Skin and Its Regenerative Powers: An Alliance between Stem Cells and Their Niche
Open accessAbstract
Tissues have a natural capacity to replace dying cells and to heal wounds. This ability resides in resident stem cells, which self-renew, preserve, and repair their tissue during homeostasis and following injury. The skin epidermis and its appendages are subjected to daily assaults from the external environment. A high demand is placed on renewal and regeneration of the skin's barrier in order to protect the body from infection and dehydration and to heal wounds. This review focuses on the epithelial stem cells of skin, where they come from, where they reside, and how they function in normal homeostasis and wound repair.
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Several studies have suggested an unanticipated level of cellular plasticity within epidermal keratinocytes, resulting in cell-fate flexibility during wound repair.
“Several studies have suggested an unanticipated level of cellular plasticity within epidermal keratinocytes, resulting in cell‐fate flexibility during wound repair.[ 8 , 9 , 10 , 11 , 12 ]”
From Sweat Gland Organoids Originating from Reprogrammed Epidermal Keratinocytes Functionally Recapitulated Damaged Skin (2021) · cites this paper as [12]
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Cotsarelis, G., Sun, T.-T., & Lavker, R. M. (1990) · Cell · doi:10.1016/0092-8674(90)90696-c · Cited by 2,276 · see citing works
Epidermal homeostasis: a balancing act of stem cells in the skin
Blanpain, C., & Fuchs, E. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2636 · Cited by 1,270 · see citing works
Self-citationAsymmetric cell divisions promote stratification and differentiation of mammalian skin
Lechler, T., & Fuchs, E. (2005) · Nature · doi:10.1038/nature03922 · Cited by 998 · see citing works
Self-citationA single type of progenitor cell maintains normal epidermis
Clayton, E., Doupé, D. P., Klein, A. M., Winton, D. J., Simons, B. D., & Jones, P. H. (2007) · Nature · doi:10.1038/nature05574 · Cited by 853 · see citing works
Joost, S., Zeisel, A., Jacob, T., Sun, X., La Manno, G., Lönnerberg, P., Linnarsson, S., & Kasper, M. (2016) · Cell Systems · doi:10.1016/j.cels.2016.08.010 · Cited by 429 · cited 2× · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript α6β4, KRT5/14, LGR5, SOX9, TCF3/4, NFATc1, and LHX2 (Joost et al., 2016; Yang et al., 2017).”
BackgroundAsymmetric cell divisions promote Notch-dependent epidermal differentiation
Williams, S. E., Beronja, S., Pasolli, H. A., & Fuchs, E. (2011) · Nature · doi:10.1038/nature09793 · Cited by 406 · see citing works
Self-citationLu, C. P., Polak, L., Rocha, A. S., Pasolli, H. A., Chen, S.-C., Sharma, N., Blanpain, C., & Fuchs, E. (2012) · Cell · doi:10.1016/j.cell.2012.04.045 · Cited by 301 · cited 8× · see citing works
“Many of these progenitors can both self-renew and sustain long-term tissue maintenance, and hence qualify as bona fide stem cell compartments (Blanpain et al., 2004; Horsley et al., 2006; Jensen et al., 2009; Lu et al., 2012; Morris et al., 2004; Snippert et al., 2010; Tumbar et al., 2004).”
