunn T., He L., Schlossman S., Duke-Cohan J. Biochemical and genetic studies of pigment-type switching. Pigment Cell Res. 2000;13(Suppl. 8):48–53. doi: 10.1034/j.1600-0749.13.s8.10.x. PubMed DOI

Sharov A.A., Fessing M., Atoyan R., Sharova T.Y., Haskell-Luevano C., Weiner L., Funa K., Brissette J.L., Gilchrest B.A., Botchkarev V.A. Bone morphogenetic protein (BMP) signaling controls hair pigmentation by means of cross-talk with the melanocortin receptor-1 pathway. Proc. Natl. Acad. Sci. USA. 2005;102:93–98. doi: 10.1073/pnas.0408455102. PubMed DOI PMC

Kretzschmar K., Cottle D.L., Donati G., Chiang M.F., Quist S.R., Gollnick H.P., Natsuga K., Lin K.I., Watt F.M. BLIMP1 is required for postnatal epidermal homeostasis but does not define a sebaceous gland progenitor under steady-state conditions. Stem Cell Rep. 2014;3:620–633. doi: 10.1016/j.stemcr.2014.08.007. PubMed DOI PMC

Suzuki D., Senoo M. Increased p63 phosphorylation marks early transition of epidermal stem cells to progenitors. J. Investig. Dermatol. 2012;132:2461–2464. doi: 10.1038/jid.2012.165. PubMed DOI PMC

Watanabe M., Natsuga K., Nishie W., Kobayashi Y., Donati G., Suzuki S., Fujimura Y., Tsukiyama T., Ujiie H., Shinkuma S., et al. Type XVII collagen coordinates proliferation in the interfollicular epidermis. Elife. 2017;6:e26635. doi: 10.7554/eLife.26635. PubMed DOI PMC

Yin C., Zhang T., Qiao L., Du J., Li S., Zhao H., Wang F., Huang Q., Meng W., Zhu H., et al. TLR7-expressing cells comprise an interfollicular epidermal stem cell population in murine epidermis. Sci. Rep. 2014;25:5831. doi: 10.1038/srep05831. PubMed DOI PMC

Sellheyer K. Nail stem cells. J. Dtsch. Dermatol. Ges. 2013;11:235–239. doi: 10.1111/ddg.12030. PubMed DOI

Takeo M., Chou W.C., Sun Q., Lee W., Rabbani P., Loomis C., Taketo M.M., Ito M. Wnt activation in nail epithelium couples nail growth to digit regeneration. Nature. 2013;499:228–232. doi: 10.1038/nature12214. PubMed DOI PMC

Naveau A., Seidel K., Klein O.D. Tooth, hair and claw: Comparing epithelial stem cell niches of ectodermal appendages. Exp. Cell Res. 2014;325:96–103. doi: 10.1016/j.yexcr.2014.02.003. PubMed DOI PMC

Shi J., Lv Z., Nie M., Lu W., Liu C., Tian Y., Li L., Zhang G., Ren R., Zhang Z., et al. Human nail stem cells are retained but hypofunctional during aging. J. Mol. Histol. 2018;49:303–316. doi: 10.1007/s10735-018-9769-0. PubMed DOI PMC

Gong X., Carmon K.S., Lin Q., Thomas A., Yi J., Liu Q. LGR6 is a high affinity receptor of R-spondins and potentially functions as a tumor suppressor. PLoS ONE. 2012;7:e37137. doi: 10.1371/journal.pone.0037137. PubMed DOI PMC

Snippert H.J., Clevers H. Tracking adult stem cells. EMBO Rep. 2011;12:113–122. doi: 10.1038/embor.2010.216. PubMed DOI PMC

Liao X.H., Nguyen H. Epidermal expression of Lgr6 is dependent on nerve endings and Schwann cells. Exp. Dermatol. 2014;23:195–198. doi: 10.1111/exd.12340. PubMed DOI PMC

Barker N., Huch M., Kujala P., van de Wetering M., Snippert H.J., van Es J.H., Sato T., Stange D.E., Begthel H., van den Born M., et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell. 2010;6:25–36. doi: 10.1016/j.stem.2009.11.013. PubMed DOI

Barker N., Rookmaaker M.B., Kujala P., Ng A., Leushacke M., Snippert H., van de Wetering M., Tan S., Van Es J.H., Huch M., et al. Lgr5(+ve) stem/progenitor cells contribute to nephron formation during kidney development. Cell Rep. 2012;2:540–552. doi: 10.1016/j.celrep.2012.08.018. PubMed DOI

de Visser K.E., Ciampricotti M., Michalak E.M., Tan D.W., Speksnijder E.N., Hau C.S., Clevers H., Barker N., Jonkers J. Developmental stage-specific contribution of LGR5(+) cells to basal and luminal epithelial lineages in the postnatal mammary gland. J. Pathol. 2012;228:300–309. doi: 10.1002/path.4096. PubMed DOI

