Transcription factor p63 bookmarks and regulates dynamic enhancers during epidermal differentiation

EMBO Reports

Volumn 16, Issue 7, 2015, Pages 863-878

  Kouwenhoven, Evelyn N ^a,b   Oti, Martin ^b   Niehues, Hanna ^a   Van Heeringen, Simon J ^b   Schalkwijk, Joost ^a   Stunnenberg, Hendrik G ^b   Van Bokhoven, Hans ^a   Zhou, Huiqing ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

epidermal differentiation; epigenomics; gene regulation; p63

Indexed keywords

MESSENGER RNA; MICRORNA 205; PROTEIN P63; RNA POLYMERASE II; TP63 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BINDING SITE; CELL DEATH; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTACT INHIBITION; CONTROLLED STUDY; ENHANCER REGION; EPIDERMIS; EPIGENETICS; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ASSOCIATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; KERATINOCYTE; MARKER GENE; NORMAL HUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; STEADY STATE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; WESTERN BLOTTING; CELL LINEAGE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; METABOLISM;

CELL DIFFERENTIATION; CELL LINEAGE; ENHANCER ELEMENTS, GENETIC; EPIDERMIS; GENE EXPRESSION REGULATION; GENETIC LOCI; HUMANS; KERATINOCYTES; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84930967957     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201439941     Document Type: Article

References (78)

