Peptidergic neurosecretory cells in insects: Organization and control by the bHLH protein DIMMED

General and Comparative Endocrinology

Volumn 162, Issue 1, 2009, Pages 2-7

  Park, Dongkook ^a   Taghert, Paul H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

bHLH; Drosophila; Neurosecretory neuron; Regulated secretory pathway

Indexed keywords

INSECT PROTEIN; PROTEIN DIMMED; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL SURVIVAL; DROSOPHILA; GENE STRUCTURE; INSECT CELL; NEUROSECRETORY CELL; NONHUMAN; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 65049085590     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2008.12.012     Document Type: Article

References (51)

1. Acampora D., Postiglione M.P., Avantaggiato V., Di Bonito M., Vaccarino F.M., Michaud J., and Simeone A. Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia gene. Genes Dev. 13 (1999) 2787-2800
2. Allan D.W., St. Pierre S.E., Miguel-Aliaga I., and Thor S. Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113 (2003) 73-86
3. Allan D.W., Park D., St. Pierre S.E., Taghert P.H., and Thor S. Regulators acting in combinatorial codes also act independently in single differentiating neurons. Neuron 45 (2005) 689-700
4. Arvan P., and Castle D. Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem. J. 332 (1998) 593-610
5. Baumgardt M., Miguel-Aliaga I., Karlsson D., Ekman H., and Thor S. Specification of neuronal identities by feed forward combinatorial coding. PLoS Biol. 5 (2007) e37
6. Beuret N., Stettler H., Renold A., Rutishauser J., and Spiess M. Expression of regulated secretory proteins is sufficient to generate granule-like structures in constitutively secreting cells. J. Biol. Chem. 279 (2004) 20242-20249
7. Cheng L., Arata A., Mizuguchi R., Qian Y., Karunaratne A., Gray P.A., Arata S., Shirasawa S., Bouchard M., Luo P., Chen C.L., Busslinger M., Goulding M., Onimaru H., and Ma Q. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci. 7 (2004) 510-517
8. Crivellato E., Nico B., Bertelli E., Nussdorfer G.G., and Ribatti D. Dense-core granules in neuroendocrine cells and neurons release their secretory constituents by piecemeal degranulation. Int. J. Mol. Med. 18 (2006) 1037-1046
9. Czyzyk T.A., Ning Y., Hsu M.S., Peng B., Mains R.E., Eipper B.A., and Pintar J.E. Deletion of peptide amidation enzymatic activity leads to edema and embryonic lethality in the mouse. Dev. Biol. 287 (2005) 301-313
10. Day R., Benjannet S., Matsuuchi L., Kelly R.B., Marcinkiewicz M., Chrétien M., and Seidah N.G. Maintained PC1 and PC2 expression in the AtT-20 variant cell line 6T3 lacking regulated secretion and POMC: restored POMC expression and regulated secretion after cAMP treatment. DNA Cell Biol. 14 (1995) 175-188
11. Ding Y.Q., Marklund U., Yuan W., Yin J., Wegman L., Ericson J., Deneris E., Johnson R.L., and Chen Z.F. Lmx1b is essential for the development of serotonergic neurons. Nat. Neurosci. 6 (2003) 933-938
12. Eipper B.A., Stoffers D.A., and Mains R.E. The biosynthesis of neuropeptides: peptide α-amidation. Annu. Rev. Neurosci. 15 (1992) 57-85
13. Fukuda M., Kanno E., and Yamamoto A. Rabphilin and Noc2 are recruited to dense-core vesicles through specific interaction with Rab27A in PC12 cells. J. Biol. Chem. 279 (2004) 13065-13075
14. Gauthier S.A., and Hewes R.S. Transcriptional regulation of neuropeptide and peptide hormone expression by the Drosophila dimmed and cryptocephal genes. J. Exp. Biol. 209 (2006) 1803-1815
