Cooperative Action of Multiple cis-Acting Elements Is Required for N-myc Expression in Branchial Arches: Specific Contribution of GATA3

REFERENCES

• Alt, F. W., R. DePinho, K. Zimmerman, E. Legouy, K. Hatton, P. Ferrier, A. Tesfaye, G. Yancopoulos, and P. Nisen. 1986. The human myc gene family. Cold Spring Harbor Symp. Quant. Biol. 51:931–941.
   PubMedGoogle Scholar
• Aubry, S., and J. Charron. 2000. N-Myc shares cellular functions wih c-Myc. DNA Cell Biol. 19:353–364.
   PubMedGoogle Scholar
• Babiss, L. E., and J. M. Friedman. 1990. Regulation of N-myc gene expression: use of an adenovirus vector to demonstrate posttranscriptional control. Mol. Cell. Biol. 10:6700–6708.
   PubMedGoogle Scholar
• Baena, E., M. Ortiz, A. C. Martinez, and I. M. de Alboran. 2007. c-Myc is essential for hematopoietic stem cell differentiation and regulates Lin(-)Sca-1(+)c-Kit(-) cell generation through p21. Exp. Hematol. 35:1333–1343.
   PubMed Web of Science ®Google Scholar
• Ball, N. S., and P. H. King. 1997. Neuron-specific Hel-N1 and HuD as novel molecular markers of neuroblastoma: a correlation of HuD messenger RNA levels with favorable prognostic features. Clin. Cancer Res. 3:1859–1865.
   PubMedGoogle Scholar
• Blanchette, M., A. R. Bataille, X. Chen, C. Poitras, J. Laganiere, C. Lefebvre, G. Deblois, V. Giguere, V. Ferretti, D. Bergeron, B. Coulombe, and F. Robert. 2006. Genome-wide computational prediction of transcriptional regulatory modules reveals new insights into human gene expression. Genome Res. 16:656–668.
   PubMed Web of Science ®Google Scholar
• Burch, J. B. 2005. Regulation of GATA gene expression during vertebrate development. Semin. Cell. Dev. Biol. 16:71–81.
   PubMed Web of Science ®Google Scholar
• Caudy, M., H. Vassin, M. Brand, R. Tuma, L. Y. Jan, and Y. N. Jan. 1988. Daughterless, a Drosophila gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex. Cell 55:1061–1067.
   PubMed Web of Science ®Google Scholar
• Chagnovich, D., B. E. Fayos, and S. L. Cohn. 1996. Differential activity of ELAV-like RNA-binding proteins in human neuroblastoma. J. Biol. Chem. 271:33587–33591.
   PubMedGoogle Scholar
• Charron, J., J. F. Gagnon, and J. F. Cadrin-Girard. 2002. Identification of N-myc regulatory regions involved in embryonic expression. Pediatr. Res. 51:48–56.
   PubMedGoogle Scholar
• Charron, J., B. A. Malynn, P. Fisher, V. Stewart, L. Jeannotte, S. P. Goff, E. J. Robertson, and F. W. Alt. 1992. Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes Dev. 6:2248–2257.
   PubMed Web of Science ®Google Scholar
• Conlon, R. A., A. G. Reaume, and J. Rossant. 1995. Notch1 is required for the coordinate segmentation of somites. Development 121:1533–1545.
   PubMed Web of Science ®Google Scholar
• Debacker, C., M. Catala, and M. C. Labastie. 1999. Embryonic expression of the human GATA-3 gene. Mech. Dev. 85:183–187.
   PubMed Web of Science ®Google Scholar
• DePinho, R. A., E. Legouy, L. B. Feldman, N. E. Kohl, G. D. Yancopoulos, and F. W. Alt. 1986. Structure and expression of the murine N-myc gene. Proc. Natl. Acad. Sci. U. S. A. 83:1827–1831.
   PubMedGoogle Scholar
• Downs, K. M., G. R. Martin, and J. M. Bishop. 1989. Contrasting patterns of myc and N-myc expression during gastrulation of the mouse embryo. Genes Dev. 3:860–869.