BackgroundMethodInfluentialSelf-citationImpaired Epidermal to Dendritic T Cell Signaling Slows Wound Repair in Aged Skin
Keyes, B. E., Liu, S., Asare, A., Naik, S., Levorse, J., Polak, L., Lu, C. P., Nikolova, M., Pasolli, H. A., & Fuchs, E. (2016) · Cell · doi:10.1016/j.cell.2016.10.052 · Cited by 266 · see citing works
Self-citationAnsell, D. M., Kloepper, J. E., Thomason, H. A., Paus, R., & Hardman, M. J. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.291 · Cited by 171 · see citing works
Flagged first, then by citations
Research works printed but not linked: 99
- Adam RC Yang H Rockowitz S Larsen SB Nikolova M Oristian DS Polak L Kadaja M Asare A Zheng D 2015 Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice Nature 521 366 370 25799994 PMC4482136
- Ahtiainen L Lefebvre S Lindfors PH Renvoise E Shirokova V Vartiainen MK Thesleff I Mikkola ML 2014 Directional cell migration, but not proliferation, drives hair placode morphogenesis Dev. Cell 28 588 602 24636260
- Ali N Zirak B Rodriguez RS Pauli ML Truong HA Lai K Ahn R Corbin K Lowe MM Scharschmidt TC 2017 Regulatory T cells in skin facilitate epithelial stem cell differentiation Cell 169 1119 1129 28552347 PMC5504703
- Aragona M Dekoninck S Rulands S Lenglez S Mascre G Simons BD Blanpain C 2017 Defining stem cell dynamics and migration during wound healing in mouse skin epidermis Nat. Commun 8 14684 28248284 PMC5339881
- Asare A Levorse J Fuchs E 2017 Coupling organelle inheritance with mitosis to balance growth and differentiation Science 355 https://doi.org/10.1126/science.aah4701 PMC5333555 28154022 · DOI
- Belkaid Y Segre JA 2014 Dialogue between skin microbiota and immunity Science 346 954 959 25414304
- Beumer J Clevers H 2016 Regulation and plasticity of intestinal stem cells during homeostasis and regeneration Development 143 3639 3649 27802133
- Blanpain C Lowry WE Geoghegan A Polak L Fuchs E 2004 Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche Cell 118 635 648 15339667
- Brownell I Guevara E Bai CB Loomis CA Joyner AL 2011 Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells Cell Stem Cell 8 552 565 21549329 PMC3089905
- Byrd KM Lough KJ Patel JH Descovich CP Curtis TA Williams SE 2016 LGN plays distinct roles in oral epithelial stratification, filiform papilla morphogenesis and hair follicle development Development 143 2803 2817 27317810 PMC5004909
- Chang CY Pasolli HA Giannopoulou EG Guasch G Gronostajski RM Elemento O Fuchs E 2013 NFIB is a governor of epithelial-melanocyte stem cell behaviour in a shared niche Nature 495 98 102 23389444 PMC3635831
- Chaplin G Jablonski NG Sussman RW Kelley EA 2014 The role of piloerection in primate thermoregulation Folia Primatol (Basel) 85 1 17 24192984
- Chi W Wu E Morgan BA 2013 Dermal papilla cell number specifies hair size, shape and cycling and its reduction causes follicular decline Development 140 1676 1683 23487317 PMC3621486
- Chuong CM Noveen A 1999 Phenotypic determination of epithelial appendages: genes, developmental pathways, and evolution J. Investig. Dermatol. Symp. Proc 4 307 311 10674387
- Chuong CM Widelitz RB 2009 The river of stem cells Cell Stem Cell 4 100 102 19200797 PMC4389586
- Claudinot S Nicolas M Oshima H Rochat A Barrandon Y 2005 Long-term renewal of hair follicles from clonogenic multipotent stem cells Proc. Natl. Acad. Sci. USA 102 14677 14682 16203973 PMC1253596
- Coles EG Gammill LS Miner JH Bronner-Fraser M 2006 Abnormalities in neural crest cell migration in laminin alpha5 mutant mice Dev. Biol 289 218 228 16316641
- Donati G Rognoni E Hiratsuka T Liakath-Ali K Hoste E Kar G Kayikci M Russell R Kretzschmar K Mulder KW 2017 Wounding induces dedifferentiation of epidermal Gata6+ cells and acquisition of stem cell properties Nat. Cell Biol 19 603 613 28504705 PMC7610974
