Defining the cellular lineage hierarchy in the interfollicular epidermis of adult skin

Nature Cell Biology

Volumn 18, Issue 6, 2016, Pages 619-631

  Sada, Aiko ^a   Jacob, Fadi ^a   Leung, Eva ^a   Wang, Sherry ^a   White, Brian S ^b,c   Shalloway, David ^a   Tumbar, Tudorita ^a  

^a Department of Obstetrics Gynecology   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DLX1 PROTEIN; EXCITATORY AMINO ACID TRANSPORTER 1; MARKER; TENASCIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL LINEAGE; CELL PROLIFERATION; CELL TRANSPORT; CONTROLLED STUDY; DILUTION; EPIDERMAL STEM CELL; EPIDERMIS; INTERFOLLICULAR EPIDERMIS; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGENERATION; SKIN; SKIN INJURY; AGING; ANIMAL; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; HOMEOSTASIS; PHYSIOLOGY; PROCEDURES; STAINING; STEM CELL;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; EPIDERMIS; GENE EXPRESSION PROFILING; HOMEOSTASIS; MICE; SKIN; STAINING AND LABELING; STEM CELLS;

EID: 84968615921     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3359     Document Type: Article

References (61)

1. Sada, A. & Tumbar, T. New insights into mechanisms of stem cell daughter fate determination in regenerative tissues. Int. Rev. Cell Mol. Biol. 300, 1-50 (2013).
2. Foudi, A. et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 27, 84-90 (2009).
3. Wilson, A. et al. Hematopoietic stem cells reversibly switch from dormancy to selfrenewal during homeostasis and repair. Cell 135, 1118-1129 (2008).
4. Zhang, Y. V., Cheong, J., Ciapurin, N., McDermitt, D. J. & Tumbar, T. Distinct selfrenewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5, 267-278 (2009).
5. Waghmare, S. K. et al. Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J. 27, 1309-1320 (2008).
6. Buczacki, S. J. et al. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495, 65-69 (2013).
7. Li, L. & Clevers, H. Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545 (2010).
8. Fuchs, E. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137, 811-819 (2009).
9. Takeda, N. et al. Interconversion between intestinal stem cell populations in distinct niches. Science 334, 1420-1424 (2011).
10. Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (2007).
11. Sangiorgi, E. & Capecchi, M. R. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40, 915-920 (2008).
12. Montgomery, R. K. et al. Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. Proc. Natl. Acad. Sci. USA 108, 179-184 (2010).
13. Metcalfe, C., Kljavin, N. M., Ybarra, R. & de Sauvage, F. J. Lgr5C stem cells are indispensable for radiation-induced intestinal regeneration. Cell Stem Cell 14, 149-159 (2014).
14. Tian, H. et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255-259 (2011).
15. Ritsma, L. et al. Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging. Nature 507, 362-365 (2014).
16. Jaks, V., Kasper, M. & Toftgard, R. The hair follicle-a stem cell zoo. Exp. Cell Res. 316, 1422-1428 (2010).
17. Plikus, M. V. et al. Epithelial stem cells and implications for wound repair. Sem. Cell Dev. Biol. 23, 946-953 (2012).
18. Dai, X. & Segre, J. A. Transcriptional control of epidermal specification and differentiation. Curr. Opin. Genet. Dev. 14, 485-491 (2004).
19. Potten, C. S., Saffhill, R. & Maibach, H. I. 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 (1987).
20. Bickenbach, J. R. Identification and behavior of label-retaining cells in oral mucosa and skin. J. Dent. Res. 60, 1611-1620 (1981).
21. Tumbar, T. et al. Defining the epithelial stem cell niche in skin. Science 303, 359-363 (2004).
22. Schluter, H., Paquet-Fifield, S., Gangatirkar, P., Li, J. & Kaur, P. Functional characterization of quiescent keratinocyte stem cells and their progeny reveals a hierarchical organization in human skin epidermis. Stem Cells 29, 1256-1268 (2011).
23. Clayton, E. et al. A single type of progenitor cell maintains normal epidermis. Nature 446, 185-189 (2007).
24. Doupe, D. P., Klein, A. M., Simons, B. D. & Jones, P. H. The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev. Cell 18, 317-323 (2010).
25. Lim, X. et al. Interfollicular epidermal stem cells self-renew via autocrine Wnt signaling. Science 342, 1226-1230 (2013).
26. Mascre, G. et al. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489, 257-262 (2012).
27. Gomez, C. et al. The interfollicular epidermis of adult mouse tail comprises two distinct cell lineages that are differentially regulated by Wnt, Edaradd, and Lrig1. Stem Cell Rep. 1, 19-27 (2013).
28. Braun, K. M. et al. Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130, 5241-5255 (2003).
