Hfp inhibits Drosophila myc transcription and cell growth in a TFIIH/Hay-dependent manner

Development

Volumn 137, Issue 17, 2010, Pages 2875-2884

  Mitchell, Naomi C ^a   Johanson, Timothy M ^a   Cranna, Nicola J ^a   Jue Er, Amanda Lee ^a   Richardson, Helena E ^a,b   Hannan, Ross D ^a,b   Quinn, Leonie M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Cell growth; Drosophila; Half pint (hfp; pUf68); Transcriptional repression

Indexed keywords

HALF PINT PROTEIN; HAYWIRE PROTEIN; MYC PROTEIN; TRANSCRIPTION FACTOR IIH; UNCLASSIFIED DRUG; DIMINUTIVE PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HALF PINT PROTEIN, DROSOPHILA; HAYWIRE PROTEIN, DROSOPHILA; HELICASE; PRIMER DNA; TRANSCRIPTION FACTOR;

5' UNTRANSLATED REGION; ARTICLE; CELL CYCLE PROGRESSION; CELL GROWTH; DROSOPHILA; GENE REPRESSION; GENETIC TRANSCRIPTION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; RNA SPLICING; ANIMAL; BIOLOGICAL MODEL; CELL CYCLE S PHASE; CELL PROLIFERATION; CYTOLOGY; DRUG ANTAGONISM; FORELIMB; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE SEQUENCE; ONCOGENE MYC; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

5' UNTRANSLATED REGIONS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL PROLIFERATION; DNA HELICASES; DNA PRIMERS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENES, INSECT; GENES, MYC; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MODELS, BIOLOGICAL; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; S PHASE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; WING;

EID: 77956211767     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.049585     Document Type: Article

References (72)

