Novel cis-regulatory modules control expression of the hairy and enhancer of split-1 (HES1) transcription factor in myoblasts

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5687-5697

  Jeziorska, Danuta M ^a   Koentges, Georgy ^a   Vance, Keith W ^a,b  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIS-REGULATORY MODULES; EXPERIMENTAL METHODOLOGY; EXPRESSION PROFILE; GENOMIC DISTANCE; GENOMICS; MYOBLASTS; NOTCH SIGNALING; TRANSCRIPTIONAL CO-ACTIVATORS; TRANSCRIPTIONAL CONTROL;

CELL CULTURE; DNA SEQUENCES; GENES; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ARTICLE; CIS REGULATORY MODULE; CONTROLLED STUDY; DNA SEQUENCE; GENE; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; HES1 GENE; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN MOTIF; SEQUENCE ANALYSIS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MICE; MYOBLASTS; NUCLEOTIDE MOTIFS; PROMOTER REGIONS, GENETIC; RECEPTORS, NOTCH; REGULATORY SEQUENCES, NUCLEIC ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE;

EID: 84857260235     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.286484     Document Type: Article

References (61)

1. Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R., and Nakanishi, S. (1992) Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 6, 2620-2634 (Pubitemid 23052889)
2. Paroush, Z., Finley, R. L., Jr., Kidd, T., Wainwright, S. M., Ingham, P. W., Brent, R., and Ish-Horowicz, D. (1994) Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79, 805-815 (Pubitemid 24371971)
3. Grbavec, D., and Stifani, S. (1996) Molecular interaction between TLE1 and the carboxyl-terminal domain of HES-1 containing the WRPW motif. Biochem. Biophys. Res. Commun. 223, 701-705 (Pubitemid 26246137)
4. Fisher, A. L., Ohsako, S., and Caudy, M. (1996) The WRPW motif of the hairy-related basic helix-loop-helix repressor proteins acts as a 4-amino acid transcription repression and protein-protein interaction domain. Mol. Cell. Biol. 16, 2670-2677 (Pubitemid 26161270)
5. Takata, T., and Ishikawa, F. (2003) Human Sir2-related protein SIRT1 associates with the bHLH repressors HES1 and HEY2 and is involved in HES1- and HEY2-mediated transcriptional repression. Biochem. Biophys. Res. Commun. 301, 250-257 (Pubitemid 36268876)
6. Kageyama, R., Ohtsuka, T., and Tomita, K. (2000) The bHLH gene Hes1 regulates differentiation of multiple cell types. Mol. Cells 10, 1-7
7. Issack, P. S., and Ziff, E. B. (1998) Genetic elements regulating HES-1 induction in Wnt-1-transformed PC12 cells. Cell Growth Differ. 9, 827-836 (Pubitemid 28471287)
8. Jarriault, S., Brou, C., Logeat, F., Schroeter, E. H., Kopan, R., and Israel, A. (1995) Signaling downstream of activated mammalian Notch. Nature 377, 355-358
9. Ong, C. T., Cheng, H. T., Chang, L. W., Ohtsuka, T., Kageyama, R., Stormo, G. D., and Kopan, R. (2006) Target selectivity of vertebrate notch proteins. Collaboration between discrete domains and CSL-binding site architecture determines activation probability. J. Biol. Chem. 281, 5106-5119 (Pubitemid 43847776)
10. Hirata, H., Yoshiura, S., Ohtsuka, T., Bessho, Y., Harada, T., Yoshikawa, K., and Kageyama, R. (2002) Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298, 840-843 (Pubitemid 35231539)
11. Jouve, C., Palmeirim, I., Henrique, D., Beckers, J., Gossler, A., Ish-Horowicz, D., and Pourquié, O. (2000) Notch signaling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127, 1421-1429 (Pubitemid 30232593)
12. Shimojo, H., Ohtsuka, T., and Kageyama, R. (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64 (Pubitemid 351467032)
