Runx1 and p21 synergistically limit the extent of hair follicle stem cell quiescence in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 12, 2013, Pages 4634-4639

  Lee, Jayhun ^a   Hoi, Charlene S L ^a,b   Lilja, Karin C ^a,c   White, Brian S ^a,d   Lee, Song Eun ^a   Shalloway, David ^a   Tumbar, Tudorita ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AML1; H2B GFP; Malignancy; Pulse chase; Skin

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; PROTEIN P15; PROTEIN P21; TRANSCRIPTION FACTOR RUNX1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE ARREST; CELL FUNCTION; CELL PROLIFERATION; CELL QUIESCENCE; CONTROLLED STUDY; HAIR FOLLICLE; HAIR FOLLICLE STEM CELL; IN VIVO STUDY; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; CELL LINE; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA 2 SUBUNIT; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DOWN-REGULATION; HAIR FOLLICLE; MICE; MICE, KNOCKOUT; P21-ACTIVATED KINASES; STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 84875277640     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213015110     Document Type: Article

References (41)

1. Orford KW, Scadden DT (2008) Deconstructing stem cell self-renewal: Genetic insights into cell-cycle regulation. Nat Rev Genet 9(2):115-128.
2. Fuchs E (2009) The tortoise and the hair: Slow-cycling cells in the stem cell race. Cell 137(5):811-819.
3. Tesio M, Trumpp A (2011) Breaking the cell cycle of HSCs by p57 and friends. Cell Stem Cell 9(3):187-192.
4. Matsumoto A, et al. (2011) p57 is required for quiescence and maintenance of adult hematopoietic stem cells. Cell Stem Cell 9(3):262-271.
5. Zou P, et al. (2011) p57(Kip2) and p27(Kip1) cooperate to maintain hematopoietic stem cell quiescence through interactions with Hsc70. Cell Stem Cell 9(3):247-261.
6. Cheng T, et al. (2000) Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 287(5459):1804-1808.
7. van Os R, et al. (2007) A limited role for p21Cip1/Waf1 in maintaining normal hematopoietic stem cell functioning. Stem Cells 25(4):836-843.
8. Viale A, et al. (2009) Cell-cycle restriction limits DNA damage and maintains selfrenewal of leukaemia stem cells. Nature 457(7225):51-56.
9. Foudi A, et al. (2009) Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 27(1):84-90.
10. Waghmare SK, et al. (2008) Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J 27(9):1309-1320.
11. Cotsarelis G (2006) Epithelial stem cells: A folliculocentric view. J Invest Dermatol 126(7):1459-1468.
12. Tumbar T (2012) Ontogeny and homeostasis of adult epithelial skin stem cells. Stem Cell Rev Rep 8(2):561-576.
13. Zhang YV, Cheong J, Ciapurin N, McDermitt DJ, Tumbar T (2009) Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5(3):267-278.
14. Speck NA, Gilliland DG (2002) Core-binding factors in haematopoiesis and leukaemia. Nat Rev Cancer 2(7):502-513.
15. Osorio KM, et al. (2008) Runx1 modulates developmental, but not injury-driven, hair follicle stem cell activation. Development 135(6):1059-1068.
16. Hoi CS, et al. (2010) Runx1 directly promotes proliferation of hair follicle stem cells and epithelial tumor formation in mouse skin. Mol Cell Biol 30(10):2518-2536.
17. Osorio KM, Lilja KC, Tumbar T (2011) Runx1 modulates adult hair follicle stem cell emergence and maintenance from distinct embryonic skin compartments. J Cell Biol 193(1):235-250.
18. Choudhury AR, et al. (2007) Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation. Nat Genet 39(1):99-105.
19. Topley GI, Okuyama R, Gonzales JG, Conti C, Dotto GP (1999) p21(WAF1/Cip1) functions as a suppressor of malignant skin tumor formation and a determinant of keratinocyte stem-cell potential. Proc Natl Acad Sci USA 96(16):9089-9094.
20. Weinberg WC, et al. (1999) Genetic deletion of p21WAF1 enhances papilloma formation but not malignant conversion in experimental mouse skin carcinogenesis. Cancer Res 59(9):2050-2054.
21. Zhou BP, et al. (2001) Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells. Nat Cell Biol 3(3):245-252.
22. Yu M, et al. (2012) Direct recruitment of polycomb repressive complex 1 to chromatin by core binding transcription factors. Mol Cell 45(3):330-343.
23. Tumbar T, et al. (2004) Defining the epithelial stem cell niche in skin. Science 303(5656): 359-363.
24. Hsu YC, Pasolli HA, Fuchs E (2011) Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144(1):92-105.
25. Zhang YV, White BS, Shalloway DI, Tumbar T (2010) Stem cell dynamics in mouse hair follicles: A story from cell division counting and single cell lineage tracing. Cell Cycle 9(8):1504-1510.
26. Suzuki A, Tsutomi Y, Akahane K, Araki T, Miura M (1998) Resistance to Fas-mediated apoptosis: Activation of caspase 3 is regulated by cell cycle regulator p21WAF1 and IAP gene family ILP. Oncogene 17(8):931-939.
27. Willis S, Day CL, Hinds MG, Huang DC (2003) The Bcl-2-regulated apoptotic pathway. J Cell Sci 116(Pt 20):4053-4056.
28. Kemp CJ (2005) Multistep skin cancer in mice as a model to study the evolution of cancer cells. Semin Cancer Biol 15(6):460-473.
29. Lapouge G, et al. (2011) Identifying the cellular origin of squamous skin tumors. Proc Natl Acad Sci USA 108(18):7431-7436.
30. White AC, et al. (2011) Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proc Natl Acad Sci USA 108(18):7425-7430.
31. Scheitz CJ, Lee TS, McDermitt DJ, Tumbar T (2012) Defining a tissue stem cell-driven Runx1/Stat3 signalling axis in epithelial cancer. EMBO J 31(21):4124-4139.
32. Hennings H, et al. (1993) FVB/N mice: An inbred strain sensitive to the chemical induction of squamous cell carcinomas in the skin. Carcinogenesis 14(11):2353-2358.
33. Devgan V, Mammucari C, Millar SE, Brisken C, Dotto GP (2005) p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 19(12):1485-1495.
34. de Nooij JC, Letendre MA, Hariharan IK (1996) A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87(7):1237-1247.
35. Ferrándiz N, et al. (2012) p21 as a transcriptional co-repressor of S-phase and mitotic control genes. PLoS ONE 7(5):e37759.
36. Marques-Torrejon MA, et al. (2012) Cyclin-dependent kinase inhibitor p21 controls adult neural stem cell expansion by regulating Sox2 gene expression. Cell Stem Cell 12(1):88-100.
37. Pippa R, et al. (2012) p27(Kip1) represses transcription by direct interaction with p130/E2F4 at the promoters of target genes. Oncogene 31(38):4207-4220.
38. Attias H (1999) Advances in Neural Information Processing Systems 12, eds Solla SA, Leen TK, Muller K-R (MIT Press, Cambridge, MA), pp 209-215.
39. Bishop CM (2006) Pattern Recognition and Machine Learning (Springer, New York).
40. Boedigheimer MJ, Ferbas J (2008) Mixture modeling approach to flow cytometry data. Cytometry A 73(5):421-429.
41. Pyne S, et al. (2009) Automated high-dimensional flow cytometric data analysis. Proc Natl Acad Sci USA 106(21):8519-8524.