The Grainyhead transcription factor Grhl3/Get1 suppresses miR-21 expression and tumorigenesis in skin: Modulation of the miR-21 target MSH2 by RNA-binding protein DND1

Oncogene

Volumn 32, Issue 12, 2013, Pages 1497-1507

  Bhandari, A ^a   Gordon, W ^a,b   Dizon, D ^a   Hopkin, A S ^a   Gordon, E ^a,b   Yu, Z ^a   Andersen, B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dnd1; Grhl3; mir 21; MSH2; skin; tumorigenesis

Indexed keywords

DND1 PROTEIN; MICRORNA 21; PROTEIN MSH2; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GRHL3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PSORIASIS; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SKIN CARCINOGENESIS; SKIN CARCINOMA;

ANIMALS; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENES, RAS; HUMANS; MICE; MICRORNAS; MUTS HOMOLOG 2 PROTEIN; NEOPLASM PROTEINS; PROMOTER REGIONS, GENETIC; SKIN; SKIN NEOPLASMS; TRANSCRIPTION FACTORS;

MUS;

EID: 84884211489     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.168     Document Type: Article

References (52)

1. Koster MI, Roop DR. Mechanisms regulating epithelial stratification. Annu Rev Cell Dev Biol 2007; 23: 93-113.
2. Andl T, Murchison EP, Liu F, Zhang Y, Yunta-Gonzalez M, Tobias JW et al. The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles. Curr Biol 2006; 16: 1041-1049.
3. Yi R, Poy MN, Stoffel M, Fuchs E. A skin microRNA promotes differentiation by repressing 'stemness'. Nature 2008; 452: 225-229.
4. Yi R, Pasolli HA, Landthaler M, Hafner M, Ojo T, Sheridan R et al. DGCR8-dependent microRNA biogenesis is essential for skin development. Proc Natl Acad Sci USA 2009; 106: 498-502.
5. Lena AM, Shalom-Feuerstein R, Rivetti di Val Cervo P, Aberdam D, Knight RA, Melino G et al. miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ 2008; 15: 1187-1195.
6. Antonini D, Russo MT, De Rosa L, Gorrese M, Del Vecchio L, Missero C. Transcriptional repression of miR-34 family contributes to p63-mediated cell cycle progression in epidermal cells. J Invest Dermatol 2010; 130: 1249-1257.
7. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
8. Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelialmesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008; 283: 14910-14914.
9. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008; 22: 894-907.
10. Christoffersen NR, Silahtaroglu A, Orom UA, Kauppinen S, Lund AH. miR-200b mediates post-transcriptional repression of ZFHX1B. RNA 2007; 13: 1172-1178.
11. Ting SB, Caddy J, Hislop N, Wilanowski T, Auden A, Zhao LL et al. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 2005; 308: 411-413.
12. Yu Z, Lin KK, Bhandari A, Spencer JA, Xu X, Wang N et al. The Grainyhead-like epithelial transactivator Get-1/Grhl3 regulates epidermal terminal differentiation and interacts functionally with LMO4. Dev Biol 2006; 299: 122-136.
13. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-2261.
14. Sonkoly E, Wei T, Pavez Lorie E, Suzuki H, Kato M, Torma H et al. Protein kinase C-dependent upregulation of miR-203 induces the differentiation of human keratinocytes. J Invest Dermatol 2010; 130: 124-134.
15. Hildebrand J, Rutze M, Walz N, Gallinat S, Wenck H, Deppert W et al. A comprehensive analysis of microRNA expression during human keratinocyte differentiation in vitro and in vivo. J Invest Dermatol 2011; 131: 20-29.
16. Yi R, O'Carroll D, Pasolli HA, Zhang Z, Dietrich FS, Tarakhovsky A et al. Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat Genet 2006; 38: 356-362.
17. Ahmed MI, Mardaryev AN, Lewis CJ, Sharov AA, Botchkareva NV. MicroRNA-21 is an important downstream component of BMP signalling in epidermal keratinocytes. J Cell Sci 2011; 124: 3399-3404.
18. Joyce CE, Zhou X, Xia J, Ryan C, Thrash B, Menter A et al. Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome. Hum Mol Genet 2011; 20: 4025-4040.
19. Sonkoly E, Wei T, Janson PC, Saaf A, Lundeberg L, Tengvall-Linder M et al. MicroRNAs: novel regulators involved in the pathogenesis of psoriasis? PLoS One 2007; 2: e610.
20. Zibert JR, Lovendorf MB, Litman T, Olsen J, Kaczkowski B, Skov L. MicroRNAs and potential target interactions in psoriasis. J Dermatol Sci 2010; 58: 177-185.
21. Dziunycz P, Iotzova-Weiss G, Eloranta JJ, Lauchli S, Hafner J, French LE et al. Squamous cell carcinoma of the skin shows a distinct microRNA profile modulated by UV radiation. J Invest Dermatol 2010; 130: 2686-2689.
22. Ting SB, Caddy J, Wilanowski T, Auden A, Cunningham JM, Elias PM et al. The epidermis of grhl3-null mice displays altered lipid processing and cellular hyperproliferation. Organogenesis 2005; 2: 33-35.
23. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550.
24. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34: 267-273.
25. Sandelin A, Wasserman WW, Lenhard B. ConSite: web-based prediction of r egulatory elements using cross-species comparison. Nucleic Acids Res 2004; 32: W249-W252.
26. Fujita S, Ito T, Mizutani T, Minoguchi S, Yamamichi N, Sakurai K et al. miR-21 Gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J Mol Biol 2008; 378: 492-504.
27. Elmen J, Lindow M, Schutz S, Lawrence M, Petri A, Obad S et al. LNA-mediated microRNA silencing in non-human primates. Nature 2008; 452: 896-899.
28. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005; 438: 685-689.
29. Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, van Rooij E et al. Modulation of K-Ras-dependent lung tumorigenesis by MicroRNA-21. Cancer Cell 2010; 18: 282-293.
30. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37: 495-500.
31. Dennis Jr G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003; 4: P3.
32. Sheibani N, Rhim JS, Allen-Hoffmann BL. Malignant human papillomavirus type 16-transformed human keratinocytes exhibit altered expression of extracellular matrix glycoproteins. Cancer Res 1991; 51: 5967-5975.
33. Jiang R, Cabras G, Sheng W, Zeng Y, Ooka T. Synergism of BARF1 with Ras induces malignant transformation in primary primate epithelial cells and human nasopharyngeal epithelial cells. Neoplasia 2009; 11: 964-973.
34. Meira LB, Cheo DL, Reis AM, Claij N, Burns DK, te Riele H et al. Mice defective in the mismatch repair gene Msh2 show increased predisposition to UVB radiationinduced skin cancer. DNA Repair (Amst) 2002; 1: 929-934.
35. Reitmair AH, Redston M, Cai JC, Chuang TC, Bjerknes M, Cheng H et al. Spontaneous intestinal carcinomas and skin neoplasms in Msh2-deficient mice. Cancer Res 1996; 56: 3842-3849.
36. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 2007; 131: 1273-1286.
37. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006; 125: 1111-1124.
38. Zhu R, Iacovino M, Mahen E, Kyba M, Matin A. Transcripts that associate with the RNA binding protein, DEAD-END (DND1), in embryonic stem (ES) cells. BMC Mol Biol 2011; 12: 37.
39. Selcuklu SD, Donoghue MT, Spillane C. miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans 2009; 37: 918-925.
40. Yu Y, Wang Y, Ren X, Tsuyada A, Li A, Liu LJ et al. Context-dependent bidirectional regulation of the MutS homolog 2 by transforming growth factor beta contributes to chemoresistance in breast cancer cells. Mol Cancer Res 2010; 8: 1633-1642.
41. Darido C, Georgy SR, Wilanowski T, Dworkin S, Auden A, Zhao Q et al. Targeting of the tumor suppressor GRHL3 by a miR-21-Dependent proto-oncogenic network results in PTEN loss and tumorigenesis. Cancer Cell 2011; 20: 635-648.
42. Ma X, Kumar M, Choudhury SN, Becker Buscaglia LE, Barker JR, Kanakamedala K et al. Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis. Proc Natl Acad Sci USA 2011; 108: 10144-10149.
43. Wang Y, Lee CG. MicroRNA and cancer-focus on apoptosis. J Cell Mol Med 2009; 13: 12-23.
44. Ribas J, Lupold SE. The transcriptional regulation of miR-21, its multiple transcripts, and their implication in prostate cancer. Cell Cycle 2010; 9: 923-929.
45. Cottonham CL, Kaneko S, Xu L. miR-21 and miR-31 converge on TIAM1 to regulate migration and invasion of colon carcinoma cells. J Biol Chem 2010; 285: 35293-35302.
46. Yang X, Wang J, Guo SL, Fan KJ, Li J, Wang YL et al. miR-21 promotes keratinocyte migration and re-epithelialization during wound healing. Int J Biol Sci 2011; 7: 685-690.
47. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 2010; 39: 493-506.
48. Sano S, Itami S, Takeda K, Tarutani M, Yamaguchi Y, Miura H et al. Keratinocytespecific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J 1999; 18: 4657-4668.
49. Kira M, Sano S, Takagi S, Yoshikawa K, Takeda J, Itami S. STAT3 deficiency in keratinocytes leads to compromised cell migration through hyperphosphorylation of p130(cas). J Biol Chem 2002; 277: 12931-12936.
50. Lin KK, Kumar V, Geyfman M, Chudova D, Ihler AT, Smyth P et al. Circadian clock genes contribute to the regulation of hair follicle cycling. PLoS Genet 2009; 5: e1000573.
51. Rabinovich A, Jin VX, Rabinovich R, Xu X, Farnham PJ. E2F in vivo binding specificity: comparison of consensus versus nonconsensus binding sites. Genome Res 2008; 18: 1763-1777.
52. Roop DR, Lowy DR, Tambourin PE, Strickland J, Harper JR, Balaschak M et al. An activated Harvey ras oncogene produces benign tumours on mouse epidermal tissue. Nature 1986; 323: 822-824.