13. Baek, J. H., Hatakeyama, J., Sakamoto, S., Ohtsuka, T., and Kageyama, R. (2006) Persistent and high levels of Hes1 expression regulate boundary formation in the developing central nervous system. Development 133, 2467-2476 (Pubitemid 44130398)
14. Wall, D. S., Mears, A. J., McNeill, B., Mazerolle, C., Thurig, S., Wang, Y., Kageyama, R., and Wallace, V. A. (2009) Progenitor cell proliferation in the retina is dependent on Notch-independent Sonic hedgehog/Hes1 activity. J. Cell Biol. 184, 101-112
15. Ingram, W. J., McCue, K. I., Tran, T. H., Hallahan, A. R., and Wainwright, B. J. (2008) Sonic Hedgehog regulates Hes1 through a novel mechanism that is independent of canonical Notch pathway signaling. Oncogene 27, 1489-1500 (Pubitemid 351317457)
16. Curry, C. L., Reed, L. L., Nickoloff, B. J., Miele, L., and Foreman, K. E. (2006) Notch-independent regulation of Hes-1 expression by c-Jun N-terminal kinase signaling in human endothelial cells. Lab. Invest. 86, 842-852 (Pubitemid 44100482)
17. Sanalkumar, R., Indulekha, C. L., Divya, T. S., Divya, M. S., Anto, R. J., Vinod, B., Vidyanand, S., Jagatha, B., Venugopal, S., and James, J. (2010) ATF2 maintains a subset of neural progenitors through CBF1/Notch-independent Hes-1 expression and synergistically activates the expression of Hes-1 in Notch-dependent neural progenitors. J. Neurochem. 113, 807-818
18. Nakayama, K., Satoh, T., Igari, A., Kageyama, R., and Nishida, E. (2008) FGF induces oscillations of Hes1 expression and Ras/ERK activation. Curr. Biol. 18, R332-R334 (Pubitemid 351522463)
19. Aguilera, C., Hoya-Arias, R., Haegeman, G., Espinosa, L., and Bigas, A. (2004) Recruitment of IκBα to the hes1 promoter is associated with transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 101, 16537-16542 (Pubitemid 39557748)
20. Sang, L., Roberts, J. M., and Coller, H. A. (2010) Hijacking HES1. How tumors co-opt the anti-differentiation strategies of quiescent cells. Trends Mol. Med. 16, 17-26
21. Farnie, G., Clarke, R. B., Spence, K., Pinnock, N., Brennan, K., Anderson, N. G., and Bundred, N. J. (2007) Novel cell culture technique for primary ductal carcinoma in situ. role of Notch and epidermal growth factor receptor signaling pathways. J. Natl. Cancer Inst. 99, 616-627 (Pubitemid 47073543)
22. Konishi, J., Kawaguchi, K. S., Vo, H., Haruki, N., Gonzalez, A., Carbone, D. P., and Dang, T. P. (2007) γ-Secretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers. Cancer Res. 67, 8051-8057 (Pubitemid 47395139)
23. Fan, X., Matsui, W., Khaki, L., Stearns, D., Chun, J., Li, Y. M., and Eberhart, C. G. (2006) Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 66, 7445-7452 (Pubitemid 44289197)
24. Hopfer, O., Zwahlen, D., Fey, M. F., and Aebi, S. (2005) The Notch pathway in ovarian carcinomas and adenomas. Br. J. Cancer 93, 709-718 (Pubitemid 41486463)
25. Cuevas, I. C., Slocum, A. L., Jun, P., Costello, J. F., Bollen, A. W., Riggins, G. J., McDermott, M. W., and Lal, A. (2005) Meningioma transcript profiles reveal deregulated Notch signaling pathway. Cancer Res. 65, 5070-5075 (Pubitemid 40827315)
26. Hallahan, A. R., Pritchard, J. I., Hansen, S., Benson, M., Stoeck, J., Hatton, B. A., Russell, T. L., Ellenbogen, R. G., Bernstein, I. D., Beachy, P. A., and Olson, J. M. (2004) The SmoA1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas. Cancer Res. 64, 7794-7800 (Pubitemid 39446912)
27. Sang, L., Coller, H. A., and Roberts, J. M. (2008) Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science 321, 1095-1100
