High Runx1 levels promote a reversible, more-differentiated cell state in hair-follicle stem cells during quiescence

Cell Reports

Volumn 6, Issue 3, 2014, Pages 499-513

  Lee, SongEun ^a   Sada, Aiko ^a   Zhang, Meng ^a   McDermitt, David J ^a   Lu, ShuYang ^a   Kemphues, Kenneth J ^a   Tumbar, Tudorita ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTOME;

ADULT; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DEGENERATION; DOWN REGULATION; HAIR FOLLICLE; HAIR GROWTH; HOMEOSTASIS; IMAGE PROCESSING; IMMUNOFLUORESCENCE; MICROARRAY ANALYSIS; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TRANSGENIC MOUSE; UPREGULATION;

MAMMALIA;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DOWN-REGULATION; GENE EXPRESSION PROFILING; HAIR FOLLICLE; HOMEOSTASIS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; STEM CELLS; TETRACYCLINE; TIME FACTORS;

EID: 84893824405     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.12.039     Document Type: Article

References (31)

1. Barrandon Y., Green H. Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. USA 1987, 84:2302-2306.
2. Blanpain C. Stem cells: Skin regeneration and repair. Nature 2010, 464:686-687.
3. Blyth K., Cameron E.R., Neil J.C. The RUNX genes: gain or loss of function in cancer. Nat. Rev. Cancer 2005, 5:376-387.
4. Ferrell J.E. Bistability, bifurcations, and Waddington's epigenetic landscape. Curr. Biol. 2012, 22:R458-R466.
5. Greco V., Chen T., Rendl M., Schober M., Pasolli H.A., Stokes N., Dela Cruz-Racelis J., Fuchs E. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 2009, 4:155-169.
6. Hoi C.S., Lee S.E., Lu S.Y., McDermitt D.J., Osorio K.M., Piskun C.M., Peters R.M., Paus R., Tumbar T. Runx1 directly promotes proliferation of hair follicle stem cells and epithelial tumor formation in mouse skin. Mol. Cell. Biol. 2010, 30:2518-2536.
7. Hsu Y.C., Pasolli H.A., Fuchs E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 2011, 144:92-105.
8. Ito M., Kizawa K., Hamada K., Cotsarelis G. 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 2004, 72:548-557.
9. Jaks V., Kasper M., Toftgård R. The hair follicle-a stem cell zoo. Exp. Cell Res. 2010, 316:1422-1428.
10. Lee J., Tumbar T. Hairy tale of signaling in hair follicle development and cycling. Semin. Cell Dev. Biol. 2012, 23:906-916.
11. Lee J., Hoi C.S., Lilja K.C., White B.S., Lee S.E., Shalloway D., Tumbar T. Runx1 and p21 synergistically limit the extent of hair follicle stem cell quiescence invivo. Proc. Natl. Acad. Sci. USA 2013, 110:4634-4639.
12. Lien W.H., Guo X., Polak L., Lawton L.N., Young R.A., Zheng D., Fuchs E. Genome-wide maps of histone modifications unwind invivo chromatin states of the hair follicle lineage. Cell Stem Cell 2011, 9:219-232.
13. Morris R.J., Liu Y., Marles L., Yang Z., Trempus C., Li S., Lin J.S., Sawicki J.A., Cotsarelis G. Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 2004, 22:411-417.
14. Müller-Röver S., Handjiski B., van der Veen C., Eichmüller S., Foitzik K., McKay I.A., Stenn K.S., Paus R. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J.Invest. Dermatol. 2001, 117:3-15.
15. Nguyen H., Rendl M., Fuchs E. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 2006, 127:171-183.
16. North T.E., de Bruijn M.F., Stacy T., Talebian L., Lind E., Robin C., Binder M., Dzierzak E., Speck N.A. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 2002, 16:661-672.
17. Osorio K.M., Lee S.E., McDermitt D.J., Waghmare S.K., Zhang Y.V., Woo H.N., Tumbar T. Runx1 modulates developmental, but not injury-driven, hair follicle stem cell activation. Development 2008, 135:1059-1068.
18. Osorio K.M., Lilja K.C., Tumbar T. Runx1 modulates adult hair follicle stem cell emergence and maintenance from distinct embryonic skin compartments. J.Cell Biol. 2011, 193:235-250.
19. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
20. Pournasr B., Khaloughi K., Salekdeh G.H., Totonchi M., Shahbazi E., Baharvand H. Concise review: alchemy of biology: generating desired cell types from abundant and accessible cells. Stem Cells 2011, 29:1933-1941.
21. Rompolas P., Mesa K.R., Greco V. Spatial organization within a niche as a determinant of stem-cell fate. Nature 2013, 502:513-518.
22. Samokhvalov I.M., Samokhvalova N.I., Nishikawa S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 2007, 446:1056-1061.
23. Scheitz C.J., Lee T.S., McDermitt D.J., Tumbar T. Defining atissue stem cell-driven Runx1/Stat3 signalling axis in epithelial cancer. EMBO J. 2012, 31:4124-4139.
24. Schwitalla S., Fingerle A.A., Cammareri P., Nebelsiek T., Göktuna S.I., Ziegler P.K., Canli O., Heijmans J., Huels D.J., Moreaux G., et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 152:25-38.
25. Simons B.D., Clevers H. Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 2011, 145:851-862.
26. Spradling A., Fuller M.T., Braun R.E., Yoshida S. Germline stem cells. Cold Spring Harb. Perspect. Biol. 2011, 3:a002642.
27. Tumbar T., Guasch G., Greco V., Blanpain C., Lowry W.E., Rendl M., Fuchs E. Defining the epithelial stem cell niche in skin. Science 2004, 303:359-363.
28. Waddington C.H. The Strategy of the Gene 1957, George Allen and Unwin, London.
29. Yanger K., Zong Y., Maggs L.R., Shapira S.N., Maddipati R., Aiello N.M., Thung S.N., Wells R.G., Greenbaum L.E., Stanger B.Z. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev. 2013, 27:719-724.
30. Zhang Y.V., Cheong J., Ciapurin N., McDermitt D.J., Tumbar T. Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 2009, 5:267-278.
31. 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 2010, 9:1504-1510.