- Doupe DP Klein AM Simons BD Jones PH 2010 The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate Dev. Cell 18 317 323 20159601
- Driskell RR Lichtenberger BM Hoste E Kretzschmar K Simons BD Charalambous M Ferron SR Herault Y Pavlovic G Ferguson-Smith AC 2013 Distinct fibroblast lineages determine dermal architecture in skin development and repair Nature 504 277 281 24336287 PMC3868929
- Festa E Fretz J Berry R Schmidt B Rodeheffer M Horowitz M Horsley V 2011 Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling Cell 146 761 771 21884937 PMC3298746
- Fuchs E Green H 1980 Changes in keratin gene expression during terminal differentiation of the keratinocyte Cell 19 1033 1042 6155214
- Fuchs EV Coppock SM Green H Cleveland DW 1981 Two distinct classes of keratin genes and their evolutionary significance Cell 27 75 84 6173133
- Fujiwara H Ferreira M Donati G Marciano DK Linton JM Sato Y Hartner A Sekiguchi K Reichardt LF Watt FM 2011 The basement membrane of hair follicle stem cells is a muscle cell niche Cell 144 577 589 21335239 PMC3056115
- Garcin CL Ansell DM Headon DJ Paus R Hardman MJ 2016 Hair follicle bulge stem cells appear dispensable for the acute phase of wound re-epithelialization Stem Cells 34 1377 1385 26756547 PMC4985639
- Ge Y Gomez NC Adam RC Nikolova M Yang H Verma A Lu CP Polak L Yuan S Elemento O 2017 Stem cell lineage infidelity drives wound repair and cancer Cell 169 636 650 28434617 PMC5510746
- Greco V Chen T Rendl M Schober M Pasolli HA Stokes N Dela Cruz-Racelis J Fuchs E 2009 A two-step mechanism for stem cell activation during hair regeneration Cell Stem Cell 4 155 169 19200804 PMC2668200
- Green KJ Getsios S Troyanovsky S Godsel LM 2010 Intercellular junction assembly, dynamics, and homeostasis Cold Spring Harb. Perspect. Biol 2 a000125 20182611 PMC2828282
- Gurtner GC Werner S Barrandon Y Longaker MT 2008 Wound repair and regeneration Nature 453 314 321 18480812
- Habib SJ Chen BC Tsai FC Anastassiadis K Meyer T Betzig E Nusse R 2013 A localized Wnt signal orients asymmetric stem cell division in vitro Science 339 1445 1448 23520113 PMC3966430
- Hattori N Mochizuki S Kishi K Nakajima T Takaishi H D’Armiento J Okada Y 2009 MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing Am. J. Pathol 175 533 546 19590036 PMC2716954
- Heath WR Carbone FR 2013 The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells Nat. Immunol 14 978 985 24048119
- Heller E Kumar KV Grill SW Fuchs E 2014 Forces generated by cell intercalation tow epidermal sheets in mammalian tissue morphogenesis Dev. Cell 28 617 632 24697897 PMC4041280
- Hirsch T Rothoeft T Teig N Bauer JW Pellegrini G De Rosa L Scaglione D Reichelt J Klausseger A Kneisz D 2017 Regeneration of the entire human epidermis using transgenic stem cells Nature Published online November 8, 2017. https://doi.org/10.1038/nature24487 PMC6283270 29144448 · DOI · Paper page
- Hoeck JD Biehs B Kurtova AV Kljavin NM de Sousa EMF Alicke B Koeppen H Modrusan Z Piskol R de Sauvage FJ 2017 Stem cell plasticity enables hair regeneration following Lgr5+ cell loss Nat. Cell Biol 19 666 676 28553937
- Horsley V O’Carroll D Tooze R Ohinata Y Saitou M Obukhanych T Nussenzweig M Tarakhovsky A Fuchs E 2006 Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland Cell 126 597 609 16901790 PMC2424190
- Hsu YC 2015 Theory and practice of lineage tracing Stem Cells 33 3197 3204 26284340 PMC4618107
- Hsu YC Li L Fuchs E 2014 Transit-amplifying cells orchestrate stem cell activity and tissue regeneration Cell 157 935 949 24813615 PMC4041217
- Hsu YC Pasolli HA Fuchs E 2011 Dynamics between stem cells, niche, and progeny in the hair follicle Cell 144 92 105 21215372 PMC3050564
- Huang YL Niehrs C 2014 Polarized Wnt signaling regulates ectodermal cell fate in Xenopus Dev. Cell 29 250 257 24780739