1. Barna, M., Pusic, A., Zollo, O., Costa, M., Kondrashov, N., Rego, E., Rao, P. H. and Ruggero, D. (2008). Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature 456, 971-975.
2. Becam, I. and Milan, M. (2008). A permissive role of Notch in maintaining the DV affinity boundary of the Drosophila wing. Dev. Biol. 322, 190-198.
3. Benassayag, C., Montero, L., Colombie, N., Gallant, P., Cribbs, D. and Morello, D. (2005). Human c-Myc isoforms differentially regulate cell growth and apoptosis in Drosophila melanogaster. Mol. Cell. Biol. 25, 9897-9909. (Pubitemid 41572738)
4. Benjamin, L. R., Chung, H. J., Sanford, S., Kouzine, F., Liu, J. and Levens, D. (2008). Hierarchical mechanisms build the DNA-binding specificity of FUSE binding protein. Proc. Natl. Acad. Sci. USA 105, 18296-18301.
5. Bentley, D. L. and Groudine, M. (1986). Novel promoter upstream of the human c-myc gene and regulation of c-myc expression in B-cell lymphomas. Mol. Cell. Biol. 6, 3481-3489.
6. Bouchard, C., Staller, P. and Eilers, M. (1998). Control of cell proliferation by Myc. Trends Cell Biol. 8, 202-206.
7. Chung, H. J. and Levens, D. (2005). c-myc expression: keep the noise down! Mol. Cells 20, 157-166.
8. Coin, F. and Egly, J. M. (1998). Ten years of TFIIH. Cold Spring Harbor Symp. Quant. Biol. 63, 105-110.
9. Coin, F. and Egly, J. M. (2003). Assay of promoter melting and extension of mRNA: role of TFIIH subunits. Methods Enzymol. 370, 713-733.
10. Coin, F., Frit, P., Viollet, B., Salles, B. and Egly, J. M. (1998). TATA binding protein discriminates between different lesions on DNA, resulting in a transcription decrease. Mol. Cell. Biol. 18, 3907-3914.
11. Coin, F., Auriol, J., Tapias, A., Clivio, P., Vermeulen, W. and Egly, J. M. (2004). Phosphorylation of XPB helicase regulates TFIIH nucleotide excision repair activity. EMBO J. 23, 4835-4846.
12. Coin, F., Oksenych, V. and Egly, J. M. (2007). Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol. Cell 26, 245-256.
13. Coller, H. A., Grandori, C., Tamayo, P., Colbert, T., Lander, E. S., Eisenman, R. N. and Golub, T. R. (2000). Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc. Natl. Acad. Sci. USA 97, 3260-3265.
14. Cranna, N. and Quinn, L. (2009). Impact of steroid hormone signals on Drosophila cell cycle during development. Cell Div. 4, 3.
15. Crichlow, G. V., Zhou, H., Hsiao, H. H., Frederick, K. B., Debrosse, M., Yang, Y., Folta-Stogniew, E. J., Chung, H. J., Fan, C., De la Cruz, E. M. et al. (2008). Dimerization of FIR upon FUSE DNA binding suggests a mechanism of c-myc inhibition. EMBO J. 27, 277-289.
16. de la Cova, C., Abril, M., Bellosta, P., Gallant, P. and Johnston, L. A. (2004). Drosophila myc regulates organ size by inducing cell competition. Cell 117, 107-116.
17. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
18. Duman-Scheel, M., Johnston, L. A. and Du, W. (2004). Repression of dMyc expression by Wingless promotes Rbf-induced G1 arrest in the presumptive Drosophila wing margin. Proc. Natl. Acad. Sci. USA 101, 3857-3862.
19. Duncan, R., Bazar, L., Michelotti, G., Tomonaga, T., Krutzsch, H., Avigan, M. and Levens, D. (1994). A sequence-specific, single-strand binding protein activates the far upstream element of c-myc and defines a new DNA-binding motif. Genes Dev. 8, 465-480.
20. Eilers, M. and Eisenman, R. N. (2008). Myc's broad reach. Genes Dev. 22, 2755-2766.
21. Fan, L., Arvai, A. S., Cooper, P. K., Iwai, S., Hanaoka, F. and Tainer, J. A. (2006). Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol. Cell 22, 27-37.
22. Gallant, P. (2005). Myc, cell competition, and compensatory proliferation. Cancer Res. 65, 6485-6487.
23. Gallant, P., Shiio, Y., Cheng, P. F., Parkhurst, S. M. and Eisenman, R. N. (1996). Myc and Max homologs in Drosophila. Science 274, 1523-1527.
24. Grandori, C., Cowley, S. M., James, L. P. and Eisenman, R. N. (2000). The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16, 653-699.
25. Grandori, C., Gomez-Roman, N., Felton-Edkins, Z. A., Ngouenet, C., Galloway, D. A., Eisenman, R. N. and White, R. J. (2005). c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 7, 311-318. (Pubitemid 40331133)
