The p63 gene is regulated by grainyhead-like 2 (GRHL2) through reciprocal feedback and determines the epithelial phenotype in human keratinocytes

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19999-20008

  Mehrazarin, Shebli ^a   Chen, Wei ^a   Oh, Ju Eun ^a   Liu, Zi X ^a   Kang, Kyung L ^a,c   Yi, Jin K ^a,c   Kim, Reuben H ^a,b   Shin, Ki Hyuk ^a,b   Park, No Hee ^a,b,c   Kang, Mo K ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Kyung Hee University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; MODULATION; MORPHOLOGY;

EPITHELIAL-MESENCHYMAL TRANSITION; FEEDBACK REGULATION; GENE SILENCING; HUMAN EPIDERMAL KERATINOCYTES; HUMAN KERATINOCYTES; MOLECULAR PHENOTYPES; MORPHOLOGICAL CHANGES; OVER-EXPRESSION;

GENE EXPRESSION;

GRAINYHEAD LIKE 2 PROTEIN; PROTEIN P63; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CADHERIN; CKAP4 PROTEIN, HUMAN; CYTOKERATIN 14; DNA BINDING PROTEIN; FIBRONECTIN; GRHL2 PROTEIN, HUMAN; HISTONE; ISOPROTEIN; KRT14 PROTEIN, HUMAN; MEMBRANE PROTEIN; MICRORNA; MIRN200 MICRORNA, HUMAN; PROTEIN BINDING; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEEDBACK SYSTEM; GENE FUNCTION; GENE OVEREXPRESSION; GENE SILENCING; GRHL2 GENE; HUMAN; HUMAN CELL; KERATINOCYTE; MARKER GENE; P63 GENE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REGULATOR GENE; ANTAGONISTS AND INHIBITORS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

BIOMARKERS; CADHERINS; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; FEEDBACK, PHYSIOLOGICAL; FIBRONECTINS; GENE EXPRESSION REGULATION; HISTONES; HUMANS; KERATIN-14; KERATINOCYTES; MEMBRANE PROTEINS; MICRORNAS; PHENOTYPE; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN ISOFORMS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84939172656     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.659144     Document Type: Article

References (29)

