An RNA interference screen uncovers a new molecule in stem cell self-renewal and long-term regeneration

Nature

Volumn 485, Issue 7396, 2012, Pages 104-108

  Chen, Ting ^a   Heller, Evan ^a   Beronja, Slobodan ^a   Oshimori, Naoki ^a   Stokes, Nicole ^a   Fuchs, Elaine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SHORT HAIRPIN RNA; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX1; UNCLASSIFIED DRUG;

BIOASSAY; CYTOLOGY; DEVELOPMENTAL BIOLOGY; GENE EXPRESSION; HAIR; HOMEOSTASIS; HOMINID; PHYSIOLOGY; PROTEIN; RNA; SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; HAIR FOLLICLE; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELL NICHE; TISSUE REGENERATION; TRANSCRIPTION REGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL PROLIFERATION; EPIDERMIS; FEMALE; HAIR FOLLICLE; MALE; MICE; REGENERATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELLS; T-BOX DOMAIN PROTEINS;

ANIMALIA; PYRONIA TITHONUS;

EID: 84860508493     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10940     Document Type: Article

References (32)

1. Li, L. & Clevers, H. Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545 (2010).
2. Fuchs, E. The tortoise and the hair: slow-cycling cells in the stemcell race. Cell 137, 811-819 (2009).
3. Zon, L. I. Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 453, 306-313 (2008). (Pubitemid 351693136)
4. He, S.,Nakada, D.&Morrison, S. J.Mechanismsof stemcell self-renewal. Annu.Rev. Cell Dev. Biol. 25, 377-406 (2009).
5. 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). (Pubitemid 39179715)
6. Greco, V. et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155-169 (2009).
7. Watt, F. M.&Jensen, K. B. Epidermalstemcell diversity andquiescence.EMBOMol. Med. 1, 260-267 (2009).
8. Ying, Q. L., Nichols, J., Chambers, I. & Smith, A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292 (2003). (Pubitemid 37487702)
9. Molofsky, A. V. et al.Bmi-1 dependence distinguishes neural stemcell self-renewal from progenitor proliferation. Nature 425, 962-967 (2003). (Pubitemid 37376927)
10. Nishino, J., Kim, I., Chada, K. & Morrison, S. J. Hmga2 promotes neural stem cell self-renewal in young but not old miceby reducingp16Ink4a andp19Arf Expression. Cell 135, 227-239 (2008).
11. Topley, G. I., Okuyama, R., Gonzales, J. G., Conti, C. & Dotto, G. P. p21WAF1/Cip1 functions as a suppressor of malignant skin tumor formation and a determinant of keratinocyte stem-cell potential. Proc. Natl Acad. Sci. USA 96, 9089-9094 (1999). (Pubitemid 29374712)
12. Kippin, T. E., Martens, D. J. & van der Kooy, D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 19, 756-767 (2005). (Pubitemid 40395086)
13. Tumbar, T. et al. Defining the epithelial stem cell niche in skin. Science 303, 359-363 (2004). (Pubitemid 38095773)
14. 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 72, 548-557 (2004). (Pubitemid 41702109)
15. Hsu, Y. C., Pasolli, H. A. & Fuchs, E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144, 92-105 (2011).
16. Osorio, K. M. et al. Runx1 modulates developmental, but not injury-driven, hair follicle stem cell activation. Development 135, 1059-1068 (2008). (Pubitemid 351578134)
17. Aggarwal, V. S. et al. Mesodermal Tbx1 is required for patterning the proximal mandible in mice. Dev. Biol. 344, 669-681 (2010).
18. Chen, L., Fulcoli, F. G., Tang, S. & Baldini, A. Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ. Res. 105, 842-851 (2009).
19. 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).
20. Xu, H. et al. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131, 3217-3227 (2004). (Pubitemid 39077444)
21. Vasioukhin, V., Degenstein, L., Wise, B. & Fuchs, E. The magical touch: genome targeting in epidermal stemcells induced by tamoxifen application tomouse skin. Proc. Natl Acad. Sci. USA 96, 8551-8556 (1999). (Pubitemid 29354829)
22. Korchynskyi, O. & ten Dijke, P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891 (2002). (Pubitemid 34968524)
23. Hollnagel, A., Oehlmann, V., Heymer, J., Ruther, U. & Nordheim, A. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J. Biol. Chem. 274, 19838-19845 (1999).
24. Fulcoli, F. G., Huynh, T., Scambler, P. J. & Baldini, A. Tbx1 regulates the BMP-Smad1 pathway in a transcription independent manner. PLoS ONE 4, e6049 (2009).
25. Blessing, M.,Nanney, L. B., King, L. E., Jones, C. M.&Hogan, B. L. Transgenic mice as a model to study the role of TGF-b-related molecules in hair follicles. Genes Dev. 7, 204-215 (1993). (Pubitemid 23084397)
26. Botchkarev, V. A. et al.Noggin is amesenchymally derived stimulator of hair-follicle induction. Nature Cell Biol. 1, 158-164 (1999). (Pubitemid 129656020)
27. Kulessa, H., Turk, G. & Hogan, B. L. Inhibition of Bmp signaling affects growth and differentiation in the anagen hair follicle. EMBO J. 19, 6664-6674 (2000). (Pubitemid 32011659)
28. Kobielak, K., Stokes, N., de la Cruz, J., Polak, L.& Fuchs, E. Loss of a quiescent niche but not follicle stemcells in the absence of bonemorphogenetic protein signaling. Proc. Natl Acad. Sci. USA 104, 10063-10068 (2007). (Pubitemid 47175263)
29. Andl, T. et al. Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131, 2257-2268 (2004). (Pubitemid 38877635)
30. Oshimori, N. & Fuchs, E. Paracrine TGF-b signaling counterbalances BMPmediated repression in hair follicle stem cell activation. Cell Stem Cell 10, 63-75 (2012).
31. R Foundation for Statistical Computing. The R Project for Statistical Computing Æhttp://www.r-project.orgæ (2011).
32. Beronja, S., Livshits, G., Williams, S. & Fuchs, E. Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nature Med. 16, 821-827 (2010).