Runx1 modulates adult hair follicle stem cell emergence and maintenance from distinct embryonic skin compartments

Journal of Cell Biology

Volumn 193, Issue 1, 2011, Pages 235-250

  Osorio, Karen M ^a   Lilja, Karin C ^a   Tumbar, Tudorita ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOID ENHANCER FACTOR 1; TRANSCRIPTION FACTOR RUNX1; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DERMIS; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EPIDERMIS; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM; EPITHELIUM CELL; FEMALE; GENETIC ENGINEERING; HAIR; HAIR FOLLICLE; HAIR FOLLICLE STEM CELL; HAIR GROWTH; HEMATOPOIESIS; KERATINOCYTE; MALE; MESENCHYME; MESENCHYME CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PARACRINE SIGNALING; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKIN; SKIN FUNCTION; STEM CELL;

ANIMALS; CELL ADHESION; CELL MOVEMENT; CORE BINDING FACTOR ALPHA 2 SUBUNIT; HAIR FOLLICLE; LYMPHOID ENHANCER-BINDING FACTOR 1; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; SKIN; STEM CELLS; WNT PROTEINS;

EID: 79955487227     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201006068     Document Type: Article

References (48)

1. Andl, T., S.T. Reddy, T. Gaddapara, and S.E. Millar. 2002. WNT signals are required for the initiation of hair follicle development. Dev. Cell. 2:643-653. doi:10.1016/S1534-5807(02)00167-3.
2. Balciunaite, G., M.P. Keller, E. Balciunaite, L. Piali, S. Zuklys, Y.D. Mathieu, J. Gill, R. Boyd, D.J. Sussman, and G.A. Holländer. 2002. Wnt glycoproteins regulate the expression of FoxN1, the gene defective in nude mice. Nat. Immunol. 3:1102-1108. doi:10.1038/ni850.
3. Blanpain, C., and E. Fuchs. 2009. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10:207-217. doi:10.1038/nrm2636.
4. Chen, A.I., J.C. de Nooij, and T.M. Jessell. 2006. Graded activity of transcription factor Runx3 specifies the laminar termination pattern of sensory axons in the developing spinal cord. Neuron. 49:395-408. doi:10.1016/j.neuron.2005.12.028.
5. Chien, A.J., W.H. Conrad, and R.T. Moon. 2009. A Wnt survival guide: from flies to human disease. J. Invest. Dermatol. 129:1614-1627. doi:10.1038/jid.2008.445.
6. DasGupta, R., and E. Fuchs. 1999. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 126:4557-4568.
7. Dzierzak, E., and N.A. Speck. 2008. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 9:129-136. doi:10.1038/ni1560.
8. Fuchs, E. 2009. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell. 137:811-819. doi:10.1016/j.cell.2009.05.002.
9. Gat, U., R. DasGupta, L. Degenstein, and E. Fuchs. 1998. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell. 95:605-614. doi:10.1016/S0092-8674(00)81631-1.
10. Growney, J.D., H. Shigematsu, Z. Li, B.H. Lee, J. Adelsperger, R. Rowan, D.P. Curley, J.L. Kutok, K. Akashi, I.R. Williams, et al. 2005. Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood. 106:494-504. doi:10.1182/blood-2004-08-3280.
11. Hoi, C.S., S.E. Lee, S.Y. Lu, D.J. McDermitt, K.M. Osorio, C.M. Piskun, R.M. Peters, R. Paus, and T. Tumbar. 2010. Runx1 directly promotes proliferation of hair follicle stem cells and epithelial tumor formation in mouse skin. Mol. Cell. Biol. 30:2518-2536. doi:10.1128/MCB.01308-09.
12. Horsley, V., A.O. Aliprantis, L. Polak, L.H. Glimcher, and E. Fuchs. 2008. NFATc1 balances quiescence and proliferation of skin stem cells. Cell. 132:299-310. doi:10.1016/j.cell.2007.11.047.
