Chromatin-Remodelling Complex NURF Is Essential for Differentiation of Adult Melanocyte Stem Cells

PLoS Genetics

Volumn 11, Issue 10, 2015, Pages

  Koludrovic, Dana ^a,b   Laurette, Patrick ^a   Strub, Thomas ^c   Keime, Céline ^a   Le Coz, Madeleine ^d   Coassolo, Sebastien ^a   Mengus, Gabrielle ^a   Larue, Lionel ^d,e   Davidson, Irwin ^a,e  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d Centre National de la Recherche Scientifique   (France)

^e Equipes labélisées Ligue Contre le Cancer ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOSOME REMODELLING FACTOR PROTEIN; REGULATOR PROTEIN; RNA; UNCLASSIFIED DRUG; CELL NUCLEUS ANTIGEN; FETAL ALZHEIMER ANTIGEN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITF PROTEIN, MOUSE; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HAIR GROWTH; IN VITRO STUDY; IN VIVO STUDY; MELANOCYTE; MELANOCYTE STEM CELL; MOUSE; NONHUMAN; RNA SEQUENCE; STEM CELL; ANIMAL; CELL CYCLE; CELL DIVISION; GENE EXPRESSION REGULATION; GENETICS; HAIR FOLLICLE; MELANOMA; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY;

ANIMALS; ANTIGENS, NUCLEAR; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR FOLLICLE; MELANOCYTES; MELANOMA; MESENCHYMAL STROMAL CELLS; MICE; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; NERVE TISSUE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84946592900     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005555     Document Type: Article

References (68)

