The Drosophila Basic Helix-Loop-Helix Protein DIMMED Directly Activates PHM, a Gene Encoding a Neuropeptide-Amidating Enzyme

REFERENCES

• Acampora, D., M. P. Postiglione, V. Avantaggiato, M. Di Bonito, F. M. Vaccarino, J. Michaud, and A. Simeone. 1999. Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia gene. Genes Dev. 13:2787–2800.
   PubMedGoogle Scholar
• Allan, D. W., D. Park, S. E. St. Pierre, P. H. Taghert, and S. Thor. 2005. Regulators acting in combinatorial codes also act independently in single differentiating neurons. Neuron 45:689–700.
   PubMedGoogle Scholar
• Allan, D. W., S. E. St. Pierre, I. Miguel-Aliaga, and S. Thor. 2003. Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113:73–86.
   PubMedGoogle Scholar
• Barolo, S., L. A. Carver, and J. W. Posakony. 2000. GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. BioTechniques 29:726–732.
   PubMed Web of Science ®Google Scholar
• Baumgardt, M., I. Miguel-Aliaga, D. Karlsson, H. Ekman, and S. Thor. 2007. Specification of neuronal identities by feedforward combinatorial coding. PLoS Biol. 5:e37.
   PubMedGoogle Scholar
• Benveniste, R. J., S. Thor, J. B. Thomas, and P. H. Taghert. 1998. Cell type-specific regulation of the Drosophila FMRF-NH2 neuropeptide gene by Apterous, a LIM homeodomain transcription factor. Development 125:4757–4765.
   PubMedGoogle Scholar
• Bertrand, N., D. S. Castro, and F. Guillemot. 2002. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3:517–530.
   PubMed Web of Science ®Google Scholar
• Borges, M., R. I. Linnoila, H. J. van de Velde, H. Chen, B. D. Nelkin, M. Mabry, S. B. Baylin, and D. W. Ball. 1997. An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 386:852–855.
   PubMed Web of Science ®Google Scholar
• Burbach, G. J., K. H. Kim, A. S. Zivony, A. Kim, J. Aranda, S. Wright, S. M. Naik, S. W. Caughman, J. C. Ansel, and C. A. Armstrong. 2001. The neurosensory tachykinins substance P and neurokinin A directly induce keratinocyte nerve growth factor. J. Investig. Dermatol. 117:1075–1082.
   PubMedGoogle Scholar
• Cabrera, C. V., and M. C. Alonso. 1991. Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. EMBO J. 10:2965–2973.
   PubMedGoogle Scholar
• Campuzano, S., L. Carramolino, C. V. Cabrera, M. Ruiz-Gomez, R. Villares, A. Boronat, and J. Modolell. 1985. Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell 40:327–338.
   PubMed Web of Science ®Google Scholar
• Castanon, I., S. Von Stetina, J. Kass, and M. K. Baylies. 2001. Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128:3145–3159.
   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
• Cronmiller, C., P. Schedl, and T. W. Cline. 1988. Molecular characterization of daughterless, a Drosophila sex determination gene with multiple roles in development. Genes Dev. 2:1666–1676.
   PubMed Web of Science ®Google Scholar
• Eipper, B. A., B. T. Bloomquist, E. J. Husten, S. L. Milgram, and R. E. Mains. 1993. Peptidylglycine alpha-amidating monooxygenase and other processing enzymes in the neurointermediate pituitary. Ann. N. Y. Acad. Sci. 680:147–160.
   PubMedGoogle Scholar
• Fisher, A., and M. Caudy. 1998. The function of hairy-related bHLH repressor proteins in cell fate decisions. Bioessays 20:298–306.
   PubMed Web of Science ®Google Scholar
• Gauthier, S. A., and R. S. Hewes. 2006. Transcriptional regulation of neuropeptide and peptide hormone expression by the Drosophila dimmed and cryptocephal genes. J. Exp. Biol. 209:1803–1815.
   PubMedGoogle Scholar
• Hendricks, T., N. Francis, D. Fyodorov, and E. S. Deneris. 1999. The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J. Neurosci. 19:10348–10356.
   PubMed Web of Science ®Google Scholar
• Herrero, P., M. Magarinos, L. Torroja, and I. Canal. 2003. Neurosecretory identity conferred by the apterous gene: lateral horn leucokinin neurons in Drosophila. J. Comp. Neurol. 457:123–132.
   PubMedGoogle Scholar
• Hewes, R. S., T. Gu, J. A. Brewster, C. Qu, and T. Zhao. 2006. Regulation of secretory protein expression in mature cells by DIMM, a basic helix-loop-helix neuroendocrine differentiation factor. J. Neurosci. 26:7860–7869.
   PubMedGoogle Scholar
• Hewes, R. S., D. Park, S. A. Gauthier, A. M. Schaefer, and P. H. Taghert. 2003. The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130:1771–1781.