   PubMedGoogle Scholar
• Ferretti, V., C. Poitras, D. Bergeron, B. Coulombe, F. Robert, and M. Blanchette. 2007. PReMod: a database of genome-wide mammalian cis-regulatory module predictions. Nucleic Acids Res. 35:D122–D126.
   PubMedGoogle Scholar
• Fujiwara, Y., C. P. Browne, K. Cunniff, S. C. Goff, and S. H. Orkin. 1996. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc. Natl. Acad. Sci. U. S. A. 93:12355–12358.
   PubMed Web of Science ®Google Scholar
• Galderisi, U., G. Di Bernardo, M. Cipollaro, G. Peluso, A. Cascino, R. Cotrufo, and M. A. Melone. 1999. Differentiation and apoptosis of neuroblastoma cells: role of N-myc gene product. J. Cell. Biochem. 73:97–105.
   PubMed Web of Science ®Google Scholar
• Gray, P. A., H. Fu, P. Luo, Q. Zhao, J. Yu, A. Ferrari, T. Tenzen, D. I. Yuk, E. F. Tsung, Z. Cai, J. A. Alberta, L. P. Cheng, Y. Liu, J. M. Stenman, M. T. Valerius, N. Billings, H. A. Kim, M. E. Greenberg, A. P. McMahon, D. H. Rowitch, C. D. Stiles, and Q. Ma. 2004. Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306:2255–2257.
   PubMed Web of Science ®Google Scholar
• Henriksson, M., and B. Luscher. 1996. Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv. Cancer Res. 68:109–182.
   PubMed Web of Science ®Google Scholar
• Hiller, S., S. Breit, Z. Q. Wang, E. F. Wagner, and M. Schwab. 1991. Localization of regulatory elements controlling human Mycn expression. Oncogene 6:969–977.
   PubMedGoogle Scholar
• Hirning, U., P. Schmid, W. A. Schulz, G. Rettenberger, and H. Hameister. 1991. A comparative analysis of N-myc and c-myc expression and cellular proliferation in mouse organogenesis. Mech. Dev. 33:119–125.
   PubMed Web of Science ®Google Scholar
• Hirvonen, H., T. P. Makela, M. Sandberg, H. Kalimo, E. Vuorio, and K. Alitalo. 1990. Expression of the myc proto-oncogenes in developing human fetal brain. Oncogene 5:1787–1797.
   PubMed Web of Science ®Google Scholar
• Imamura, Y., S. M. Iguchi-Ariga, and H. Ariga. 1992. The upstream region of the mouse N-myc gene: identification of an enhancer element that functions preferentially in neuroblastoma IMR32 cells. Biochim. Biophys. Acta 1132:177–187.
   PubMedGoogle Scholar
• Imamura, Y., T. Nakagawa, S. M. Iguchi-Ariga, and H. Ariga. 1993. Transcriptional regulation of the N-myc gene: identification of positive regulatory element and its double- and single-stranded DNA binding proteins. Biochim. Biophys. Acta 1216:273–285.
   PubMedGoogle Scholar
• Kato, K., A. Kanamori, Y. Wakamatsu, S. Sawai, and H. Kondoh. 1991. Tissue distribution of N-myc expression in the early organogenesis period of the mouse embryo. Dev. Growth Differ. 33:29–36.
   Google Scholar
• Kenney, A. M., H. R. Widlund, and D. H. Rowitch. 2004. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131:217–228.
   PubMed Web of Science ®Google Scholar
• Knoepfler, P. S., P. F. Cheng, and R. N. Eisenman. 2002. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev. 16:2699–2712.
   PubMed Web of Science ®Google Scholar
• Koppen, A., R. Ait-Aissa, S. Hopman, J. Koster, F. Haneveld, R. Versteeg, and L. J. Valentijn. 2007. Dickkopf-1 is down-regulated by MYCN and inhibits neuroblastoma cell proliferation. Cancer Lett. 256:218–228.