28. Vance, K. W., Carreira, S., Brosch, G., and Goding, C. R. (2005) Tbx2 is overexpressed and plays an important role in maintaining proliferation and suppression of senescence in melanomas. Cancer Res. 65, 2260-2268 (Pubitemid 40490135)
29. Hagège, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W., and Forné, T. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc. 2, 1722-1733
30. Granier, C., Gurchenkov, V., Perea-Gomez, A., Camus, A., Ott, S., Papanayotou, C., Iranzo, J., Moreau, A., Reid, J., Koentges, G., Sabéran-Djoneidi, D., and Collignon, J. (2011) Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the peri-implantation mouse embryo. Dev. Biol. 349, 350-362
31. Nam, Y., Sliz, P., Pear, W. S., Aster, J. C., and Blacklow, S. C. (2007) Cooperative assembly of higher order Notch complexes functions as a switch to induce transcription. Proc. Natl. Acad. Sci. U.S.A. 104, 2103-2108 (Pubitemid 46391359)
32. Takebayashi, K., Sasai, Y., Sakai, Y., Watanabe, T., Nakanishi, S., and Kageyama, R. (1994) Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J. Biol. Chem. 269, 5150-5156
33. Kuroda, K., Tani, S., Tamura, K., Minoguchi, S., Kurooka, H., and Honjo, T. (1999) Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J. Biol. Chem. 274, 7238-7244
34. Azakie, A., Lamont, L., Fineman, J. R., and He, Y. (2005) Divergent transcriptional enhancer factor-1 regulates the cardiac troponin T promoter. Am. J. Physiol. Cell Physiol. 289, C1522-C1534 (Pubitemid 41636357)
35. 1-adrenergic induction of the skeletal α-actin promoter during cardiac myocyte hypertrophy. Transcriptional enhancer factor-1 and protein kinase C as conserved transducers of the fetal program in cardiac growth. J. Biol. Chem. 270, 410-417
36. Swartz, E. A., Johnson, A. D., and Owens, G. K. (1998) Two MCAT elements of the SM α-actin promoter function differentially in SM vs. non-SM cells. Am. J. Physiol. 275, C608-C618
37. Zhao, B., Lei, Q. Y., and Guan, K. L. (2008) The Hippo-YAP pathway. New connections between regulation of organ size and cancer. Curr. Opin. Cell Biol. 20, 638-646
38. Camargo, F. D., Gokhale, S., Johnnidis, J. B., Fu, D., Bell, G. W., Jaenisch, R., and Brummelkamp, T. R. (2007) YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17, 2054-2060 (Pubitemid 350180465)
39. Dong, J., Feldmann, G., Huang, J., Wu, S., Zhang, N., Comerford, S. A., Gayyed, M. F., Anders, R. A., Maitra, A., and Pan, D. (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133 (Pubitemid 47410268)
40. Tomczak, K. K., Marinescu, V. D., Ramoni, M. F., Sanoudou, D., Montanaro, F., Han, M., Kunkel, L. M., Kohane, I. S., and Beggs, A. H. (2004) Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J. 18, 403-405
41. Shimizu, N., Smith, G., and Izumo, S. (1993) Both a ubiquitous factor mTEF-1 and a distinct muscle-specific factor bind to the M-CAT motif of the myosin heavy chain beta gene. Nucleic Acids Res. 21, 4103-4110 (Pubitemid 23258728)
42. Hucl, T., Brody, J. R., Gallmeier, E., Iacobuzio-Donahue, C. A., Farrance, I. K., and Kern, S. E. (2007) High cancer-specific expression of mesothelin (MSLN) is attributable to an upstream enhancer containing a transcription enhancer factor-dependent MCAT motif. Cancer Res. 67, 9055-9065 (Pubitemid 47535890)
43. Krebs, L. T., Iwai, N., Nonaka, S., Welsh, I. C., Lan, Y., Jiang, R., Saijoh, Y., O'Brien, T. P., Hamada, H., and Gridley, T. (2003) Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev. 17, 1207-1212 (Pubitemid 36583163)
44. Oswald, F., Täuber, B., Dobner, T., Bourteele, S., Kostezka, U., Adler, G., Liptay, S., and Schmid, R. M. (2001) p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol. Cell. Biol. 21, 7761-7774 (Pubitemid 32988785)