1. Goding CR, (2000) Mitf from neural crest to melanoma: signal transduction and transcription in the melanocyte lineage. Genes Dev 14: 1712–1728. 10898786
2. Widlund HR, Fisher DE, (2003) Microphthalamia-associated transcription factor: a critical regulator of pigment cell development and survival. Oncogene 22: 3035–3041. 12789278
3. Steingrimsson E, Copeland NG, Jenkins NA, (2004) Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 38: 365–411. 15568981
4. Hoek KS, (2011) MITF: the power and the glory. Pigment cell & melanoma research 24: 262–263.
5. Osawa M, Egawa G, Mak SS, Moriyama M, Freter R, et al. (2005) Molecular characterization of melanocyte stem cells in their niche. Development 132: 5589–5599. 16314490
6. Nishimura EK, (2011) Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell Melanoma Res 24: 401–410. doi: 10.1111/j.1755-148X.2011.00855.x 21466661
7. Lin JY, Fisher DE, (2007) Melanocyte biology and skin pigmentation. Nature 445: 843–850. 17314970
8. White RM, Zon LI, (2008) Melanocytes in development, regeneration, and cancer. Cell Stem Cell 3: 242–252. doi: 10.1016/j.stem.2008.08.005 18786412
9. Robinson KC, Fisher DE, (2009) Specification and loss of melanocyte stem cells. Semin Cell Dev Biol 20: 111–116. doi: 10.1016/j.semcdb.2008.11.016 19124082
10. Hoek KS, Goding CR, (2010) Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res 23: 746–759. doi: 10.1111/j.1755-148X.2010.00757.x 20726948
11. Giuliano S, Ohanna M, Ballotti R, Bertolotto C, (2011) Advances in melanoma senescence and potential clinical application. Pigment Cell Melanoma Res 24: 295–308. doi: 10.1111/j.1755-148X.2010.00820.x 21143770
12. Strub T, Giuliano S, Ye T, Bonet C, Keime C, et al. (2011) Essential role of microphthalmia transcription factor for DNA replication, mitosis and genomic stability in melanoma. Oncogene 30: 2319–2332. doi: 10.1038/onc.2010.612 21258399
13. Goding C, Meyskens FL, Jr. (2006) Microphthalmic-associated transcription factor integrates melanocyte biology and melanoma progression. Clin Cancer Res 12: 1069–1073. 16489058
14. Carreira S, Goodall J, Denat L, Rodriguez M, Nuciforo P, et al. (2006) Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes & development 20: 3426–3439.
15. Carreira S, Goodall J, Aksan I, La Rocca SA, Galibert MD, et al. (2005) Mitf cooperates with Rb1 and activates p21Cip1 expression to regulate cell cycle progression. Nature 433: 764–769. 15716956
16. Saez-Ayala M, Montenegro MF, Sanchez-Del-Campo L, Fernandez-Perez MP, Chazarra S, et al. (2013) Directed phenotype switching as an effective antimelanoma strategy. Cancer Cell 24: 105–119. doi: 10.1016/j.ccr.2013.05.009 23792190
17. Laurette P, Strub T, Koludrovic D, Keime C, Le Gras S, et al. (2015) Transcription factor MITF and remodeller BRG1 define chromatin organisation at regulatory elements in melanoma cells. eLife doi: 10.7554/eLife.06857
18. Tsukiyama T, Daniel C, Tamkun J, Wu C, (1995) ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83: 1021–1026. 8521502
19. Tsukiyama T, Wu C, (1995) Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83: 1011–1020. 8521501
20. Alkhatib SG, Landry JW, (2011) The nucleosome remodeling factor. FEBS Lett 585: 3197–3207. doi: 10.1016/j.febslet.2011.09.003 21920360
21. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, et al. (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86–90. 16728976
22. Mizuguchi G, Wu C, (1999) Nucleosome remodeling factor NURF and in vitro transcription of chromatin. Methods Mol Biol 119: 333–342. 10804523
23. Mizuguchi G, Tsukiyama T, Wisniewski J, Wu C, (1997) Role of nucleosome remodeling factor NURF in transcriptional activation of chromatin. Molecular Cell 1: 141–150. 9659911
24. Xiao H, Sandaltzopoulos R, Wang HM, Hamiche A, Ranallo R, et al. (2001) Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol Cell 8: 531–543. 11583616
25. Hamiche A, Kang JG, Dennis C, Xiao H, Wu C, (2001) Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proceedings of the National Academy of Sciences of the United States of America 98: 14316–14321. 11724935
26. Kang JG, Hamiche A, Wu C, (2002) GAL4 directs nucleosome sliding induced by NURF. Embo J 21: 1406–1413. 11889046
27. Barak O, Lazzaro MA, Lane WS, Speicher DW, Picketts DJ, et al. (2003) Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J 22: 6089–6100. 14609955
28. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, et al. (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142: 967–980. doi: 10.1016/j.cell.2010.08.020 20850016
29. Ruthenburg AJ, Li H, Milne TA, Dewell S, McGinty RK, et al. (2011) Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 145: 692–706. doi: 10.1016/j.cell.2011.03.053 21596426
30. Li H, Ilin S, Wang W, Duncan EM, Wysocka J, et al. (2006) Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442: 91–95. 16728978
31. Badenhorst P, Voas M, Rebay I, Wu C, (2002) Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev 16: 3186–3198. 12502740
32. Goller T, Vauti F, Ramasamy S, Arnold HH, (2008) Transcriptional regulator BPTF/FAC1 is essential for trophoblast differentiation during early mouse development. Mol Cell Biol 28: 6819–6827. doi: 10.1128/MCB.01058-08 18794365
33. Landry J, Sharov AA, Piao Y, Sharova LV, Xiao H, et al. (2008) Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet 4: e1000241. doi: 10.1371/journal.pgen.1000241 18974875
34. Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, et al. (2011) Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev 25: 275–286. doi: 10.1101/gad.2007311 21289071
35. Mulder KW, Wang X, Escriu C, Ito Y, Schwarz RF, et al. (2012) Diverse epigenetic strategies interact to control epidermal differentiation. Nat Cell Biol 14: 753–763. doi: 10.1038/ncb2520 22729083
36. Rambow F, Job B, Petit V, Gesbert F, Delmas V, et al. (2015) New functional signatures for understanding melanoma biology from tumor cell lineage-specific analysis. Cell Reports under revision.