15. Goshu E., Jin H., Lovejoy J., Marion J.F., Michaud J.L., and Fan C.M. Sim2 contributes to neuroendocrine hormone gene expression in the anterior hypothalamus. Mol. Endocrinol. 18 (2004) 1251-1262
16. Guo X., Cheng L., Liu Y., Fan W., and Lu D. Cloning, expression, and functional characterization of zebrafish Mist1. Biochem. Biophys. Res. Commun. 59 (2007) 20-26
17. Han M., Park D., Vanderzalm P.J., Mains R.E., Eipper B.A., and Taghert P.H. Drosophila uses two distinct neuropeptide amidating enzymes, dPAL1 and dPAL2. J. Neurochem. 90 (2004) 129-141
18. Hewes R.S., Schaefer A.M., and Taghert P.H. The cryptocephal gene (ATF4) encodes multiple basic leucine zipper proteins controlling molting and metamorphosis in Drosophila. Genetics 155 (2000) 1711-1723
19. Hewes R.S., Park D., Gauthier S.A., Schaefer A.M., and Taghert P.H. The bHLH protein DIMMED controls neuroendocrine cell differentiation in Drosophila. Development 130 (2003) 1771-1781
20. Hewes R.S., Gu T., Brewster J.A., Qu C., and Zhao T. Regulation of secretory protein expression in mature cells by DIMM, a basic helix-loop-helix neuroendocrine differentiation factor. J. Neurosci. 26 (2006) 7860-7869
21. Hosoya T., Oda Y., Takahashi S., Morita M., Kawauchi S., Ema M., Yamamoto M., and Fujii-Kuriyama Y. Defective development of secretory neurons in the hypothalamus of Arnt2-knockout mice. Genes Cells 6 (2001) 361-374
22. Husain Q.M., and Ewer J. Use of targetable gfp-tagged neuropeptide for visualizing neuropeptide release following execution of a behavior. J. Neurobiol. 59 (2004) 181-191
23. Jiang N., Kolhekar A.S., Jacobs P.S., Mains R.E., Eipper B.A., and Taghert P.H. PHM is required for normal developmental transitions and for biosynthesis of secretory peptides in Drosophila. Dev. Biol. 226 (2000) 118-136
24. Johnson C.L., Kowalik A.S., Rajakumar N., and Pin C.L. Mist1 is necessary for the establishment of granule organization in serous exocrine cells of the gastrointestinal tract. Mech. Dev. 121 (2004) 261-272
25. Kim T., Tao-Cheng J.H., Eiden L.E., and Loh Y.P. Chromogranin A, an "on/off" switch controlling dense-core secretory granule biogenesis. Cell 106 (2001) 499-509
26. Kim S.K., and Rulifson E.J. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431 (2004) 316-320
27. Kim Y.J., Zitnan D., Galizia C.G., Cho K.H., and Adams M.E. A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr. Biol. 16 (2006) 1395-1407
28. Kolhekar A.S., Roberts M.S., Jiang N., Johnson R.C., Mains R.E., Eipper B.A., and Taghert P.H. Neuropeptide amidation in Drosophila: separate genes encode the two enzymes catalyzing amidation. J. Neurosci. 17 (1997) 1363-1376
29. 2+ signaling, and exocytosis in Mist1 null mice. J. Biol. Chem. 280 (2005) 12668-12675
30. Massari M.E., and Murre C. Helix-loop-helix proteins: regulators of transcription in eukaryotes. Mol. Cell Biol. 20 (2000) 429-440
31. McBrayer Z., Ono H., Shimell M., Parvy J.P., Beckstead R.B., Warren J.T., Thummel C.S., Dauphin-Villemant C., Gilbert L.I., and O'Connor M.B. Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev. Cell 13 (2007) 857-871
32. Malosio M.L., Benfante R., Racchetti G., Borgonovo B., Rosa P., and Meldolesi J. Neurosecretory cells without neurosecretion: evidence of an independently regulated trait of the cell phenotype. J. Physiol. 520 (1999) 43-52
33. Martin T.F. Tuning exocytosis for speed: fast and slow modes. Biochim. Biophys. Acta 1641 (2003) 157-165