- Ito M Kizawa K Hamada K Cotsarelis G 2004 Hair follicle stem cells in the lower bulge form the secondary germ, a biochemically distinct but functionally equivalent progenitor cell population, at the termination of catagen Differentiation 72 548 557 15617565
- Ito M Liu Y Yang Z Nguyen J Liang F Morris RJ Cotsarelis G 2005 Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis Nat. Med 11 1351 1354 16288281
- Ito M Yang Z Andl T Cui C Kim N Millar SE Cotsarelis G 2007 Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding Nature 447 316 320 17507982
- Jamora C DasGupta R Kocieniewski P Fuchs E 2003 Links between signal transduction, transcription and adhesion in epithelial bud development Nature 422 317 322 12646922 PMC2424170
- Jensen KB Collins CA Nascimento E Tan DW Frye M Itami S Watt FM 2009 Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis Cell Stem Cell 4 427 439 19427292 PMC2698066
- Kawakami Y Rodriguez Esteban C Raya M Kawakami H Marti M Dubova I Izpisua Belmonte JC 2006 Wnt/beta-catenin signaling regulates vertebrate limb regeneration Genes Dev 20 3232 3237 17114576 PMC1686599
- Keyes BE Segal JP Heller E Lien WH Chang CY Guo X Oristian DS Zheng D Fuchs E 2013 Nfatc1 orchestrates aging in hair follicle stem cells Proc. Natl. Acad. Sci. USA 110 E4950 E4959 24282298 PMC3870727
- Knoblich JA 2008 Mechanisms of asymmetric stem cell division Cell 132 583 597 18295577
- Kong HH Segre JA 2017 The molecular revolution in cutaneous biology: investigating the skin microbiome J. Invest. Dermatol 137 e119 e122 28411842
- Lam AK Phillips BT 2017 Wnt signaling polarizes C. elegans asymmetric cell divisions during development Results Probl. Cell Differ 61 83 114 28409301 PMC6057142
- Langton AK Herrick SE Headon DJ 2008 An extended epidermal response heals cutaneous wounds in the absence of a hair follicle stem cell contribution J. Invest. Dermatol 128 1311 1318 18037901
- Legue E Sequeira I Nicolas JF 2010 Hair follicle renewal: authentic morphogenesis that depends on a complex progression of stem cell lineages Development 137 569 577 20110322
- Levy V Lindon C Harfe BD Morgan BA 2005 Distinct stem cell populations regenerate the follicle and interfollicular epidermis Dev. Cell 9 855 861 16326396
- Lim X Tan SH Koh WL Chau RM Yan KS Kuo CJ van Amerongen R Klein AM Nusse R 2013 Interfollicular epidermal stem cells self-renew via autocrine Wnt signaling Science 342 1226 1230 24311688 PMC4081860
- Lu CP Polak L Keyes BE Fuchs E 2016 Spatiotemporal antagonism in mesenchymal-epithelial signaling in sweat versus hair fate decision Science 354 https://doi.org/10.1126/science.aah6102 PMC5333576 28008008 · DOI · Paper page
- Mascre G Dekoninck S Drogat B Youssef KK Brohee S Sotiropoulou PA Simons BD Blanpain C 2012 Distinct contribution of stem and progenitor cells to epidermal maintenance Nature 489 257 262 22940863
- Mesa KR Rompolas P Zito G Myung P Sun TY Brown S Gonzalez DG Blagoev KB Haberman AM Greco V 2015 Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool Nature 522 94 97 25849774 PMC4457634
- Miyoshi H Ajima R Luo CT Yamaguchi TP Stappenbeck TS 2012 Wnt5a potentiates TGF-beta signaling to promote colonic crypt regeneration after tissue injury Science 338 108 113 22956684 PMC3706630
- Morris RJ Liu Y Marles L Yang Z Trempus C Li S Lin JS Sawicki JA Cotsarelis G 2004 Capturing and profiling adult hair follicle stem cells Nat. Biotechnol 22 411 417 15024388
- Muller-Rover S Handjiski B van der Veen C Eichmuller S Foitzik K McKay IA Stenn KS Paus R 2001 A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages J. Invest. Dermatol 117 3 15 11442744
- Nijhof JG Braun KM Giangreco A van Pelt C Kawamoto H Boyd RL Willemze R Mullenders LH Watt FM de Gruijl FR 2006 The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells Development 133 3027 3037 16818453
- Noramly S Morgan BA 1998 BMPs mediate lateral inhibition at successive stages in feather tract development Development 125 3775 3787 9729486