Hao H.X., Xie Y., Zhang Y., Charlat O., Oster E., Avello M., Lei H., Mickanin C., Liu D., Ruffner H., et al. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature. 2012;485:195–200. doi: 10.1038/nature11019. PubMed DOI

Ren X., Xia W., Xu P., Shen H., Dai X., Liu M., Shi Y., Ye X., Dang Y. Lgr4 deletion delays the hair cycle and inhibits the activation of hair follicle stem cells. J. Investig. Dermatol. 2020;140:1706–1712. doi: 10.1016/j.jid.2019.12.034. PubMed DOI PMC

Page M.E., Lombard P., Ng F., Göttgens B., Jensen K.B. The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell. 2013;13:471–482. doi: 10.1016/j.stem.2013.07.010. PubMed DOI PMC

Gur G., Rubin C., Katz M., Amit I., Citri A., Nilsson J., Amariglio N., Henriksson R., Rechavi G., Hedman H., et al. LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J. 2004;23:3270–3281. doi: 10.1038/sj.emboj.7600342. PubMed DOI PMC

Laederich M.B., Funes-Duran M., Yen L., Ingalla E., Wu X., Carraway K.L., 3rd, Sweeney C. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J. Biol. Chem. 2004;279:47050–47056. doi: 10.1074/jbc.M409703200. PubMed DOI

Waters J.M., Richardson G.D., Jahoda C.A. Hair follicle stem cells. Semin. Cell. Dev. Biol. 2007;18:245–254. doi: 10.1016/j.semcdb.2007.02.003. PubMed DOI

Panteleyev A.A. Functional anatomy of the hair follicle: The Secondary Hair Germ. Exp. Dermatol. 2018;27:701–720. doi: 10.1111/exd.13666. PubMed DOI

Michel M., Török N., Godbout M.J., Lussier M., Gaudreau P., Royal A., Germain L. Keratin 19 as a biochemical marker of skin stem cells in vivo and in vitro: Keratin 19 expressing cells are differentially localized in function of anatomic sites, and their number varies with donor age and culture stage. J. Cell Sci. 1996;109:1017–1028. PubMed

Komine M., Freedberg I.M., Blumenberg M. Regulation of epidermal expression of keratin K17 in inflammatory skin diseases. J. Investig. Dermatol. 1996;107:569–575. doi: 10.1111/1523-1747.ep12582820. PubMed DOI

Kumar A., Nithya J. Cytokeratin: A review on current concepts. Int. J. Orofac. Biol. 2018;2:6–11. doi: 10.4103/ijofb.ijofb_3_18. DOI

Barrandon Y., Green H. Cell size as a determinant of the clone-forming ability of human keratinocytes. Proc. Natl. Acad. Sci. USA. 1985;82:5390–5394. doi: 10.1073/pnas.82.16.5390. PubMed DOI PMC

Inoue K., Aoi N., Sato T., Yamauchi Y., Suga H., Eto H., Kato H., Araki J., Yoshimura K. Differential expression of stem-cell-associated markers in human hair follicle epithelial cells. Lab. Investig. 2009;89:844–856. doi: 10.1038/labinvest.2009.48. PubMed DOI

Piwko-Czuchra A., Koegel H., Meyer H., Bauer M., Werner S., Brakebusch C., Fässler R. Beta1 integrin-mediated adhesion signalling is essential for epidermal progenitor cell expansion. PLoS ONE. 2009;4:e5488. doi: 10.1371/journal.pone.0005488. PubMed DOI PMC

Nanba D. Human keratinocyte stem cells: From cell biology to cell therapy. J. Dermatol. Sci. 2019;96:66–72. doi: 10.1016/j.jdermsci.2019.10.002. PubMed DOI

Marconi A., Dallaglio K., Lotti R., Vaschieri C., Truzzi F., Fantini F., Pincelli C. Survivin identifies keratinocyte stem cells and is downregulated by anti-beta1 integrin during anoikis. Stem Cells. 2007;25:149–155. doi: 10.1634/stemcells.2006-0165. PubMed DOI

Kim S.H., Sistrunk C., Miliani de Marval P.L., Rodriguez-Puebla M.L. Characterization of hair-follicle side population cells in mouse epidermis and skin tumors. Oncol Lett. 2017;14:6497–6504. doi: 10.3892/ol.2017.7048. PubMed DOI PMC

Yano S., Ito Y., Fujimoto M., Hamazaki T.S., Tamaki K., Okochi H. Characterization and localization of side population cells in mouse skin. Stem Cells. 2005;23:834–841. doi: 10.1634/stemcells.2004-0226. PubMed DOI

Rhee H., Polak L., Fuchs E. Lhx2 maintains stem cell character in hair follicles. Science. 2006;312:1946–1949. doi: 10.1126/science.1128004. PubMed DOI PMC

Merrill B.J., Gat U., DasGupta R., Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 2001;15:1688–1705. doi: 10.1101/gad.891401. PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Genomic and Transcriptomic Characterization of Atypical Recurrent Flank Alopecia in the Cesky Fousek

. 2022 Apr 07 ; 13 (4) : . [epub] 20220407

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...