   PubMed Web of Science ®Google Scholar
• Korinek, V., N. Barker, P. Moerer, E. van Donselaar, G. Huls, P. J. Peters, and H. Clevers. 1998. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19:379–383.
   PubMed Web of Science ®Google Scholar
• Kothary, R., S. Clapoff, S. Darling, M. D. Perry, L. A. Moran, and J. Rossant. 1989. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105:707–714.
   PubMed Web of Science ®Google Scholar
• Larochelle, C., M. L. Tremblay, D. Bernier, J. Aubin, and L. Jeannotte. 1999. Multiple cis-acting regulatory regions are required for restricted spatio-temporal Hoxa5 gene expression. Dev. Dyn. 214:127–140.
   PubMedGoogle Scholar
• Lazarova, D. L., B. A. Spengler, J. L. Biedler, and R. A. Ross. 1999. HuD, a neuronal-specific RNA-binding protein, is a putative regulator of N-myc pre-mRNA processing/stability in malignant human neuroblasts. Oncogene 18:2703–2710.
   PubMedGoogle Scholar
• Li, Y., H. Zhang, S. C. Choi, Y. Litingtung, and C. Chiang. 2004. Sonic Hedgehog signaling regulates Gli3 processing, mesenchymal proliferation, and differentiation during mouse lung organogenesis. Dev. Biol. 270:214–231.
   PubMedGoogle Scholar
• Lieuw, K. H., G. Li, Y. Zhou, F. Grosveld, and J. D. Engel. 1997. Temporal and spatial control of murine GATA-3 transcription by promoter- proximal regulatory elements. Dev. Biol. 188:1–16.
   PubMedGoogle Scholar
• Lim, K. C., G. Lakshmanan, S. E. Crawford, Y. Gu, F. Grosveld, and J. D. Engel. 2000. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat. Genet. 25:209–212.
   PubMed Web of Science ®Google Scholar
• Lutz, W., J. Leon, and M. Eilers. 2002. Contributions of Myc to tumorigenesis. Biochim. Biophys. Acta 1602:61–71.
   PubMed Web of Science ®Google Scholar
• Malynn, B. A., I. M. de Alboran, R. C. O'Hagan, R. T. Bronson, L. Davidson, R. DePinho, and F. W. Alt. 2000. N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation. Genes Dev. 14:1390–1399.
   PubMed Web of Science ®Google Scholar
• Manabe, A., S. M. Iguchi Ariga, H. Iizuka, and H. Ariga. 1996. Transcriptional repression activity of N-MYC protein requires phosphorylation by MAP kinase. Biochem. Biophys. Res. Commun. 219:813–823.
   PubMed Web of Science ®Google Scholar
• Manohar, C. F., M. L. Short, A. Nguyen, N. N. Nguyen, D. Chagnovich, Q. W. Yang, and S. L. Cohn. 2002. HuD, a neuronal-specific RNA-binding protein, increases the in vivo stability of MYCN RNA. J. Biol. Chem. 277:1967–1973.
   PubMedGoogle Scholar
• Martins, R. A., F. Zindy, S. Donovan, J. Zhang, S. Pounds, A. Wey, P. S. Knoepfler, R. N. Eisenman, M. F. Roussel, and M. A. Dyer. 2008. N-myc coordinates retinal growth with eye size during mouse development. Genes Dev. 22:179–193.
   PubMedGoogle Scholar
• Moens, C. B., A. B. Auerbach, R. A. Conlon, A. L. Joyner, and J. Rossant. 1992. A targeted mutation reveals a role for N-myc in branching morphogenesis in the embryonic mouse lung. Genes Dev. 6:691–704.
   PubMedGoogle Scholar
• Moens, C. B., B. R. Stanton, L. F. Parada, and J. Rossant. 1993. Defects in heart and lung development in compound heterozygotes for two different targeted mutations at the N-myc locus. Development 119:485–499.
   PubMedGoogle Scholar
• Morgenbesser, S. D., and R. A. DePinho. 1994. Use of transgenic mice to study myc family gene function in normal mammalian development and in cancer. Semin. Cancer Biol. 5:21–36.