13. Ishitani, T., J. Ninomiya-Tsuji, S. Nagai, M. Nishita, M. Meneghini, N. Barker, M. Waterman, B. Bowerman, H. Clevers, H. Shibuya, and K. Matsumoto. 1999. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature. 399:798-802. doi:10.1038/21674.
14. Kaufman, C.K., P. Zhou, H.A. Pasolli, M. Rendl, D. Bolotin, K.C. Lim, X. Dai, M.L. Alegre, and E. Fuchs. 2003. GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 17:2108-2122. doi:10.1101/gad.1115203.
15. Korinek, V., N. Barker, P.J. Morin, D. van Wichen, R. de Weger, K.W. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 275:1784-1787. doi:10.1126/science.275.5307.1784.
16. Kramps, T., O. Peter, E. Brunner, D. Nellen, B. Froesch, S. Chatterjee, M. Murone, S. Züllig, and K. Basler. 2002. Wnt/wingless signaling requires BCL9/ legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell. 109:47-60. doi:10.1016/S0092-8674(02)00679-7.
17. Legué, E., and J.F. Nicolas. 2005. Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors. Development. 132:4143-4154. doi:10.1242/dev.01975.
18. Legué, E., I. Sequeira, and J.F. Nicolas. 2010. Hair follicle renewal: authentic morphogenesis that depends on a complex progression of stem cell lineages. Development. 137:569-577. doi:10.1242/dev.044123.
19. Lepper, C., S.J. Conway, and C.M. Fan. 2009. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 460:627-631. doi:10.1038/nature08209.
20. Levy, V., C. Lindon, B.D. Harfe, and B.A. Morgan. 2005. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev. Cell. 9:855-861. doi:10.1016/j.devcel.2005.11.003.
21. Lowry, W.E., C. Blanpain, J.A. Nowak, G. Guasch, L. Lewis, and E. Fuchs. 2005. Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev. 19:1596-1611. doi:10.1101/gad.1324905.
22. Maretto, S., M. Cordenonsi, S. Dupont, P. Braghetta, V. Broccoli, A.B. Hassan, D. Volpin, G.M. Bressan, and S. Piccolo. 2003. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA. 100:3299-3304. doi:10.1073/pnas.0434590100.
23. Merrill, B.J., U. Gat, R. DasGupta, and E. Fuchs. 2001. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 15:1688-1705. doi:10.1101/gad.891401.
24. Messina, G., and G. Cossu. 2009. The origin of embryonic and fetal myoblasts: a role of Pax3 and Pax7. Genes Dev. 23:902-905. doi:10.1101/gad.1797009.
25. Nakamura, M., J.P. Sundberg, and R. Paus. 2001. Mutant laboratory mice with abnormalities in hair follicle morphogenesis, cycling, and/or structure: annotated tables. Exp. Dermatol. 10:369-390. doi:10.1034/j.1600-0625.2001.100601.x.
26. North, T., T.L. Gu, T. Stacy, Q. Wang, L. Howard, M. Binder, M. Marín-Padilla, and N.A. Speck. 1999. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development. 126:2563-2575.
27. North, T.E., M.F. de Bruijn, T. Stacy, L. Talebian, E. Lind, C. Robin, M. Binder, E. Dzierzak, and N.A. Speck. 2002. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity. 16:661-672. doi:10.1016/S1074-7613(02)00296-0.
28. Nowak, J.A., L. Polak, H.A. Pasolli, and E. Fuchs. 2008. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell. 3:33-43. doi:10.1016/j.stem.2008.05.009.
29. Osorio, K.M., S.E. Lee, D.J. McDermitt, S.K. Waghmare, Y.V. Zhang, H.N. Woo, and T. Tumbar. 2008. Runx1 modulates developmental, but not injurydriven, hair follicle stem cell activation. Development. 135:1059-1068. doi:10.1242/dev.012799.
