Jarid2 regulates mouse epidermal stem cell activation and differentiation

EMBO Journal

Volumn 30, Issue 17, 2011, Pages 3635-3646

  Mejetta, Stefania ^a   Morey, Lluis ^a   Pascual, Gloria ^a   Kuebler, Bernd ^a   Mysliwiec, Matthew R ^b   Lee, Youngsook ^b   Shiekhattar, Ramin ^c   Di Croce, Luciano ^a,d   Benitah, Salvador Aznar ^a,d  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c WISTAR INSTITUTE   (United States)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

epidermal homeostasis; epidermal stem cells; Jarid2; polycomb group proteins; polycomb repressive complex 2

Indexed keywords

BETA ACTIN; CELL PROTEIN; FILAGGRIN; JARID2 PROTEIN; LORICRIN; PROTEIN P16; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPIDERMIS; EPIDERMIS CELL; GENE DELETION; HAIR FOLLICLE; KERATINOCYTE; METHYLATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN FUNCTION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EPIDERMIS; HAIR FOLLICLE; HISTONES; HUMANS; KERATINOCYTES; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; STEM CELLS;

EID: 80052261506     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.265     Document Type: Article

References (50)

1. Barradas M Anderton E Acosta JC Li S Banito A Rodriguez-Niedenführ M Maertens G Banck M Zhou MM Walsh MJ Peters G Gil J (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 23: 1177-1182
2. Blanpain C Lowry WE Geoghegan A Polak L Fuchs E (2004) Self-renewal multipotency and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648 (Pubitemid 39179715)
3. Braun KM Niemann C Jensen UB Sundberg JP Silva-Vargas V Watt FM (2003) Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130: 5241-5255 (Pubitemid 37369682)
4. Cao R Wang L Wang H Xia L Erdjument-Bromage H Tempst P Jones RS Zhang Y (2002) Role of histone H3 lysine 27 methyl-ation in Polycomb-group silencing. Science 298: 1039-1043 (Pubitemid 35247314)
5. Cao R Zhang Y (2004) SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol Cell 15: 57-67 (Pubitemid 38850219)
6. Chen H Gu X Su IH Bottino R Contreras JL Tarakhovsky A Kim SK (2009) Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 23: 975-985
7. Clayton E Doupé DP Klein AM Winton DJ Simons BD Jones PH (2007) A single type of progenitor cell maintains normal epidermis. Nature 446: 185-189 (Pubitemid 46398664)
8. Czermin B Melfi R McCabe D Seitz V Imhof A Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196 (Pubitemid 35292439)
9. De Napoles M Mermoud JE Wakao R Tang YA Endoh M Appanah R Nesterova TB Silva J Otte AP Vidal M Koseki H Brockdorff N (2004) Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 7: 663-676 (Pubitemid 39462687)
10. Ezhkova E Lien WH Stokes N Pasolli HA Silva JM Fuchs E (2011) EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes Dev 25: 485-498
11. Ezhkova E Pasolli HA Parker JS Stokes N Su IH Hannon G Tarakhovsky A Fuchs E (2009) Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 136: 1122-1135
12. Gandarillas A Watt FM (1997) c-Myc promotes differentiation of human epidermal stem cells. Genes Dev 11 : 2869-2882 (Pubitemid 27481687)
13. Greco V Chen T Rendl M Schober M Pasolli HA Stokes N Dela Cruz-Racelis J Fuchs E (2009) A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4: 155-169
14. Herz HM Shilatifard A (2010) The JARID2-PRC2 duality. Genes Dev 24: 857-861
15. Hsu YC Pasolli HA Fuchs E (2011) Dynamics between stem cells niche and progeny in the hair follicle. Cell 144: 92-105
16. Ito M Kizawa K Hamada K Cotsarelis G (2004) 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 (Pubitemid 41702109)
17. Jensen KB Driskell RR Watt FM (2010) Assaying proliferation and differentiation capacity of stem cells using disaggregated adult mouse epidermis. Nat Protocol 5: 898-911
18. Jung J Kim TG Lyons GE Kim HR Lee Y (2005a) Jumonji regulates cardiomyocyte proliferation via interaction with retinoblastoma protein. J Biol Chem 280: 30916-30923 (Pubitemid 41291823)
19. Jung J Mysliwiec MR Lee Y (2005b) Roles of JUMONJI in mouse embryonic development. Dev Dyn 232: 21-32 (Pubitemid 40070855)
20. Kirmizis A Bartley SM Kuzmichev A Margueron R Reinberg D Green R Farnham PJ (2004) Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 18: 1592-1605 (Pubitemid 38868910)
21. Kouzarides T (2007) Chromatin modifications and their function. Cell 128: 693-705 (Pubitemid 46273577)
22. Kuzmichev A Nishioka K Erdjument-Bromage H Tempst P Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of Zeste protein. Genes Dev 16: 2893-2905 (Pubitemid 35334738)
23. Landeira D Fisher AG (2011) Inactive yet indispensable: the tale of Jarid2. Trends Cell Biol 21: 74-80