- Nowak JA Polak L Pasolli HA Fuchs E 2008 Hair follicle stem cells are specified and function in early skin morphogenesis Cell Stem Cell 3 33 43 18593557 PMC2877596
- Nusse R Clevers H 2017 Wnt/beta-catenin signaling, disease, and emerging therapeutic modalities Cell 169 985 999 28575679
- Okada A Tomasetto C Lutz Y Bellocq JP Rio MC Basset P 1997 Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of pro-gelatinase A J. Cell Biol 137 67 77 9105037 PMC2139851
- Oshima H Rochat A Kedzia C Kobayashi K Barrandon Y 2001 Morphogenesis and renewal of hair follicles from adult multipotent stem cells Cell 104 233 245 11207364
- Ouspenskaia T Matos I Mertz AF Fiore VF Fuchs E 2016 WNT-SHH antagonism specifies and expands stem cells prior to niche formation Cell 164 156 169 26771489 PMC4850916
- Page ME Lombard P Ng F Gottgens B Jensen KB 2013 The epidermis comprises autonomous compartments maintained by distinct stem cell populations Cell Stem Cell 13 471 482 23954751 PMC3793873
- Park S Gonzalez DG Guirao B Boucher JD Cockburn K Marsh ED Mesa KR Brown S Rompolas P Haberman AM 2017 Tissue-scale coordination of cellular behaviour promotes epidermal wound repair in live mice Nat. Cell Biol 19 155 163 28248302 PMC5581297
- Petersen CP Reddien PW 2009 A wound-induced Wnt expression program controls planarian regeneration polarity Proc. Natl. Acad. Sci. USA 106 17061 17066 19805089 PMC2743725
- Plikus MV Mayer JA de la Cruz D Baker RE Maini PK Maxson R Chuong CM 2008 Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration Nature 451 340 344 18202659 PMC2696201
- Plikus MV Widelitz RB Maxson R Chuong CM 2009 Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity Int. J. Dev. Biol 53 857 868 19378257 PMC2759942
- Plikus MV Chuong CM 2014 Macroenvironmental regulation of hair cycling and collective regenerative behavior Cold Spring Harb. Perspect. Med 4 a015198 24384813 PMC3869280
- Potten CS Saffhill R Maibach HI 1987 Measurement of the transit time for cells through the epidermis and stratum corneum of the mouse and Guinea-pig Cell Tissue Kinet 20 461 472 3450396
- Qiao L Gao H Zhang T Jing L Xiao C Xiao Y Luo N Zhu H Meng W Xu H 2014 Snail modulates the assembly of fibronectin via alpha5 integrin for myocardial migration in zebrafish embryos Sci. Rep 4 4470 24667151 PMC3966048
- Rabbani P Takeo M Chou W Myung P Bosenberg M Chin L Taketo MM Ito M 2011 Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration Cell 145 941 955 21663796 PMC3962257
- Rompolas P Mesa KR Greco V 2013 Spatial organization within a niche as a determinant of stem-cell fate Nature 502 513 518 24097351 PMC3895444
- Rompolas P Mesa KR Kawaguchi K Park S Gonzalez D Brown S Boucher J Klein AM Greco V 2016 Spatiotemporal coordination of stem cell commitment during epidermal homeostasis Science 352 1471 1474 27229141 PMC4958018
- Roy E Neufeld Z Cerone L Wong HY Hodgson S Livet J Khosrotehrani K 2016 Bimodal behaviour of interfollicular epidermal progenitors regulated by hair follicle position and cycling EMBO J 5 2658 2670 PMC5167353 27797819
- Sada A Jacob F Leung E Wang S White BS Shalloway D Tumbar T 2016 Defining the cellular lineage hierarchy in the interfollicular epidermis of adult skin Nat. Cell Biol 18 619 631 27183471 PMC4884151
- Sendoel A Dunn JG Rodriguez EH Naik S Gomez NC Hurwitz B Levorse J Dill BD Schramek D Molina H 2017 Translation from unconventional 5’ start sites drives tumour initiation Nature 541 494 499 28077873 PMC5287289
- Sennett R Wang Z Rezza A Grisanti L Roitershtein N Sicchio C Mok KW Heitman NJ Clavel C Ma’ayan A 2015 An integrated transcriptome atlas of embryonic hair follicle progenitors, their niche, and the developing skin Dev. Cell 34 577 591 26256211 PMC4573840