45. Strano, S., Monti, O., Pediconi, N., Baccarini, A., Fontemaggi, G., Lapi, E., Mantovani, F., Damalas, A., Citro, G., Sacchi, A., Del Sal, G., Levrero, M., and Blandino, G. (2005) The transcriptional coactivator Yes-associated protein drives p73 gene-target specificity in response to DNA damage. Mol. Cell 18, 447-459 (Pubitemid 40704759)
46. Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., Wang, W., Weng, Z., Green, R. D., Crawford, G. E., and Ren, B. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39, 311-318 (Pubitemid 46328487)
47. Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer- Frick, I., Shoukry, M., Wright, C., Chen, F., Afzal, V., Ren, B., Rubin, E. M., and Pennacchio, L. A. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858
48. Jarriault, S., Le Bail, O., Hirsinger, E., Pourquié, O., Logeat, F., Strong, C. F., Brou, C., Seidah, N. G., and Isra l A. (1998) Delta-1 activation of notch-1 signaling results in HES-1 transactivation. Mol. Cell. Biol. 18, 7423-7431 (Pubitemid 28533061)
49. Hwang, J. J., Chambon, P., and Davidson, I. (1993) Characterization of the transcription activation function and the DNA binding domain of transcriptional enhancer factor-1. EMBO J. 12, 2337-2348 (Pubitemid 23194184)
50. Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y., and DePamphilis, M. L. (2001) TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev. 15, 1229-1241 (Pubitemid 32472752)
51. Yagi, R., Chen, L. F., Shigesada, K., Murakami, Y., and Ito, Y. (1999) A WW domain-containing yes-associated protein (YAP) is a novel transcriptional co-activator. EMBO J. 18, 2551-2562 (Pubitemid 29213286)
52. Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002) Capturing chromosome conformation. Science 295, 1306-1311 (Pubitemid 34157624)
53. Tolhuis, B., Palstra, R. J., Splinter, E., Grosveld, F., and de Laat, W. (2002) Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell 10, 1453-1465 (Pubitemid 36050885)
54. Tiwari, V. K., McGarvey, K. M., Licchesi, J. D., Ohm, J. E., Herman, J. G., Schübeler, D., and Baylin, S. B. (2008) PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol. 6, 2911-2927
55. Kobayashi, T., Mizuno, H., Imayoshi, I., Furusawa, C., Shirahige, K., and Kageyama, R. (2009) The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev. 23, 1870-1875
56. Lai, E. C. (2004) Notch signaling. Control of cell communication and cell fate. Development 131, 965-973
57. Rebeiz, M., Reeves, N. L., and Posakony, J. W. (2002) SCORE. A computational approach to the identification of cis-regulatory modules and target genes in whole-genome sequence data. Site clustering over random expectation. Proc. Natl. Acad. Sci. U.S.A. 99, 9888-9893 (Pubitemid 34831142)
58. Morel, V., and Schweisguth, F. (2000) Repression by suppressor of hairless and activation by Notch are required to define a single row of single-minded expressing cells in the Drosophila embryo. Genes Dev. 14, 377-388 (Pubitemid 30106492)
59. Bailey, A. M., and Posakony, J. W. (1995) Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev. 9, 2609-2622 (Pubitemid 3001579)
60. Cave, J. W., Loh, F., Surpris, J. W., Xia, L., and Caudy, M. A. (2005) ADNA transcription code for cell-specific gene activation by notch signaling. Curr. Biol. 15, 94-104
61. Arnett, K. L., Hass, M., McArthur, D. G., Ilagan, M. X., Aster, J. C., Kopan, R., and Blacklow, S. C. (2010) Structural and mechanistic insights into cooperative assembly of dimeric Notch transcription complexes. Nat. Struct. Mol. Biol. 17, 1312-1317