The Retinoid-Related Orphan Receptor RORα Promotes Keratinocyte Differentiation via FOXN1

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Dai, Jun ^a   Brooks, Yang ^a   Lefort, Karine ^b   Getsios, Spiro ^c   Dotto, G Paolo ^a,d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYC PROTEIN; PROTEIN P53; RETINOID RELATED ORPHAN RECEPTOR ALPHA; STRUCTURAL PROTEIN; TRANSCRIPTION FACTOR FOXN1; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; EPIDERMOID CYST; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE SILENCING; HISTOGENESIS; HUMAN; HUMAN CELL; IN VIVO STUDY; KERATINOCYTE; LOSS OF FUNCTION MUTATION; PERMEABILITY BARRIER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SKIN CARCINOMA;

CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KERATINOCYTES; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; PROTEIN ISOFORMS; SKIN NEOPLASMS;

EID: 84880852248     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070392     Document Type: Article

References (59)

1. Giguere V, Tini M, Flock G, Ong E, Evans RM, et al. (1994) Isoform-specific amino-terminal domains dictate DNA-binding properties of ROR alpha, a novel family of orphan hormone nuclear receptors. Genes Dev 8: 538-553.
2. Jetten AM, Joo JH, (2006) Retinoid-related Orphan Receptors (RORs): Roles in Cellular Differentiation and Development. Adv Dev Biol 16: 313-355.
3. Jetten AM, (2009) Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl Recept Signal 7: e003.
4. Becker-Andre M, Andre E, DeLamarter JF, (1993) Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences. Biochem Biophys Res Commun 194: 1371-1379.
5. Lau P, Fitzsimmons RL, Raichur S, Wang SC, Lechtken A, et al. (2008) The orphan nuclear receptor, RORalpha, regulates gene expression that controls lipid metabolism: staggerer (SG/SG) mice are resistant to diet-induced obesity. J Biol Chem 283: 18411-18421.
6. Fitzsimmons RL, Lau P, Muscat GE, (2012) Retinoid-related orphan receptor alpha and the regulation of lipid homeostasis. The Journal of steroid biochemistry and molecular biology 130: 159-168.
7. Crumbley C, Wang Y, Banerjee S, Burris TP, (2012) Regulation of expression of citrate synthase by the retinoic acid receptor-related orphan receptor alpha (RORalpha). PloS one 7: e33804.
8. Zhu Y, McAvoy S, Kuhn R, Smith DI, (2006) RORA, a large common fragile site gene, is involved in cellular stress response. Oncogene 25: 2901-2908.
9. Steinmayr M, Andre E, Conquet F, Rondi-Reig L, Delhaye-Bouchaud N, et al. (1998) staggerer phenotype in retinoid-related orphan receptor alpha-deficient mice. Proc Natl Acad Sci U S A 95: 3960-3965.
10. Slominski A, Fischer TW, Zmijewski MA, Wortsman J, Semak I, et al. (2005) On the role of melatonin in skin physiology and pathology. Endocrine 27: 137-148.
11. Blanpain C, Fuchs E, (2009) Epidermal homeostasis: a balancing act of stem cells in the skin. Nature reviews Molecular cell biology 10: 207-217.
12. Fuchs E, (2008) Skin stem cells: rising to the surface. J Cell Biol 180: 273-284.
13. Feingold KR, (2007) Thematic review series: skin lipids. The role of epidermal lipids in cutaneous permeability barrier homeostasis. J Lipid Res 48: 2531-2546.
14. Dotto GP, (2009) Crosstalk of Notch with p53 and p63 in cancer growth control. Nat Rev Cancer 9: 587-595.
15. Nguyen BC, Lefort K, Mandinova A, Antonini D, Devgan V, et al. (2006) Cross-regulation between Notch and p63 in keratinocyte commitment to differentiation. Genes Dev 20: 1028-1042.
16. 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.
17. Restivo G, Nguyen BC, Dziunycz P, Ristorcelli E, Ryan RJ, et al. (2011) IRF6 is a mediator of Notch pro-differentiation and tumour suppressive function in keratinocytes. The EMBO journal 30: 4571-4585.