24. Landeira D Sauer S Poot R Dvorkina M Mazzarella L Jorgensen HF Pereira CF Leleu M Piccolo FM Spivakov M Brookes E Pombo A Fisher C Skarnes WC Snoek T Bezstarosti K Demmers J Klose RJ Casanova M Tavares L et al (2010) Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA Polymerase II to developmental regulators. Nat Cell Biol 12: 618-624
25. Lee Y Song AJ Baker R Micales B Conway SJ Lyons GE (2000) Jumonji a nuclear protein that is necessary for normal heart development. Circ Res 86: 932-938 (Pubitemid 30324304)
26. Levine SS Weiss A Erdjument-Bromage H Shao Z Tempst P Kingstone RE (2002) The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol Cell Biol 22: 6070-6078 (Pubitemid 34857827)
27. Levy V Lindon C Harfe BD Morgan BA (2005) Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell 9: 855-861 (Pubitemid 41724112)
28. Li G Margueron R Ku M Chambon P Bernstein BE Reinberg D (2010) Jarid2 and PRC2 partners in regulating gene expression. Genes Dev 24: 368-380
29. Litchi U Anders J Yuspa SH (2008) Isolation and short-term culture of primary keratinocytes hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc 3: 799-810 (Pubitemid 351639024)
30. Majewski IJ Ritchie ME Phipson B Corbin J Pakusch M Ebert A Busslinger M Koseki H Hu Y Smyth GK Alexander WS Hilton DJ Blewitt ME (2010) Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells. Blood 1 1 6 : 731-739
31. Margueron R Li G Sarma K Blais A Zavadi J Woodcock CL Dynlacht BD Reinberg D (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 32: 503-518
32. Morris RJ Liu Y Marles L Yang Z Trempus C Li S Lin JS Sawicki JA Cotsarelis G (2004) Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22: 411-417 (Pubitemid 38451371)
33. Mysliwiec MR Chen J Powers PA Bartley CR Schneider MD Lee Y (2006) Generation of a conditional null allele of jumonji. Genesis 44: 407-411 (Pubitemid 44454045)
34. Nowak JA Fuchs E (2009) Isolation and culture of epithelial stem cells. Methods Mol Biol 482: 215-232
35. Nowak JA Polak L Pasolli HA Fuchs E (2008) Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3: 33-43
36. Pasini D Cloos PA Walfridsson J Olsson L Bukowski JP Johansen JV Bak M Tommerup N Rappsilber J Helin K (2010) JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464: 306-310
37. Peng JC Valouev A Swigut T Zhang J Zhao Y Sidow A Wysocka J (2009) Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139: 1290-1302
38. Pereira JD Sansom SN Smith J Dobenecker MW Tarakhovsky A Livesey FJ (2010) Ezh2 the histone methyltransferase of PRC2 regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci USA 107: 15957-15962
39. Sasai N Kato Y Kimura G Takeuchi T Yamaguchi M (2007) The Drosophila jumonji gene encodes a JmjC-containing nuclear protein that is required for metamorphosis. FEBS J 274: 6139-6151 (Pubitemid 350139203)
40. Sauvageau M Sauvageau G (2010) Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 7: 299-313
41. Schneider MR Schmidt-Ullrich R Paus R (2009) The hair follicle as a dynamic miniorgan. Curr Biol 19: R132-R142
42. Shen X Kim W Fujiwara Y Simon MD Liu Y Mysliwiec MR Yuan GC Lee Y Orkin SH (2009) Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139: 1303-1314
43. Su IH Basavaraj A Krutchinsky AN Hobert O Ullrich A Chait BT Tarakhovsky A (2003) Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol 4: 124-131 (Pubitemid 36193013)
44. Surface LE Thornton SR Boyer LA (2010) Polycomb group proteins set the stage for early lineage commitment. Cell Stem Cell 7: 288-298
45. Takeuchi T Watanabe Y Takano-Shimizu T Kondo S (2006) Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn 235: 2449-2459 (Pubitemid 44325259)
46. Takeuchi T Yamazaki Y Katoh-Fukui Y Tsuchiya R Kondo S Motoyama J Higashinakagawa T (1995) Gene trap capture of a novel mouse gene jumonji required for neural tube formation. Genes Dev 9: 1211-1222
47. Tiede S Kloepper JE Bodò E Tiwari S Kruse C Paus R (2007) Hair follicle stem cells: walking the maze. Eur J Cell Biol 86: 355-376 (Pubitemid 46971920)
48. Toyoda M Shirato H Nakajima K Kojima M Takahashi M Kubota M Suzuki-Migishima R Motegi Y Yokoyama M Takeuchi T (2003) Jumonji downregulates cardiac cell proliferation by repressing cyclin D1 expression. Dev Cell 5: 85-97 (Pubitemid 36827344)
49. Tumbar T Guasch G Greco V Blanpain C Lowry WE Rendl M Fuchs E (2004) Defining the epithelial stem cell niche in skin. Science 303: 359-363 (Pubitemid 38095773)
50. Wang H Wang L Erdjument-Bromage H Vidal M Tempst P Jones RS Zhang Y (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431: 873-878 (Pubitemid 39434086)