- Shook B Rivera Gonzalez G Ebmeier S Grisotti G Zwick R Horsley V 2016 The role of adipocytes in tissue regeneration and stem cell niches Annu. Rev. Cell Dev. Biol 32 609 631 27146311 PMC5157158
- Snippert HJ Haegebarth A Kasper M Jaks V van Es JH Barker N van de Wetering M van den Born M Begthel H Vries RG 2010 Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin Science 327 1385 1389 20223988
- St-Jacques B Dassule HR Karavanova I Botchkarev VA Li J Danielian PS McMahon JA Lewis PM Paus R McMahon AP 1998 Sonic hedgehog signaling is essential for hair development Curr. Biol 8 1058 1068 9768360
- Stevens LJ Page-McCaw A 2012 A secreted MMP is required for re-epithelialization during wound healing Mol. Biol. Cell 23 1068 1079 22262460 PMC3302734
- Stoick-Cooper CL Weidinger G Riehle KJ Hubbert C Major MB Fausto N Moon RT 2007 Distinct Wnt signaling pathways have opposing roles in appendage regeneration Development 134 479 489 17185322
- Sugioka K Mizumoto K Sawa H 2011 Wnt regulates spindle asymmetry to generate asymmetric nuclear beta-catenin in C. elegans Cell 146 942 954 21925317
- Taylor G Lehrer MS Jensen PJ Sun TT Lavker RM 2000 Involvement of follicular stem cells in forming not only the follicle but also the epidermis Cell 102 451 461 10966107
- Tumbar T Guasch G Greco V Blanpain C Lowry WE Rendl M Fuchs E 2004 Defining the epithelial stem cell niche in skin Science 303 359 363 14671312 PMC2405920
- Vasioukhin V Degenstein L Wise B Fuchs E 1999 The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin Proc. Natl. Acad. Sci. USA 96 8551 8556 10411913 PMC17554
- Watt FM Green H 1982 Stratification and terminal differentiation of cultured epidermal cells Nature 295 434 436 6895777
- Watt FM Jones PH 1993 Expression and function of the keratinocyte integrins Dev. Suppl 185 192 8049472
- Whyte JL Smith AA Liu B Manzano WR Evans ND Dhamdhere GR Fang MY Chang HY Oro AE Helms JA 2013 Augmenting endogenous Wnt signaling improves skin wound healing PLoS One 8 e76883 24204695 PMC3799989
- Williams SE Ratliff LA Postiglione MP Knoblich JA Fuchs E 2014 Par3-mInsc and Galphai3 cooperate to promote oriented epidermal cell divisions through LGN Nat. Cell Biol 16 758 769 25016959 PMC4159251
- Woo WM Zhen HH Oro AE 2012 Shh maintains dermal papilla identity and hair morphogenesis via a Noggin-Shh regulatory loop Genes Dev 26 1235 1246 22661232 PMC3371411
- Wu X Shen QT Oristian DS Lu CP Zheng Q Wang HW Fuchs E 2011 Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3beta Cell 144 341 352 21295697 PMC3050560
- Yang H Adam RC Ge Y Hua ZL Fuchs E 2017 Epithelial-mesenchymal micro-niches govern stem cell lineage choices Cell 169 483 496.e413 28413068 PMC5510744
- Zielins ER Atashroo DA Maan ZN Duscher D Walmsley GG Hu M Senarath-Yapa K McArdle A Tevlin R Wearda T 2014 Wound healing: an update Regen. Med 9 817 830 25431917
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- Authors
- Gonzales, K. A. U., & Fuchs, E.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Fuchs, Elaine
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2017-11
- Volume
- 43
- Issue
- 4
- Pages
- 387-401
- ISSN
- 1534-5807 (ISSN-L)
- PMC
- PMC5797699
- OpenAlex
- W2769238697
- Cited by
- 414
- References
- 9
- Citations by year
- 2026: 18 · 2025: 44 · 2024: 46 · 2023: 35 · 2022: 63 · 2021: 65 · 2020: 54 · 2019: 52 · 2018: 37
- FWCI
- 9.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (R37-AR27883, R01-AR050452, R01-AR31737)
- Topics
- Health Sciences › Medicine › Urology › Hair Growth and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Keywords
- skin regeneration, epithelial stem cells, stem cell niche, wound healing, skin barrier, epidermis, self-renewal, tissue homeostasis, skin appendages
- MeSH terms
- Animals, Cell Differentiation, Epidermis, Epithelial Cells, Humans, Regeneration, Skin, Stem Cells
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