   PubMed Web of Science ®Google Scholar
• Hewes, R. S., and P. H. Taghert. 2001. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 11:1126–1142.
   PubMed Web of Science ®Google Scholar
• Hindmarch, C., S. Yao, G. Beighton, J. Paton, and D. Murphy. 2006. A comprehensive description of the transcriptome of the hypothalamoneurohypophyseal system in euhydrated and dehydrated rats. Proc. Natl. Acad. Sci. USA 103:1609–1614.
   PubMedGoogle Scholar
• Hosoya, T., Y. Oda, S. Takahashi, M. Morita, S. Kawauchi, M. Ema, M. Yamamoto, and Y. Fujii-Kuriyama. 2001. Defective development of secretory neurones in the hypothalamus of Arnt2-knockout mice. Genes Cells 6:361–374.
   PubMedGoogle Scholar
• Jiang, N., A. S. Kolhekar, P. S. Jacobs, R. E. Mains, B. A. Eipper, and P. H. Taghert. 2000. PHM is required for normal developmental transitions and for biosynthesis of secretory peptides in Drosophila. Dev. Biol. 226:118–136.
   PubMedGoogle Scholar
• Keith, B., D. M. Adelman, and M. C. Simon. 2001. Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt. Proc. Natl. Acad. Sci. USA 98:6692–6697.
   PubMed Web of Science ®Google Scholar
• Kim, H. S., H. Seo, C. Yang, J. F. Brunet, and K. S. Kim. 1998. Noradrenergic-specific transcription of the dopamine beta-hydroxylase gene requires synergy of multiple cis-acting elements including at least two Phox2a-binding sites. J. Neurosci. 18:8247–8260.
   PubMed Web of Science ®Google Scholar
• Kolhekar, A. S., M. S. Roberts, N. Jiang, R. C. Johnson, R. E. Mains, B. A. Eipper, and P. H. Taghert. 1997. Neuropeptide amidation in Drosophila: separate genes encode the two enzymes catalyzing amidation. J. Neurosci. 17:1363–1376.
   PubMed Web of Science ®Google Scholar
• Lemercier, C., R. Q. To, R. A. Carrasco, and S. F. Konieczny. 1998. The basic helix-loop-helix transcription factor Mist1 functions as a transcriptional repressor of myoD. EMBO J. 17:1412–1422.
   PubMed Web of Science ®Google Scholar
• Massari, M. E., and C. Murre. 2000. Helix-loop-helix proteins: regulators of transcription in eukaryotic organisms. Mol. Cell. Biol. 20:429–440.
   PubMed Web of Science ®Google Scholar
• Michaud, J. L., C. DeRossi, N. R. May, B. C. Holdener, and C. M. Fan. 2000. ARNT2 acts as the dimerization partner of SIM1 for the development of the hypothalamus. Mech. Dev. 90:253–261.
   PubMedGoogle Scholar
• Michaud, J. L., T. Rosenquist, N. R. May, and C. M. Fan. 1998. Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev. 12:3264–3275.
   PubMedGoogle Scholar
• Miguel-Aliaga, I., D. W. Allan, and S. Thor. 2004. Independent roles of the dachshund and eyes absent genes in BMP signaling, axon pathfinding and neuronal specification. Development 131:5837–5848.
   PubMedGoogle Scholar
• Moore, A. W., S. Barbel, L. Y. Jan, and Y. N. Jan. 2000. A genomewide survey of basic helix-loop-helix factors in Drosophila. Proc. Natl. Acad. Sci. USA 97:10436–10441.
   PubMedGoogle Scholar
• Morin, X., H. Cremer, M. R. Hirsch, R. P. Kapur, C. Goridis, and J. F. Brunet. 1997. Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 18:411–423.
   PubMed Web of Science ®Google Scholar
• Nakai, S., H. Kawano, T. Yudate, M. Nishi, J. Kuno, A. Nagata, K. Jishage, H. Hamada, H. Fujii, K. Kawamura, et al. 1995. The POU domain transcription factor Brn-2 is required for the determination of specific neuronal lineages in the hypothalamus of the mouse. Genes Dev. 9:3109–3121.
   PubMedGoogle Scholar
• Nakajima, Y., M. Morimoto, Y. Takahashi, H. Koseki, and Y. Saga. 2006. Identification of Epha4 enhancer required for segmental expression and the regulation by Mesp2. Development 133:2517–2525.
   PubMedGoogle Scholar
• Nassel, D. R., and U. Homberg. 2006. Neuropeptides in interneurons of the insect brain. Cell Tissue Res. 326:1–24.
   PubMedGoogle Scholar
• Ohsako, S., J. Hyer, G. Panganiban, I. Oliver, and M. Caudy. 1994. Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 8:2743–2755.