1. Rinne T, Hamel B, van Bokhoven H, Brunner HG, (2006) Pattern of p63 mutations and their phenotypes-update. Am J Med Genet A 140: 1396-1406
2. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, et al, (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398: 714-718
3. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A, (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398: 708-713
4. Ferone G, Thomason HA, Antonini D, De Rosa L, Hu B, Gemei M, Zhou H, Ambrosio R, Rice DP, Acampora D, et al, (2012) Mutant p63 causes defective expansion of ectodermal progenitor cells and impaired FGF signalling in AEC syndrome. EMBO Mol Med 4: 192-205
5. Lo Iacono N, Mantero S, Chiarelli A, Garcia E, Mills AA, Morasso MI, Costanzo A, Levi G, Guerrini L, Merlo GR, (2008) Regulation of Dlx5 and Dlx6 gene expression by p63 is involved in EEC and SHFM congenital limb defects. Development 135: 1377-1388
6. Vernersson Lindahl E, Garcia EL, Mills AA, (2013) An allelic series of Trp63 mutations defines TAp63 as a modifier of EEC syndrome. Am J Med Genet A 161A: 1961-1971
7. Medawar A, Virolle T, Rostagno P, de la Forest-Divonne S, Gambaro K, Rouleau M, Aberdam D, (2008) DeltaNp63 is essential for epidermal commitment of embryonic stem cells. PLoS ONE 3: e3441
8. Rostagno P, Wolchinsky Z, Vigano AM, Shivtiel S, Zhou H, Van Bokhoven H, Ferone G, Missero C, Mantovani R, Aberdam D, et al, (2010) Embryonic stem cells as an ectodermal cellular model of human p63-related dysplasia syndromes. Biochem Biophys Res Commun 395: 131-135
9. Blanpain C, Fuchs E, (2009) Epidermal homeostasis: a balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 10: 207-217
10. Lopez-Pajares V, Yan K, Zarnegar BJ, Jameson KL, Khavari PA, (2013) Genetic pathways in disorders of epidermal differentiation. Trends Genet 29: 31-40
11. Muller FB, Kuster W, Wodecki K, Almeida H Jr, Bruckner-Tuderman L, Krieg T, Korge BP, Arin MJ, (2006) Novel and recurrent mutations in keratin KRT5 and KRT14 genes in epidermolysis bullosa simplex: implications for disease phenotype and keratin filament assembly. Hum Mutat 27: 719-720
12. Maestrini E, Monaco AP, McGrath JA, Ishida-Yamamoto A, Camisa C, Hovnanian A, Weeks DE, Lathrop M, Uitto J, Christiano AM, (1996) A molecular defect in loricrin, the major component of the cornified cell envelope, underlies Vohwinkel's syndrome. Nat Genet 13: 70-77
13. Mulder KW, Wang X, Escriu C, Ito Y, Schwarz RF, Gillis J, Sirokmany G, Donati G, Uribe-Lewis S, Pavlidis P, et al, (2012) Diverse epigenetic strategies interact to control epidermal differentiation. Nat Cell Biol 14: 753-763
14. Truong AB, Kretz M, Ridky TW, Kimmel R, Khavari PA, (2006) p63 regulates proliferation and differentiation of developmentally mature keratinocytes. Genes Dev 20: 3185-3197
15. Koster MI, Kim S, Mills AA, DeMayo FJ, Roop DR, (2004) p63 is the molecular switch for initiation of an epithelial stratification program. Genes Dev 18: 126-131
16. Shen J, van den Bogaard EH, Kouwenhoven EN, Bykov VJ, Rinne T, Zhang Q, Tjabringa GS, Gilissen C, van Heeringen SJ, Schalkwijk J, et al, (2013) APR-246/PRIMA-1(MET) rescues epidermal differentiation in skin keratinocytes derived from EEC syndrome patients with p63 mutations. Proc Natl Acad Sci USA 110: 2157-2162
17. Della Gatta G, Bansal M, Ambesi-Impiombato A, Antonini D, Missero C, di Bernardo D, (2008) Direct targets of the TRP63 transcription factor revealed by a combination of gene expression profiling and reverse engineering. Genome Res 18: 939-948
18. Kouwenhoven EN, van Heeringen SJ, Tena JJ, Oti M, Dutilh BE, Alonso ME, de la Calle-Mustienes E, Smeenk L, Rinne T, Parsaulian L, et al, (2010) Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet 6: e1001065
19. McDade SS, Henry AE, Pivato GP, Kozarewa I, Mitsopoulos C, Fenwick K, Assiotis I, Hakas J, Zvelebil M, Orr N, et al, (2012) Genome-wide analysis of p63 binding sites identifies AP-2 factors as co-regulators of epidermal differentiation. Nucleic Acids Res 40: 7190-7206
20. Van Ruissen F, de Jongh GJ, Zeeuwen PL, Van Erp PE, Madsen P, Schalkwijk J, (1996) Induction of normal and psoriatic phenotypes in submerged keratinocyte cultures. J Cell Physiol 168: 442-452
21. Fuchs E, (2008) Skin stem cells: rising to the surface. J Cell Biol 180: 273-284
22. Kretz M, Siprashvili Z, Chu C, Webster DE, Zehnder A, Qu K, Lee CS, Flockhart RJ, Groff AF, Chow J, et al, (2013) Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature 493: 231-235
23. Parsa R, Yang A, McKeon F, Green H, (1999) Association of p63 with proliferative potential in normal and neoplastic human keratinocytes. J Invest Dermatol 113: 1099-1105
24. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA, (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3
25. Kohler S, Doelken SC, Mungall CJ, Bauer S, Firth HV, Bailleul-Forestier I, Black GC, Brown DL, Brudno M, Campbell J, et al, (2014) The Human Phenotype Ontology project: linking molecular biology and disease through phenotype data. Nucleic Acids Res 42: D966-D974
26. Aberdam D, Candi E, Knight RA, Melino G, (2008) miRNAs, 'stemness' and skin. Trends Biochem Sci 33: 583-591
27. Candi E, Amelio I, Agostini M, Melino G, (2014) MicroRNAs and p63 in epithelial stemness. Cell Death Differ 22: 12-21
28. Shenoy A, Blelloch RH, (2014) Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat Rev Mol Cell Biol 15: 565-576
29. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN, (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23: 4051-4060
30. Lena AM, Shalom-Feuerstein R, Rivetti di Val Cervo P, Aberdam D, Knight RA, Melino G, Candi E, (2008) miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ 15: 1187-1195
31. Yi R, Poy MN, Stoffel M, Fuchs E, (2008) A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452: 225-229
32. Encode Project Consortium, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M, (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74
33. Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, Zhang X, Durham T, Miri M, Deshpande V, De Jager PL, et al, (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152: 642-654
34. Karlic R, Chung HR, Lasserre J, Vlahovicek K, Vingron M, (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci USA 107: 2926-2931
35. van Heeringen SJ, (2013) Vertebrate Motif Clusters. figshare: http://dx.doi.org/10.6084/m9.figshare.819997
36. Feuerborn A, Srivastava PK, Kuffer S, Grandy WA, Sijmonsma TP, Gretz N, Brors B, Grone HJ, (2011) The Forkhead factor FoxQ1 influences epithelial differentiation. J Cell Physiol 226: 710-719
37. Wong CF, Barnes LM, Dahler AL, Smith L, Serewko-Auret MM, Popa C, Abdul-Jabbar I, Saunders NA, (2003) E2F modulates keratinocyte squamous differentiation: implications for E2F inhibition in squamous cell carcinoma. J Biol Chem 278: 28516-28522
38. Ogata A, Shimizu T, Abe R, Shimizu H, Sakai M, (2004) Expression of c-maf and mafB genes in the skin during rat embryonic development. Acta Histochem 106: 65-67
39. Bollag WB, (2007) Differentiation of human keratinocytes requires the vitamin d receptor and its coactivators. J Invest Dermatol 127: 748-750
40. Kommagani R, Leonard MK, Lewis S, Romano RA, Sinha S, Kadakia MP, (2009) Regulation of VDR by deltaNp63alpha is associated with inhibition of cell invasion. J Cell Sci 122: 2828-2835
41. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA, (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153: 307-319
42. Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-Andre V, Sigova AA, Hoke HA, Young RA, (2013) Super-enhancers in the control of cell identity and disease. Cell 155: 934-947
43. Pasquali L, Gaulton KJ, Rodriguez-Segui SA, Mularoni L, Miguel-Escalada I, Akerman I, Tena JJ, Moran I, Gomez-Marin C, van de Bunt M, et al, (2014) Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants. Nat Genet 46: 136-143
44. Shimomura Y, Wajid M, Shapiro L, Christiano AM, (2008) P-cadherin is a p63 target gene with a crucial role in the developing human limb bud and hair follicle. Development 135: 743-753
45. Ferone G, Mollo MR, Thomason HA, Antonini D, Zhou H, Ambrosio R, De Rosa L, Salvatore D, Getsios S, van Bokhoven H, et al, (2013) p63 control of desmosome gene expression and adhesion is compromised in AEC syndrome. Hum Mol Genet 22: 531-543
46. Sandilands A, Sutherland C, Irvine AD, McLean WH, (2009) Filaggrin in the frontline: role in skin barrier function and disease. J Cell Sci 122: 1285-1294
47. Masse I, Barbollat-Boutrand L, Molina M, Berthier-Vergnes O, Joly-Tonetti N, Martin MT, Caron de Fromentel C, Kanitakis J, Lamartine J, (2012) Functional interplay between p63 and p53 controls RUNX1 function in the transition from proliferation to differentiation in human keratinocytes. Cell Death Dis 3: e318
48. Kommagani R, Caserta TM, Kadakia MP, (2006) Identification of vitamin D receptor as a target of p63. Oncogene 25: 3745-3751
49. Martynova E, Pozzi S, Basile V, Dolfini D, Zambelli F, Imbriano C, Pavesi G, Mantovani R, (2012) Gain-of-function p53 mutants have widespread genomic locations partially overlapping with p63. Oncotarget 3: 132-143