34. Michaud J.L., Rosenquist T., May N.R., and Fan C.M. Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev. 12 (1998) 3264-3275
35. Miguel-Aliaga I., Thor S., and Gould A.P. Post-mitotic specification of Drosophila insulinergic neurons from pioneer neurons. PLoS Biol. 6 (2008) e58
36. Moore A.W., Barbel S., Jan L.Y., and Jan Y.N. A genome wide survey of basic helix-loop-helix factors in Drosophila. Proc. Natl. Acad. Sci. USA 97 (2000) 10436-10441
37. Nakai S., Kawano H., Yudate T., Nishi M., Kuno J., Nagata A., Jishage K., Hamada H., Fujii H., Kawamura K., et al. The POU domain transcription factor Brn2 is required for the determination of specific neuronal lineages in the hypothalamus of the mouse. Genes Dev. 9 (1995) 3109-3121
38. O'Donnell P.J., Driscoll W.J., Bäck N., Muth E., and Mueller G.P. Peptidylglycine-α-amidating monooxygenase and pro-atrial natriuretic peptide constitute the major membrane-associated proteins of rat atrial secretory granules. J. Mol. Cell Cardiol. 35 (2003) 915-922
39. Ouafik L., May V., Keutmann H.T., and Eipper B.A. Developmental regulation of peptidylglycine α-amidating monooxygenase PAM, in rat heart atrium and ventricle. Tissue-specific changes in distribution of PAM activity, mRNA levels, and protein forms. J. Biol. Chem. 264 (1992) 5839-5845
40. Pance A., Livesey F.J., and Jackson A.P. A role for the transcriptional repressor REST in maintaining the phenotype of neurosecretory-deficient PC12 cells. J. Neurochem. 99 (2006) 1435-1444
41. Park D., Han M., Kim Y.C., Han K.A., and Taghert P.H. Ap-let neurons-a peptidergic circuit potentially controlling ecdysial behavior in Drosophila. Dev. Biol. 269 (2004) 95-108
42. Park D., Veenstra J.A., Park J.H., and Taghert P.H. Mapping peptidergic cells in Drosophila: where DIMM fits in. PLoS ONE 3 (2008) e1896
43. Park D., Shafer O.T., Shepherd S.P., Suh H., Trigg J.S., and Taghert P.H. The Drosophila basic helix-loop-helix protein DIMMED directly activates PHM, a gene-encoding a neuropeptide-amidating enzyme. Mol. Cell Biol. 28 (2008) 410-421
44. Pin C.L., Bonvissuto A.C., and Konieczny S.F. Mist1 expression is a common link among serous exocrine cells exhibiting regulated exocytosis. Anat. Rec. 259 (2000) 157-167
45. Ramsey V.G., Doherty J.M., Chen C.C., Stappenback T.S., Konieczny S.F., and Mills J.C. The maturation of mucus-secreting gastric progenitors into digestive-enzyme secreting zymogenic cells requires Mist1. Development 134 (2007) 211-222
46. Renn S.C., Park J.H., Rosbash M., Hall J.C., and Taghert P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99 (1999) 791-802
47. Reynolds S.E., Taghert P.H., and Truman J.W. Eclosion hormone and bursicon titres and the onset of hormonal responsiveness during the last day of adult development in Manduca sexta L. J. Exp. Biol. 78 (1979) 77-86
48. Schonemann M.D., Ryan A.K., McEvilly R.J., O'Connell S.M., Arias C.A., Kalla K.A., Li P., Sawchenko P.E., and Rosenfeld M.G. Development and survival of the endocrine hypothalamus and posterior pituitary gland requires the neuronal POU domain factor Brn2. Genes Dev. 9 (1995) 3122-3135
49. Tran T., Jia D., Sun Y., and Konieczny S.F. The bHLH domain of Mistl is sufficient to activate gene transcription. Gene Expr. 13 (2007) 241-253
50. Wang W., and Lufkin T. The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev. Biol. 227 (2000) 432-449
51. Zitnan D., Kingan T.G., Hermesman J.L., and Adams M.E. Identification of ecdysis-triggering hormone from an epitracheal endocrine system. Science 271 (1996) 88-91