29. Chang, H. & Nathans, J. Responses of hair follicle-associated structures to loss of planar cell polarity signaling. Proc. Natl. Acad. Sci. USA 110, E908-E917 (2013).
30. Zhang, Y. V., White, B. S., Shalloway, D. I. & Tumbar, T. Stem cell dynamics in mouse hair follicles: A story from cell division counting and single cell lineage tracing. Cell Cycle 9, 1504-1510 (2010).
31. Muller-Rover, S. et al. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J. Invest. Dermatol. 117, 3-15 (2001).
32. Trempus, C. S. et al. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Invest. Dermatol. 120, 501-511 (2003).
33. Blanpain, C., Lowry, W. E., Geoghegan, A., Polak, L. & Fuchs, E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118, 635-648 (2004).
34. Lien, W. H. et al. Genome-wide maps of histone modifications unwind in vivo chromatin states of the hair follicle lineage. Cell Stem Cell 9, 219-232 (2011).
35. Edmondson, S. R. et al. Insulin-like growth factor binding protein-3 (IGFBP-3) localizes to and modulates proliferative epidermal keratinocytes in vivo. Br. J. Dermatol. 152, 225-230 (2005).
36. Weger, N. & Schlake, T. Igf-I signalling controls the hair growth cycle and the differentiation of hair shafts. J. Invest. Dermatol. 125, 873-882 (2005).
37. Firth, S. M. & Baxter, R. C. Cellular actions of the insulin-like growth factor binding proteins. Endocr. Rev. 23, 824-854 (2002).
38. Lee, J. et al. Runx1 and p21 synergistically limit the extent of hair follicle stem cell quiescence in vivo. Proc. Natl. Acad. Sci. USA 110, 4634-4639 (2013).
39. Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013 (2011).
40. Nathans, J.Generation of an inducible Slc1a3-cre/ERT transgenic allele. MGI Direct Data Submission: [MGI Ref ID J:157151] (2010).
41. Klein, A. M. & Simons, B. D. Universal patterns of stem cell fate in cycling adult tissues. Development 138, 3103-3111 (2011).
42. Ivanova, A. et al. In vivo genetic ablation by Cre-mediated expression of diphtheria toxin fragment A. Genesis 43, 129-135 (2005).
43. Coulombe, P. A. Wound epithelialization: accelerating the pace of discovery. J. Invest. Dermatol. 121, 219-230 (2003).
44. Mackie, E. J., Halfter, W. & Liverani, D. Induction of tenascin in healing wounds. J. Cell Biol. 107, 2757-2767 (1988).
45. Roshan, A. et al. Human keratinocytes have two interconvertible modes of proliferation. Nat. Cell Biol. 18, 145-156 (2016).
46. Paquet-Fifield, S. et al. A role for pericytes as microenvironmental regulators of human skin tissue regeneration. J. Clin. Invest. 119, 2795-2806 (2009).
47. Lopez-Rovira, T., Silva-Vargas, V. & Watt, F. M. Different consequences of 1 integrin deletion in neonatal and adult mouse epidermis reveal a context-dependent role of integrins in regulating proliferation, differentiation, and intercellular communication. J. Invest. Dermatol. 125, 1215-1227 (2005).
48. Ishitsuka, Y. et al. Pituitary tumor-transforming gene 1 enhances proliferation and suppresses early differentiation of keratinocytes. J. Invest. Dermatol. 132, 1775-1784 (2012).
49. Sugiyama-Nakagiri, Y., Ohuchi, A., Hachiya, A. & Kitahara, T. Involvement of IGF-1/IGFBP-3 signaling on the conspicuousness of facial pores. Arch. Dermatol. Res. 302, 661-667 (2010).
50. Diamond, I., Owolabi, T., Marco, M., Lam, C. & Glick, A. Conditional gene expression in the epidermis of transgenic mice using the tetracycline-regulated transactivators tTA and rTA linked to the keratin 5 promoter. J. Invest. Dermatol. 115, 788-794 (2000).
51. Vasioukhin, V., Degenstein, L., Wise, B. & Fuchs, E. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl. Acad. Sci. USA 96, 8551-8556 (1999).
52. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neurosci. 13, 133-140 (2010).
53. Waghmare, S.K. Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J 27, 1309-1320 (2008).
54. Tumbar, T. et al. Defining the epithelial stem cell niche in skin. Science 303, 359-363 (2004).
55. Lee, J. et al. Runx1 and p21 synergistically limit the extent of hair follicle stem cell quiescence in vivo. Proc Natl Acad Sci U S A 110, 4634-4639 (2013).
56. Clayton, E. et al. A single type of progenitor cell maintains normal epidermis. Nature 446, 185-189 (2007).
57. Mascre, G. et al. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489, 257-262 (2012).
58. Claeskens, G. & Hjort, N. L. Model Selection and Model Averaging (Cambridge University Press, 2008).
59. Lechler, T. & Fuchs, E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 71, 275-280 (2005).
60. Klein, A.M. & Simons, B.D. Universal patterns of stem cell fate in cycling adult tissues. Development 138, 3103-3111 (2011).
61. Potten, C.S., Saffhill, R. & Maibach, H.I. 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 (1987).