26. Grewal, S. S., Li, L., Orian, A., Eisenman, R. N. and Edgar, B. A. (2005). Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat. Cell Biol. 7, 295-302.
27. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
28. Herranz, H., Perez, L., Martin, F. A. and Milan, M. (2008). A Wingless and Notch double-repression mechanism regulates G1-S transition in the Drosophila wing. EMBO J. 27, 1633-1645.
29. Huh, J. R., Guo, M. and Hay, B. A. (2004). Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr. Biol. 14, 1262-1266.
30. Johnston, L. A. and Edgar, B. A. (1998). Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394, 82-84.
31. Johnston, L. A. and Gallant, P. (2002). Control of growth and organ size in Drosophila. BioEssays 24, 54-64.
32. Johnston, L. A., Prober, D. A., Edgar, B. A., Eisenman, R. N. and Gallant, P. (1999). Drosophila myc regulates cellular growth during development. Cell 98, 779-790.
33. Karlsson, C., Korayem, A. M., Scherfer, C., Loseva, O., Dushay, M. S. and Theopold, U. (2004). Proteomic analysis of the Drosophila larval hemolymph clot. J. Biol. Chem. 279, 52033-52041. (Pubitemid 39656574)
34. Kim, T. H., Barrera, L. O., Zheng, M., Qu, C., Singer, M. A., Richmond, T. A., Wu, Y., Green, R. D. and Ren, B. (2005). A high-resolution map of active promoters in the human genome. Nature 436, 876-880. (Pubitemid 41160649)
35. Levens, D. (2002). Disentangling the MYC web. Proc. Natl. Acad. Sci. USA 99, 5757-5759.
36. Levens, D. L. (2003). Reconstructing MYC. Genes Dev. 17, 1071-1077.
37. Liao, D. J. and Dickson, R. B. (2000). c-Myc in breast cancer. Endocr. Relat. Cancer 7, 143-164.
38. Liu, J. and Levens, D. (2006). Making myc. Curr. Top. Microbiol. Immunol. 302, 1-32.
39. Liu, J., He, L., Collins, I., Ge, H., Libutti, D., Li, J., Egly, J. and Levens, D. (2000). The FBP interacting repressor targets TFIIH to inhibit activated transcription. Mol. Cell 5, 331-341.
40. Liu, J., Akoulitchev, S., Weber, A., Ge, H., Chuikov, S., Libutti, D., Wang, X. W., Conaway, J. W., Harris, C. C., Conaway, R. C. et al. (2001). Defective interplay of activators and repressors with TFIH in xeroderma pigmentosum. Cell 104, 353-363.
41. Liu, J., Kouzine, F., Nie, Z., Chung, H. J., Elisha-Feil, Z., Weber, A., Zhao, K. and Levens, D. (2006). The FUSE/FBP/FIR/TFIIH system is a molecular machine programming a pulse of c-myc expression. EMBO J. 25, 2119-2130. (Pubitemid 43756228)
42. Maines, J. Z., Stevens, L. M., Tong, X. and Stein, D. (2004). Drosophila dMyc is required for ovary cell growth and endoreplication. Development 131, 775-786.
43. Marcu, K. B., Bossone, S. A. and Patel, A. J. (1992). myc function and regulation. Annu. Rev. Biochem. 61, 809-860.
44. Martin, F. A., Perez-Garijo, A. and Morata, G. (2009). Apoptosis in Drosophila: compensatory proliferation and undead cells. Int. J. Dev. Biol. 53, 1341-1347.
45. Matsushita, K., Tomonaga, T., Shimada, H., Shioya, A., Higashi, M., Matsubara, H., Harigaya, K., Nomura, F., Libutti, D., Levens, D. et al. (2006). An essential role of alternative splicing of c-myc suppressor FUSE-binding protein-interacting repressor in carcinogenesis. Cancer Res. 66, 1409-1417.
46. Merino, C., Reynaud, E., Vazquez, M. and Zurita, M. (2002). DNA repair and transcriptional effects of mutations in TFIIH in Drosophila development. Mol. Biol. Cell 13, 3246-3256.
47. Milan, M. (1998). Cell cycle control in the Drosophila wing. BioEssays 20, 969-971. (Pubitemid 29032173)
48. Mitchell, N., Cranna, N., Richardson, H. and Quinn, L. (2008). The Ecdysone-inducible zinc-finger transcription factor Crol regulates Wg transcription and cell cycle progression in Drosophila. Development 135, 2707-2716.
49. Mounkes, L. C. and Fuller, M. T. (1999). Molecular characterization of mutant alleles of the DNA repair/basal transcription factor haywire/ERCC3 in Drosophila. Genetics 152, 291-297.
50. Mounkes, L. C., Jones, R. S., Liang, B. C., Gelbart, W. and Fuller, M. T. (1992). A Drosophila model for xeroderma pigmentosum and Cockayne's syndrome: haywire encodes the fly homolog of ERCC3, a human excision repair gene. Cell 71, 925-937.