   PubMed Web of Science ®Google Scholar
• Mugrauer, G., F. W. Alt, and P. Ekblom. 1988. N-myc proto-oncogene expression during organogenesis in the developing mouse as revealed by in situ hybridization. J. Cell Biol. 107:1325–1335.
   PubMed Web of Science ®Google Scholar
• Mugrauer, G., and P. Ekblom. 1991. Contrasting expression patterns of three members of the myc family of protooncogenes in the developing and adult mouse kidney. J. Cell Biol. 112:13–25.
   PubMed Web of Science ®Google Scholar
• O'Hagan, R. C., N. Schreiber-Agus, K. Chen, G. David, J. A. Engelman, R. Schwab, L. Alland, C. Thomson, D. R. Ronning, J. C. Sacchettini, P. Meltzer, and R. DePinho. 2000. Gene-target recognition among members of the myc superfamily and implications for oncogenesis. Nat. Genet. 24:113–119.
   PubMed Web of Science ®Google Scholar
• Okubo, T., P. S. Knoepfler, R. N. Eisenman, and B. L. Hogan. 2005. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 132:1363–1374.
   PubMed Web of Science ®Google Scholar
• Olson, E. N. 1990. MyoD family: a paradigm for development. Genes Dev. 4:1454–1461.
   PubMed Web of Science ®Google Scholar
• Pandolfi, P. P., M. E. Roth, A. Karis, M. W. Leonard, E. Dzierzak, F. G. Grosveld, J. D. Engel, and M. H. Lindenbaum. 1995. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet. 11:40–44.
   PubMedGoogle Scholar
• Pevny, L., C. S. Lin, V. D'Agati, M. C. Simon, S. H. Orkin, and F. Costantini. 1995. Development of hematopoietic cells lacking transcription factor GATA-1. Development 121:163–172.
   PubMed Web of Science ®Google Scholar
• Pilon, N., D. Raiwet, R. S. Viger, and D. W. Silversides. 2008. Novel pre- and post-gastrulation expression of Gata4 within cells of the inner cell mass and migratory neural crest cells. Dev. Dyn. 237:1133–1143.
   PubMedGoogle Scholar
• Ross, R. A., J. L. Biedler, and B. A. Spengler. 2003. A role for distinct cell types in determining malignancy in human neuroblastoma cell lines and tumors. Cancer Lett. 197:35–39.
   PubMed Web of Science ®Google Scholar
• Sawai, S., A. Shimono, Y. Wakamatsu, C. Palmes, K. Hanaoka, and H. Kondoh. 1993. Defects of embryonic organogenesis resulting from targeted disruption of the N-myc gene in the mouse. Development 117:1445–1455.
   PubMed Web of Science ®Google Scholar
• Schmid, P., W. A. Schulz, and H. Hameister. 1989. Dynamic expression pattern of the myc protooncogene in midgestation mouse embryos. Science 243:226–228.
   PubMed Web of Science ®Google Scholar
• Sivak, L. E., G. Pont-Kingdon, K. Le, G. Mayr, K. F. Tai, B. T. Stevens, and W. L. Carroll. 1999. A novel intron element operates posttranscriptionally to regulate human N-myc expression. Mol. Cell. Biol. 19:155–163.
   PubMedGoogle Scholar
• Sjostrom, S. K., G. Finn, W. C. Hahn, D. H. Rowitch, and A. M. Kenney. 2005. The Cdk1 complex plays a prime role in regulating N-myc phosphorylation and turnover in neural precursors. Dev. Cell 9:327–338.
   PubMed Web of Science ®Google Scholar
• Stanton, B. R., and L. F. Parada. 1992. The N-myc proto-oncogene: developmental expression and in vivo site-directed mutagenesis. Brain Pathol. 2:71–83.
   PubMedGoogle Scholar
• Stanton, B. R., A. S. Perkins, L. Tessarollo, D. A. Sassoon, and L. F. Parada. 1992. Loss of N-myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes Dev. 6:2235–2247.