30. Paus, R., S. Müller-Röver, C. Van Der Veen, M. Maurer, S. Eichmüller, G. Ling, U. Hofmann, K. Foitzik, L. Mecklenburg, and B. Handjiski. 1999. A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J. Invest. Dermatol. 113:523-532. doi:10.1046/j.1523-1747.1999.00740.x.
31. Plikus, M.V., J.A. Mayer, D. de la Cruz, R.E. Baker, P.K. Maini, R. Maxson, and C.M. Chuong. 2008. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature. 451:340-344. doi:10.1038/nature06457.
32. Raveh, E., S. Cohen, D. Levanon, V. Negreanu, Y. Groner, and U. Gat. 2006. Dynamic expression of Runx1 in skin affects hair structure. Mech. Dev. 123:842-850. doi:10.1016/j.mod.2006.08.002.
33. Sakakura, C., Y. Yamaguchi-Iwai, M. Satake, S.C. Bae, A. Takahashi, E. Ogawa, A. Hagiwara, T. Takahashi, A. Murakami, K. Makino, et al. 1994. Growth inhibition and induction of differentiation of t(8;21) acute myeloid leukemia cells by the DNA-binding domain of PEBP2 and the AML1/ MTG8(ETO)-specific antisense oligonucleotide. Proc. Natl. Acad. Sci. USA. 91:11723-11727. doi:10.1073/pnas.91.24.11723.
34. Samokhvalov, I.M., N.I. Samokhvalova, and S. Nishikawa. 2007. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature. 446:1056-1061. doi:10.1038/nature05725.
35. Sano, S., S. Itami, K. Takeda, M. Tarutani, Y. Yamaguchi, H. Miura, K. Yoshikawa, S. Akira, and J. Takeda. 1999. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J. 18:4657-4668. doi:10.1093/emboj/18.17.4657.
36. Schmidt-Ullrich, R., and R. Paus. 2005. Molecular principles of hair follicle induction and morphogenesis. Bioessays. 27:247-261. doi:10.1002/bies.20184.
37. Schneider, M.R., R. Schmidt-Ullrich, and R. Paus. 2009. The hair follicle as a dynamic miniorgan. Curr. Biol. 19:R132-R142. doi:10.1016/j.cub.2008.12.005.
38. Slack, J.M. 2008. Origin of stem cells in organogenesis. Science. 322:1498-1501. doi:10.1126/science.1162782.
39. Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70-71. doi:10.1038/5007.
40. Tumbar, T. 2006. Epithelial skin stem cells. Methods Enzymol. 419:73-99. doi:10.1016/S0076-6879(06)19004-7.
41. Tumbar, T., G. Guasch, V. Greco, C. Blanpain, W.E. Lowry, M. Rendl, and E. Fuchs. 2004. Defining the epithelial stem cell niche in skin. Science. 303:359-363. doi:10.1126/science.1092436.
42. Vasioukhin, V., L. Degenstein, B. Wise, and E. Fuchs. 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. doi:10.1073/pnas.96.15.8551.
43. Vidal, V.P., M.C. Chaboissier, S. Lützkendorf, G. Cotsarelis, P. Mill, C.C. Hui, N. Ortonne, J.P. Ortonne, and A. Schedl. 2005. Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr. Biol. 15:1340-1351. doi:10.1016/j.cub.2005.06.064.
44. Watt, F.M., and B.L. Hogan. 2000. Out of Eden: stem cells and their niches. Science. 287:1427-1430. doi:10.1126/science.287.5457.1427.
45. Waghmare, S.K., R. Bansal, J. Lee, Y.V. Zhang, D.J. McDermitt, and T. Tumbar. 2008. Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J. 27:1309-1320. doi:10.1038/emboj.2008.72.
46. Zervas, M., S. Millet, S. Ahn, and A.L. Joyner. 2004. Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron. 43:345-357. doi:10.1016/j.neuron.2004.07.010.
47. Zhang, Y.V., J. Cheong, N. Ciapurin, D.J. McDermitt, and T. Tumbar. 2009. Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell. 5:267-278. doi:10.1016/j.stem.2009.06.004.
48. Zhou, P., C. Byrne, J. Jacobs, and E. Fuchs. 1995. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev. 9:700-713. doi:10.1101/gad.9.6.700.