   PubMedGoogle Scholar
• Park, D., M. Han, Y. C. Kim, K. A. Han, and P. H. Taghert. 2004. Ap-let neurons: a peptidergic circuit potentially controlling ecdysial behavior in Drosophila. Dev. Biol. 269:95–108.
   PubMedGoogle Scholar
• Pattyn, A., X. Morin, H. Cremer, C. Goridis, and J. F. Brunet. 1999. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366–370.
   PubMed Web of Science ®Google Scholar
• Pin, C. L., A. C. Bonvissuto, and S. F. Konieczny. 2000. Mist1 expression is a common link among serous exocrine cells exhibiting regulated exocytosis. Anat. Rec. 259:157–167.
   PubMedGoogle Scholar
• Pin, C. L., J. M. Rukstalis, C. Johnson, and S. F. Konieczny. 2001. The bHLH transcription factor Mist1 is required to maintain exocrine pancreas cell organization and acinar cell identity. J. Cell Biol. 155:519–530.
   PubMedGoogle Scholar
• Powell, L. M., P. I. Zur Lage, D. R. Prentice, B. Senthinathan, and A. P. Jarman. 2004. The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. Mol. Cell. Biol. 24:9517–9526.
   PubMed Web of Science ®Google Scholar
• Ramsey, V. G., J. M. Doherty, C. C. Chen, T. S. Stappenbeck, S. F. Konieczny, and J. C. Mills. 2007. The maturation of mucus-secreting gastric epithelial progenitors into digestive-enzyme secreting zymogenic cells requires Mist1. Development 134:211–222.
   PubMedGoogle Scholar
• Rukstalis, J. M., A. Kowalik, L. Zhu, D. Lidington, C. L. Pin, and S. F. Konieczny. 2003. Exocrine specific expression of Connexin32 is dependent on the basic helix-loop-helix transcription factor Mist1. J. Cell Sci. 116:3315–3325.
   PubMedGoogle Scholar
• Rushlow, C. A., A. Hogan, S. M. Pinchin, K. M. Howe, M. Lardelli, and D. Ish-Horowicz. 1989. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 8:3095–3103.
   PubMedGoogle Scholar
• Schonemann, M. D., A. K. Ryan, R. J. McEvilly, S. M. O'Connell, C. A. Arias, K. A. Kalla, P. Li, P. E. Sawchenko, and M. G. Rosenfeld. 1995. Development and survival of the endocrine hypothalamus and posterior pituitary gland requires the neuronal POU domain factor Brn-2. Genes Dev. 9:3122–3135.
   PubMedGoogle Scholar
• Swanson, D. J., E. Zellmer, and E. J. Lewis. 1997. The homeodomain protein Arix interacts synergistically with cyclic AMP to regulate expression of neurotransmitter biosynthetic genes. J. Biol. Chem. 272:27382–27392.
   PubMedGoogle Scholar
• Taghert, P. H., R. S. Hewes, J. H. Park, M. A. O'Brien, M. Han, and M. E. Peck. 2001. Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila. J. Neurosci. 21:6673–6686.
   PubMedGoogle Scholar
• Taghert, P. H., and L. E. Schneider. 1990. Interspecific comparison of a Drosophila gene encoding FMRFamide-related neuropeptides. J. Neurosci. 10:1929–1942.
   PubMedGoogle Scholar
• Taghert, P. H., and J. A. Veenstra. 2003. Drosophila neuropeptide signaling. Adv. Genet. 49:1–65.
   PubMedGoogle Scholar
• Wang, W., and T. Lufkin. 2000. The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev. Biol. 227:432–449.
   PubMedGoogle Scholar
• Yang, C., H. S. Kim, H. Seo, C. H. Kim, J. F. Brunet, and K. S. Kim. 1998. Paired-like homeodomain proteins, Phox2a and Phox2b, are responsible for noradrenergic cell-specific transcription of the dopamine beta-hydroxylase gene. J. Neurochem. 71:1813–1826.
   PubMedGoogle Scholar
• Yoo, S. H., C. H. Ko, P. L. Lowrey, E. D. Buhr, E. J. Song, S. Chang, O. J. Yoo, S. Yamazaki, C. Lee, and J. S. Takahashi. 2005. A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo. Proc. Natl. Acad. Sci. USA 102:2608–2613.
   PubMed Web of Science ®Google Scholar
• Zellmer, E., Z. Zhang, D. Greco, J. Rhodes, S. Cassel, and E. J. Lewis. 1995. A homeodomain protein selectively expressed in noradrenergic tissue regulates transcription of neurotransmitter biosynthetic genes. J. Neurosci. 15:8109–8120.
   PubMedGoogle Scholar
• Zhu, L., T. Tran, J. M. Rukstalis, P. Sun, B. Damsz, and S. F. Konieczny. 2004. Inhibition of Mist1 homodimer formation induces pancreatic acinar-to-ductal metaplasia. Mol. Cell. Biol. 24:2673–2681.
   PubMed Web of Science ®Google Scholar