50. Tran MN, Choi W, Wszolek MF, Navai N, Lee IL, Nitti G, Wen S, Flores ER, Siefker-Radtke A, Czerniak B, et al, (2013) The p63 protein isoform DeltaNp63alpha inhibits epithelial-mesenchymal transition in human bladder cancer cells: role of MIR-205. J Biol Chem 288: 3275-3288
51. Tucci P, Agostini M, Grespi F, Markert EK, Terrinoni A, Vousden KH, Muller PA, Dotsch V, Kehrloesser S, Sayan BS, et al, (2012) Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer. Proc Natl Acad Sci USA 109: 15312-15317
52. van den Bogaard EH, Bergboer JG, Vonk-Bergers M, van Vlijmen-Willems IM, Hato SV, der van Valk PG, Schroder JM, Joosten I, Zeeuwen PL, Schalkwijk J, (2013) Coal tar induces AHR-dependent skin barrier repair in atopic dermatitis. J Clin Invest 123: 917-927
53. Rizzo JM, Romano RA, Bard J, Sinha S, (2014) RNA-seq studies reveal new insights into p63 and the transcriptomic landscape of the mouse skin. J Invest Dermatol 135: 629-632
54. Romano RA, Smalley K, Magraw C, Serna VA, Kurita T, Raghavan S, Sinha S, (2012) DeltaNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development 139: 772-782
55. Chakravarti D, Su X, Cho MS, Bui NH, Coarfa C, Venkatanarayan A, Benham AL, Flores Gonzalez RE, Alana J, Xiao W, et al, (2014) Induced multipotency in adult keratinocytes through down-regulation of DeltaNp63 or DGCR8. Proc Natl Acad Sci USA 111: E572-E581
56. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297
57. Cullen BR, (2004) Transcription and processing of human microRNA precursors. Mol Cell 16: 861-865
58. Sudou N, Yamamoto S, Ogino H, Taira M, (2012) Dynamic in vivo binding of transcription factors to cis-regulatory modules of cer and gsc in the stepwise formation of the Spemann-Mangold organizer. Development 139: 1651-1661
59. Rada-Iglesias A, Bajpai R, Prescott S, Brugmann SA, Swigut T, Wysocka J, (2012) Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest. Cell Stem Cell 11: 633-648
60. Thomason HA, Zhou H, Kouwenhoven EN, Dotto GP, Restivo G, Nguyen BC, Little H, Dixon MJ, van Bokhoven H, Dixon J, (2010) Cooperation between the transcription factors p63 and IRF6 is essential to prevent cleft palate in mice. J Clin Invest 120: 1561-1569
61. Fakhouri WD, Rahimov F, Attanasio C, Kouwenhoven EN, Ferreira De Lima RL, Felix TM, Nitschke L, Huver D, Barrons J, Kousa YA, et al, (2014) An etiologic regulatory mutation in IRF6 with loss- and gain-of-function effects. Hum Mol Genet 23: 2711-2720
62. Zaret KS, Carroll JS, (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25: 2227-2241
63. Rheinwald JG, Green H, (1977) Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature 265: 421-424
64. Rinne T, Clements SE, Lamme E, Duijf PH, Bolat E, Meijer R, Scheffer H, Rosser E, Tan TY, McGrath JA, et al, (2008) A novel translation re-initiation mechanism for the p63 gene revealed by amino-terminal truncating mutations in Rapp-Hodgkin/Hay-Wells-like syndromes. Hum Mol Genet 17: 1968-1977
65. Smeenk L, van Heeringen SJ, Koeppel M, van Driel MA, Bartels SJ, Akkers RC, Denissov S, Stunnenberg HG, Lohrum M, (2008) Characterization of genome-wide p53-binding sites upon stress response. Nucleic Acids Res 36: 3639-3654
66. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408
67. Li H, Durbin R, (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595
68. Feng J, Liu T, Qin B, Zhang Y, Liu XS, (2012) Identifying ChIP-seq enrichment using MACS. Nat Protoc 7: 1728-1740
69. Wu TD, Nacu S, (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873-881
70. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, et al, (2013) Ensembl 2013. Nucleic Acids Res 41: D48-D55
71. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L, (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515
72. Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, Farrell CM, Hart J, Landrum MJ, McGarvey KM, et al, (2014) RefSeq: an update on mammalian reference sequences. Nucleic Acids Res 42: D756-D763
73. Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, et al, (2013) The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res 41: D64-D69
74. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al, (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
75. Michaud J, Simpson KM, Escher R, Buchet-Poyau K, Beissbarth T, Carmichael C, Ritchie ME, Schutz F, Cannon P, Liu M, et al, (2008) Integrative analysis of RUNX1 downstream pathways and target genes. BMC Genom 9: 363
76. Quinlan AR, Hall IM, (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842
77. van Heeringen SJ, Veenstra GJ, (2011) GimmeMotifs: a de novo motif prediction pipeline for ChIP-sequencing experiments. Bioinformatics 27: 270-271
78. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210