51. Orian, A., van Steensel, B., Delrow, J., Bussemaker, H. J., Li, L., Sawado, T., Williams, E., Loo, L. W. M., Cowley, S. M., Yost, C. et al. (2003). Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 17, 1101-1114.
52. Orian, A., Grewal, S. S., Knoepfler, P. S., Edgar, B. A., Parkhurst, S. M. and Eisenman, R. N. (2005). Genomic binding and transcriptional regulation by the Drosophila Myc and Mnt transcription factors. Cold Spring Harbor Symp. Quant. Biol. 70, 299-307.
53. Perez-Garijo, A., Martin, F. A. and Morata, G. (2004). Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131, 5591-5598.
54. Peter, A., Schottler, P., Werner, M., Beinert, N., Dowe, G., Burkert, P., Mourkioti, F., Dentzer, L., He, Y., Deak, P. et al. (2002). Mapping and identification of essential gene functions on the X chromosome of Drosophila. EMBO Rep. 3, 34-38. (Pubitemid 34144812)
55. Pierce, S. B., Yost, C., Britton, J. S., Loo, L. W., Flynn, E. M., Edgar, B. A. and Eisenman, R. N. (2004). dMyc is required for larval growth and endoreplication in Drosophila. Development 131, 2317-2327.
56. Poortinga, G., Hannan, K. M., Snelling, H., Walkley, C. R., Jenkins, A., Sharkey, K., Wall, M., Brandenburger, Y., Palatsides, M., Pearson, R. B. et al. (2004). MAD1 and c-MYC regulate UBF and rDNA transcription during granulocyte differentiation. EMBO J. 23, 3325-3335.
57. Prober, D. A. and Edgar, B. A. (2002). Interactions between Ras1, dMyc, and dPI3K signaling in the developing Drosophila wing. Genes Dev. 16, 2286-2299.
58. Quinn, L. M., Herr, A., McGarry, T. J. and Richardson, H. (2001). The Drosophila Geminin homolog: roles for Geminin in limiting DNA replication, in anaphase and in neurogenesis. Genes Dev. 15, 2741-2754. (Pubitemid 32988883)
59. Quinn, L. M., Dickins, R. A., Coombe, M., Hime, G. R., Bowtell, D. D. and Richardson, H. (2004). Drosophila Hfp negatively regulates dmyc and stg to inhibit cell proliferation. Development 131, 1411-1423.
60. Regan, C. L. and Fuller, M. T. (1988). Interacting genes that affect microtubule function: the nc2 allele of the haywire locus fails to complement mutations in the testis-specific beta-tubulin gene of Drosophila. Genes Dev. 2, 82-92.
61. Reyes, R. and Izquierdo, J. M. (2008). Half pint couples transcription and splicing of eIF4E-1,2 gene during fly development. Biochem. Biophys. Res. Commun. 374, 758-762.
62. Ruggero, D., Montanaro, L., Ma, L., Xu, W., Londei, P., Cordon-Cardo, C. and Pandolfi, P. P. (2004). The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat. Med. 10, 484-486.
63. Ryoo, H. D., Gorenc, T. and Steller, H. (2004). Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev. Cell 7, 491-501.
64. Schmidt, E. V. (1999). The role of c-myc in cellular growth control. Oncogene 18, 2988-2996. (Pubitemid 29276538)
65. Schreiber-Agus, N., Stein, D., Chen, K., Goltz, J. S., Stevens, L. and DePinho, R. A. (1997). Drosophila Myc is oncogenic in mammalian cells and plays a role in the diminutive phenotype. Proc. Natl. Acad. Sci. USA 94, 1235-1240.
66. Siddall, N. A., Lin, J. I., Hime, G. R. and Quinn, L. M. (2009). Myc-what we have learned from flies. Curr. Drug Targets 10, 590-601.
67. Spencer, C. A. and Groudine, M. (1990). Molecular analysis of the c-myc transcription elongation block. Implications for the generation of Burkitt's lymphoma. Ann. NY Acad. Sci. 599, 12-28.
68. Strobl, L. J. and Eick, D. (1992). Hold back of RNA polymerase II at the transcription start site mediates down-regulation of c-myc in vivo. EMBO J. 11, 3307-3314.
69. Van Buskirk, C. and Schupbach, T. (2002). Half pint regulates alternative splice site selection in Drosophila. Dev. Cell 2, 343-353.
70. Vennstrom, B., Sheiness, D., Zabielski, J. and Bishop, J. M. (1982). Isolation and characterization of c-myc, a cellular homolog of the oncogene (v-myc) of avian myelocytomatosis virus strain 29. J. Virol. 42, 773-779.
71. Weber, A., Liu, J., Collins, I. and Levens, D. (2005). TFIIH operates through an expanded proximal promoter to fine tune c-myc expression. Mol. Cell 25, 147-161. (Pubitemid 40039807)
72. Wells, B. S., Yoshida, E. and Johnston, L. A. (2006). Compensatory proliferation in Drosophila imaginal discs requires Dronc-dependent p53 activity. Curr. Biol. 16, 1606-1615.