1. Oh, J. E., Kim, R. H., Shin, K. H., Park, N. H., and Kang, M. K. (2011) DeltaNp63-alpha triggers epithelial-mesenchymal transition and confers stem cell properties in normal human keratinocytes. J. Biol. Chem. 286, 38757-38767
2. Pellegrini, G., Dellambra, E., Golisano, O., Martinelli, E., Fantozzi, I., Bondanza, S., Ponzin, D., McKeon, F., and De Luca, M. (2001) p63 identifies keratinocyte stem cells. Proc. Natl. Acad. Sci. 98, 3156-3161
3. Ghioni, P., Bolognese, F., Duijf, P. H., Van Bokhoven, H., Mantovani, R., and Guerrini, L. (2002) Complex transcriptional effects of p63 isoforms: identification of novel activation and repression domains. Mol. Cell. Biol. 22, 8659-8668
4. Hay, E. D., and Zuk, A. (1995) Transformations between epithelium and mesenchyme: normal, pathological, and experimentally induced. Am. J. Kidney Dis. 26, 678-690
5. Grille, S. J., Bellacosa, A., Upson, J., Klein-Szanto, A. J., van Roy, F., Lee-Kwon, W., Donowitz, M., Tsichlis, P. N., and Larue, L. (2003) The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 63, 2172-2178
6. Moreno-Bueno, G., Peinado, H., Molina, P., Olmeda, D., Cubillo, E., Santos, V., Palacios, J., Portillo, F., and Cano, A. (2009) The morphological and molecular features of the epithelial-to-mesenchymal transition. Nat. Protoc. 4, 1591-1613
7. Docherty, N. G., O'Sullivan, O. E., Healy, D. A., Murphy, M., O'neill, A. J., Fitzpatrick, J. M., and Watson, R. W. (2006) TGF-β1-induced EMT can occur independently of its proapoptotic effects and is aided by EGF receptor activation. Am. J. Physiol. Renal Physiol. 290, F1202-F1212
8. Thiery, J. P. (2003) Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15, 740-746
9. Chen, W., Xiao Liu, Z., Oh, J. E., Shin, K. H., Kim, R. H., Jiang, M., Park, N. H., and Kang, M. K. (2012) Grainyhead-like 2 (GRHL2) inhibits keratinocyte differentiation through epigenetic mechanism. Cell Death Dis. 3, e450
10. Chen, W., Dong, Q., Shin, K. H., Kim, R. H., Oh, J. E., Park, N. H., and Kang, M. K. (2010) Grainyhead-like 2 enhances the human telomerase reverse transcriptase gene expression by inhibiting DNA methylation at the 5′-CpG island in normal human keratinocytes. J. Biol. Chem. 285, 40852-40863
11. Xiang, X., Deng, Z., Zhuang, X., Ju, S., Mu, J., Jiang, H., Zhang, L., Yan, J., Miller, D., and Zhang, H. G. (2012) Grhl2 determines the epithelial phenotype of breast cancers and promotes tumor progression. PLoS ONE 7, e50781
12. Wellner, U., Schubert, J., Burk, U. C., Schmalhofer, O., Zhu, F., Sonntag, A., Waldvogel, B., Vannier, C., Darling, D., zur Hausen, A., Brunton, V. G., Morton, J., Sansom, O., Schüler, J., Stemmler, M. P., Herzberger, C., Hopt, U., Keck, T., Brabletz, S., and Brabletz, T. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 11, 1487-1495
13. Kang, M. K., Bibb, C., Baluda, M. A., Rey, O., and Park, N. H. (2000) In vitro replication and differentiation of normal human oral keratinocytes. Exp. Cell Res. 258, 288-297
14. Kang, M. K., Guo, W., and Park, N. H. (1998) Replicative senescence of normal human oral keratinocytes is associated with the loss of telomerase activity without shortening of telomeres. Cell Growth Differ. 9, 85-95
15. Kang, M. K., and Park, N. H. (2007) Extension of cell life span using exogenous telomerase. Methods Mol. Biol. 371, 151-165
16. Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W. G., and Quaranta, V. (1997) Induction of cell migration by Matrix Metalloprotease-2 cleavage of Laminin-5. Science 277, 225-228
17. Kang, M. K., Kameta, A., Shin, K. H., Baluda, M. A., and Park, N. H. (2004) Senescence occurs with hTERT repression and limited telomere shortening in human oral keratinocytes cultured with feeder cells. J. Cell. Physiol. 199, 364-370
18. Kang, X., Chen, W., Kim, R. H., Kang, M. K., and Park, N. H. (2009) Regulation of the hTERT promoter activity by MSH2, the hnRNPs K and D, and GRHL2 in human oral squamous cell carcinoma cells. Oncogene 28, 565-574
19. Xu, J., Lamouille, S., and Derynck, R. (2009) TGF-β-induced epithelial to mesenchymal transition. Cell Res. 19, 156-172
20. Gandarillas, A., and Watt, F. M. (1997) c-Myc promotes differentiation of human epidermal stem cells. Genes Dev. 11, 2869-2882
21. Varma, S., Cao, Y., Tagne, J. B., Lakshminarayanan, M., Li, J., Friedman, T. B., Morell, R. J., Warburton, D., Kotton, D. N., and Ramirez, M. I. (2012) The transcription factors Grainyhead-like 2 and NK2-homeobox 1 form a regulatory loop that coordinates lung epithelial cell morphogenesis and differentiation. J. Biol. Chem. 287, 37282-37295
22. Cieply, B., Riley, P., 4th, Pifer, P. M., Widmeyer, J., Addison, J. B., Ivanov, A. V., Denvir, J., and Frisch, S. M. (2012) Suppression of the epithelial-mesenchymal transition by Grainyhead-like-2. Cancer Res. 72, 2440-2453
23. Korpal, M., Lee, E. S., Hu, G., and Kang, Y. (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283, 14910-14914
24. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., and Marshak, D. R. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147
25. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D. J., and Horwitz, E. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells: the International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317
26. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676
27. Barbareschi, M., Pecciarini, L., Cangi, M. G., Macrì, E., Rizzo, A., Viale, G., and Doglioni, C. (2001) p63, a p53 homologue, is a selective nuclear marker of myoepithelial cells of the human breast. Am. J. Surg. Pathol. 25, 1054-1060
28. Laurikkala, J., Mikkola, M. L., James, M., Tummers, M., Mills, A. A., and Thesleff, I. (2006) p63 regulates multiple signaling pathways required for ectodermal organogenesis and differentiation. Development 133, 1553-1563
29. Cieply, B., Farris, J., Denvir, J., Ford, H. L., and Frisch, S. M. (2013) Epithelial-mesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and Grainyhead-like-2. Cancer Res. 73, 6299-6309