37. Giuliano S, Cheli Y, Ohanna M, Bonet C, Beuret L, et al. (2010) Microphthalmia-associated transcription factor controls the DNA damage response and a lineage-specific senescence program in melanomas. Cancer Research 70: 3813–3822. doi: 10.1158/0008-5472.CAN-09-2913 20388797
38. Ohanna M, Giuliano S, Bonet C, Imbert V, Hofman V, et al. (2011) Senescent cells develop a PARP-1 and nuclear factor-{kappa}B-associated secretome (PNAS). Genes & development 25: 1245–1261.
39. Vogler M, (2012) BCL2A1: the underdog in the BCL2 family. Cell Death Differ 19: 67–74. doi: 10.1038/cdd.2011.158 22075983
40. Okuwaki M, (2008) The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J Biochem 143: 441–448. 18024471
41. Haq R, Shoag J, Andreu-Perez P, Yokoyama S, Edelman H, et al. (2013) Oncogenic BRAF regulates oxidative metabolism via PGC1alpha and MITF. Cancer Cell 23: 302–315. doi: 10.1016/j.ccr.2013.02.003 23477830
42. Vazquez F, Lim JH, Chim H, Bhalla K, Girnun G, et al. (2013) PGC1alpha expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 23: 287–301. doi: 10.1016/j.ccr.2012.11.020 23416000
43. Colombo S, Champeval D, Rambow F, Larue L, (2012) Transcriptomic analysis of mouse embryonic skin cells reveals previously unreported genes expressed in melanoblasts. J Invest Dermatol 132: 170–178. doi: 10.1038/jid.2011.252 21850021
44. Laurette P, Strub T, Koludrovic D, Keime C, Le Gras S, et al. (2015) Transcription factor MITF and remodeller BRG1 define chromatin organisation at regulatory elements in melanoma cells. Elife Mar 24;4.
45. Delmas V, Martinozzi S, Bourgeois Y, Holzenberger M, Larue L, (2003) Cre-mediated recombination in the skin melanocyte lineage. Genesis 36: 73–80. 12820167
46. Jordan SA, Jackson IJ, (2000) MGF (KIT ligand) is a chemokinetic factor for melanoblast migration into hair follicles. Dev Biol 225: 424–436. 10985860
47. Harris ML, Buac K, Shakhova O, Hakami RM, Wegner M, et al. (2013) A dual role for SOX10 in the maintenance of the postnatal melanocyte lineage and the differentiation of melanocyte stem cell progenitors. PLoS Genet 9: e1003644. doi: 10.1371/journal.pgen.1003644 23935512
48. Nishikawa SI, Osawa M, (2005) Melanocyte system for studying stem cell niche. Ernst Schering Res Found Workshop: 1–13.
49. Schouwey K, Larue L, Radtke F, Delmas V, Beermann F, (2009) Transgenic expression of Notch in melanocytes demonstrates RBP-Jkappa-dependent signaling. Pigment Cell Melanoma Res. 1:134–136.
50. Schouwey K, Delmas V, Larue L, Zimber-Strobl U, Strobl LJ, et al. (2007) Notch1 and Notch2 receptors influence progressive hair graying in a dose-dependent manner. Dev Dyn 236: 282–289. 17080428
51. McGill GG, Horstmann M, Widlund HR, Du J, Motyckova G, et al. (2002) Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109: 707–718. 12086670
52. Freter R, Osawa M, Nishikawa S, (2010) Adult stem cells exhibit global suppression of RNA polymerase II serine-2 phosphorylation. Stem Cells 28: 1571–1580. doi: 10.1002/stem.476 20641035
53. Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, et al. (2011) Chromatin remodeling complex NURF regulates thymocyte maturation. Genes & development 25: 275–286.
54. Caramel J, Papadogeorgakis E, Hill L, Browne GJ, Richard G, et al. (2013) A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell 24: 466–480. doi: 10.1016/j.ccr.2013.08.018 24075834
55. Denecker G, Vandamme N, Akay O, Koludrovic D, Taminau J, et al. (2014) Identification of a ZEB2-MITF-ZEB1 transcriptional network that controls melanogenesis and melanoma progression. Cell Death Differ. 8:1250–1261
56. Dar AA, Nosrati M, Bezrookove V, de Semir D, Majid S, et al. (2015) The Role of BPTF in Melanoma Progression and in Response to BRAF-Targeted Therapy. J Natl Cancer Inst 107.
57. Li A, Ma Y, Yu X, Mort RL, Lindsay CR, et al. (2011) Rac1 drives melanoblast organization during mouse development by orchestrating pseudopod- driven motility and cell-cycle progression. Dev Cell 21: 722–734. doi: 10.1016/j.devcel.2011.07.008 21924960
58. Lindsay CR, Lawn S, Campbell AD, Faller WJ, Rambow F, et al. (2011) P-Rex1 is required for efficient melanoblast migration and melanoma metastasis. Nat Commun 2: 555. doi: 10.1038/ncomms1560 22109529
59. Rabbani P, Takeo M, Chou W, Myung P, Bosenberg M, et al. (2011) Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 145: 941–955. doi: 10.1016/j.cell.2011.05.004 21663796
60. Song H, Spichiger-Haeusermann C, Basler K, (2009) The ISWI-containing NURF complex regulates the output of the canonical Wingless pathway. EMBO Rep 10: 1140–1146. doi: 10.1038/embor.2009.157 19713963
61. Nishimura EK, Granter SR, Fisher DE, (2005) Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 307: 720–724. 15618488
62. Osawa M, Fisher DE, (2008) Notch and melanocytes: diverse outcomes from a single signal. J Invest Dermatol 128: 2571–2574. doi: 10.1038/jid.2008.289 18927539
63. Kumano K, Masuda S, Sata M, Saito T, Lee SY, et al. (2008) Both Notch1 and Notch2 contribute to the regulation of melanocyte homeostasis. Pigment Cell Melanoma Res 21: 70–78. doi: 10.1111/j.1755-148X.2007.00423.x 18353145
64. Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A, (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24: 1253–1265. doi: 10.1101/gad.566910 20504901
65. Eckey M, Kuphal S, Straub T, Rummele P, Kremmer E, et al. (2012) Nucleosome remodeler SNF2L suppresses cell proliferation and migration and attenuates Wnt signaling. Mol Cell Biol 32: 2359–2371. doi: 10.1128/MCB.06619-11 22508985
66. Mackenzie MA, Jordan SA, Budd PS, Jackson IJ, (1997) Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev Biol 192: 99–107. 9405100
67. Lammerts van Bueren K, Scambler PJ, (2009) FACS-GAL isolation of β-galactosidase expressing cells from mid gestation mouse embryos Protcol exchange.
68. Herquel B, Ouararhni K, Martianov I, Le Gras S, Ye T, et al. (2013) Trim24-repressed VL30 retrotransposons regulate gene expression by producing noncoding RNA. Nature structural & molecular biology 20: 339–346.