18. Sen GL, Boxer LD, Webster DE, Bussat RT, Qu K, et al. (2012) ZNF750 is a p63 target gene that induces KLF4 to drive terminal epidermal differentiation. Developmental cell 22: 669-677.
19. Wang X, Pasolli HA, Williams T, Fuchs E, (2008) AP-2 factors act in concert with Notch to orchestrate terminal differentiation in skin epidermis. The Journal of cell biology 183: 37-48.
20. Lambertini C, Pantano S, Dotto GP, (2010) Differential control of Notch1 gene transcription by Klf4 and Sp3 transcription factors in normal versus cancer-derived keratinocytes. PLoS One 5: e10369.
21. Janes SM, Ofstad TA, Campbell DH, Watt FM, Prowse DM, (2004) Transient activation of FOXN1 in keratinocytes induces a transcriptional programme that promotes terminal differentiation: contrasting roles of FOXN1 and Akt. J Cell Sci 117: 4157-4168.
22. Brissette JL, Li J, Kamimura J, Lee D, Dotto GP, (1996) The product of the mouse nude locus, Whn, regulates the balance between epithelial cell growth and differentiation. Genes & development 10: 2212-2221.
23. Dotto GP, (1999) Signal Transduction Pathways Controlling the Switch between Keratinocyte Growth and Differentiation. Critical Reviews in Oral Biology and Medicine 10: 442-457.
24. Zheng Y, Du X, Wang W, Boucher M, Parimoo S, et al. (2005) Organogenesis from dissociated cells: generation of mature cycling hair follicles from skin-derived cells. J Invest Dermatol 124: 867-876.
25. Simpson CL, Kojima S, Getsios S, (2010) RNA interference in keratinocytes and an organotypic model of human epidermis. Methods Mol Biol 585: 127-146.
26. Hu B, Castillo E, Harewood L, Ostano P, Reymond A, et al. (2012) Multifocal epithelial tumors and field cancerization from loss of mesenchymal CSL signaling. Cell 149: 1207-1220.
27. Mandinova A, Kolev V, Neel V, Hu B, Stonely W, et al. (2009) A positive FGFR3/FOXN1 feedback loop underlies benign skin keratosis versus squamous cell carcinoma formation in humans. J Clin Invest 119: 3127-3137.
28. Adams JC, Watt FM, (1989) Fibronectin inhibits the terminal differentiation of human keratinocytes. Nature 340: 307-309.
29. Dotto GP, (2008) Notch tumor suppressor function. Oncogene 27: 5115-5123.
30. Krieg P, Rosenberger S, de Juanes S, Latzko S, Hou J, et al. (2012) Aloxe3 Knockout Mice Reveal a Function of Epidermal Lipoxygenase-3 as Hepoxilin Synthase and Its Pivotal Role in Barrier Formation. The Journal of investigative dermatology.
31. Akiyama M, (2006) Harlequin ichthyosis and other autosomal recessive congenital ichthyoses: the underlying genetic defects and pathomechanisms. J Dermatol Sci 42: 83-89.
32. Hara-Chikuma M, Verkman AS, (2008) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J Mol Med 86: 221-231.
33. Schmuth M, Haqq CM, Cairns WJ, Holder JC, Dorsam S, et al. (2004) Peroxisome proliferator-activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. The Journal of investigative dermatology 122: 971-983.
34. Wu X, Nguyen BC, Dziunycz P, Chang S, Brooks Y, et al. (2010) Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature 465: 368-372.
35. Yang XO, Pappu BP, Nurieva R, Akimzhanov A, Kang HS, et al. (2008) T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 28: 29-39.
36. Rangarajan A, Talora C, Okuyama R, Nicolas M, Mammucari C, et al. (2001) Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. Embo J 20: 3427-3436.
37. Baxter RM, Brissette JL, (2002) Role of the nude gene in epithelial terminal differentiation. J Invest Dermatol 118: 303-309.
38. Yu Z, Schneider C, Boeglin WE, Brash AR, (2007) Epidermal lipoxygenase products of the hepoxilin pathway selectively activate the nuclear receptor PPARalpha. Lipids 42: 491-497.