   PubMed Web of Science ®Google Scholar
• Strieder, V., and W. Lutz. 2002. Regulation of N-myc expression in development and disease. Cancer Lett. 180:107–119.
   PubMedGoogle Scholar
• Tabaries, S., J. Lapointe, T. Besch, M. Carter, J. Woollard, C. K. Tuggle, and L. Jeannotte. 2005. Cdx protein interaction with Hoxa5 regulatory sequences contributes to Hoxa5 regional expression along the axial skeleton. Mol. Cell. Biol. 25:1389–1401.
   PubMedGoogle Scholar
• Tai, K. F., S. W. Rogers, G. Pont-Kingdon, and W. L. Carroll. 1999. Definition of the human N-myc promoter region during development in a transgenic mouse model. Pediatr. Res. 46:255–262.
   PubMedGoogle Scholar
• Thisse, B., C. Stoetzel, C. Gorostiza-Thisse, and F. Perrin-Schmitt. 1988. Sequence of the Twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J. 7:2175–2183.
   PubMed Web of Science ®Google Scholar
• van Genderen, C., R. M. Okamura, I. Farinas, R. G. Quo, T. G. Parslow, L. Bruhn, and R. Grosschedl. 1994. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8:2691–2703.
   PubMed Web of Science ®Google Scholar
• Villares, R., and C. V. Cabrera. 1987. The achaete-scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50:415–424.
   PubMed Web of Science ®Google Scholar
• Wada, R. K., R. C. Seeger, C. P. Reynolds, T. Alloggiamento, J. M. Yamashiro, C. Ruland, A. C. Black, and J. D. Rosenblatt. 1992. Cell type-specific expression and negative regulation by retinoic acid of the human N-myc promoter in neuroblastoma cells. Oncogene 7:711–717.
   PubMed Web of Science ®Google Scholar
• Wei, J. S., Y. K. Song, S. Durinck, Q. R. Chen, A. T. Cheuk, P. Tsang, Q. Zhang, C. J. Thiele, A. Slack, J. Shohet, and J. Khan. 2008. The MYCN oncogene is a direct target of miR-34a. Oncogene 27:5204–5213.
   PubMed Web of Science ®Google Scholar
• Woodruff, K. A., J. D. Rosenblatt, T. B. Moore, R. H. Medzoyan, D. S. M. Pai, J. L. Noland, J. M. Yamashiro, and R. K. Wada. 1995. Cell type-specific activity of the N-myc promoter in human neuroblastoma cells is mediated by a downstream silencer. Oncogene 10:1335–1341.
   PubMedGoogle Scholar
• Xin, M., C. A. Davis, J. D. Molkentin, C. L. Lien, S. A. Duncan, J. A. Richardson, and E. N. Olson. 2006. A threshold of GATA4 and GATA6 expression is required for cardiovascular development. Proc. Natl. Acad. U. S. A. 103:11189–11194.
   PubMed Web of Science ®Google Scholar
• Xu, L., Y. Meng, R. Wallen, and R. A. DePinho. 1995. Loss of transcriptional attenuation in N-myc is associated with progression towards a more malignant phenotype. Oncogene 11:1865–1872.
   PubMedGoogle Scholar
• Xu, L., R. Wallen, V. Patel, and R. A. DePinho. 1993. Role of first exon/intron sequences in the regulation of myc family oncogenic potency. Oncogene 8:2547–2553.
   PubMedGoogle Scholar
• Zimmerman, K., E. Legouy, V. Steward, R. A. DePinho, and F. W. Alt. 1990. Differential regulation of the N-myc gene in transfected cells and transgenic mice. Mol. Cell. Biol. 10:2096–2103.
   PubMedGoogle Scholar
• Zimmerman, K., G. D. Yancopoulos, R. G. Collum, R. K. Smith, N. E. Kohl, K. A. Denis, M. M. Nau, O. N. Witte, D. Toran-Allerand, C. E. Gee, J. D. Minna, and F. W. Alt. 1986. Differential expression of myc familly genes during murine development. Nature 319:780–783.
   PubMed Web of Science ®Google Scholar