39. Yamanaka Y, Akiyama M, Sugiyama-Nakagiri Y, Sakai K, Goto M, et al. (2007) Expression of the keratinocyte lipid transporter ABCA12 in developing and reconstituted human epidermis. Am J Pathol 171: 43-52.
40. Scott CA, Rajpopat S, Di WL (2012) Harlequin ichthyosis: ABCA12 mutations underlie defective lipid transport, reduced protease regulation and skin-barrier dysfunction. Cell and tissue research.
41. Corsini E, Viviani B, Zancanella O, Lucchi L, Visioli F, et al. (2003) Induction of adipose differentiation related protein and neutral lipid droplet accumulation in keratinocytes by skin irritants. J Invest Dermatol 121: 337-344.
42. Hara-Chikuma M, Verkman AS, (2008) Roles of aquaporin-3 in the epidermis. J Invest Dermatol 128: 2145-2151.
43. Mecklenburg L, Tychsen B, Paus R, (2005) Learning from nudity: lessons from the nude phenotype. Exp Dermatol 14: 797-810.
44. Weiner L, Han R, Scicchitano BM, Li J, Hasegawa K, et al. (2007) Dedicated epithelial recipient cells determine pigmentation patterns. Cell 130: 932-942.
45. Cai J, Lee J, Kopan R, Ma L, (2009) Genetic interplays between Msx2 and Foxn1 are required for Notch1 expression and hair shaft differentiation. Developmental biology 326: 420-430.
46. Hanyu O, Nakae H, Miida T, Higashi Y, Fuda H, et al. (2012) Cholesterol sulfate induces expression of the skin barrier protein filaggrin in normal human epidermal keratinocytes through induction of RORalpha. Biochemical and biophysical research communications 428: 99-104.
47. Solt LA, Griffin PR, Burris TP, (2010) Ligand regulation of retinoic acid receptor-related orphan receptors: implications for development of novel therapeutics. Curr Opin Lipidol 21: 204-211.
48. Bitsch F, Aichholz R, Kallen J, Geisse S, Fournier B, et al. (2003) Identification of natural ligands of retinoic acid receptor-related orphan receptor alpha ligand-binding domain expressed in Sf9 cells-a mass spectrometry approach. Anal Biochem 323: 139-149.
49. Kallen J, Schlaeppi JM, Bitsch F, Delhon I, Fournier B, (2004) Crystal structure of the human RORalpha Ligand binding domain in complex with cholesterol sulfate at 2.2 A. J Biol Chem. 279: 14033-14038.
50. Kuroki T, Ikuta T, Kashiwagi M, Kawabe S, Ohba M, et al. (2000) Cholesterol sulfate, an activator of protein kinase C mediating squamous cell differentiation: a review. Mutat Res 462: 189-195.
51. Schmuth M, Jiang YJ, Dubrac S, Elias PM, Feingold KR, (2008) Thematic review series: skin lipids. Peroxisome proliferator-activated receptors and liver X receptors in epidermal biology. Journal of lipid research 49: 499-509.
52. Pace-Asciak CR, (2009) The hepoxilins and some analogues: a review of their biology. Br J Pharmacol 158: 972-981.
53. Brash AR, Yu Z, Boeglin WE, Schneider C, (2007) The hepoxilin connection in the epidermis. FEBS J 274: 3494-3502.
54. Kim H, Lee JM, Lee G, Bhin J, Oh SK, et al. (2011) DNA damage-induced RORalpha is crucial for p53 stabilization and increased apoptosis. Molecular cell 44: 797-810.
55. Wang Y, Solt LA, Kojetin DJ, Burris TP, (2012) Regulation of p53 stability and apoptosis by a ROR agonist. PloS one 7: e34921.
56. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, et al. (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110: 251-260.
57. Sahar S, Sassone-Corsi P, (2009) Metabolism and cancer: the circadian clock connection. Nature reviews Cancer 9: 886-896.
58. Janich P, Pascual G, Merlos-Suarez A, Batlle E, Ripperger J, et al. (2011) The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480: 209-214.
59. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B, (2001) Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 15: 2069-2082.