Drosophila neuroendocrine cells comprising the corpora cardiaca (CC) are essential for systemic glucose regulation and represent functional orthologues of vertebrate pancreatic α-cells. Although Drosophila CC cells have been regarded as developmental orthologues of pituitary gland, the genetic regulation of CC development is poorly understood. From a genetic screen, we identified multiple novel regulators of CC development, including Notch signaling factors. Our studies demonstrate that the disruption of Notch signaling can lead to the expansion of CC cells. Live imaging demonstrates localized emergence of extra precursor cells as the basis of CC expansion in Notch mutants. Contrary to a recent report, we unexpectedly found that CC cells originate from head mesoderm. We show that Tinman expression in head mesoderm is regulated by Notch signaling and that the combination of Daughterless and Tinman is sufficient for ectopic CC specification in mesoderm. Understanding the cellular, genetic, signaling, and transcriptional basis of CC cell specification and expansion should accelerate discovery of molecular mechanisms regulating ontogeny of organs that control metabolism.
Vyšlo v časopise: Specification of Corpora Cardiaca Neuroendocrine Cells from Mesoderm Is Regulated by Notch Signaling. PLoS Genet 7(8): e32767. doi:10.1371/journal.pgen.1002241 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002241
1. RulifsonEJKimSKNusseR 2002 Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296 1118 1120
2. IkeyaTGalicMBelawatPNairzKHafenE 2002 Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 12 1293 1300
3. KimSKRulifsonEJ 2004 Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431 316 320
4. LeeGParkJH 2004 Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167 311 323
5. ParkDTaghertPH 2009 Peptidergic neurosecretory cells in insects: organization and control by the bHLH protein DIMMED. Gen Comp Endocrinol 162 2 7
6. AggarwalSKKingRC 1971 An electron microscopic study of the corpus cardiacum of adult Drosophila melanogaster and its afferent nerves. J Morphol 134 437 445
7. CognigniPBaileyAPMiguel-AliagaI 2010 Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab 13 92 104
8. HartensteinVTepassUGruszynski-DefeoE 1994 Embryonic development of the stomatogastric nervous system in Drosophila. J Comp Neurol 350 367 381
9. De VelascoBShenJGoSHartensteinV 2004 Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Dev Biol 274 280 294
10. De VelascoBMandalLMkrtchyanMHartensteinV 2006 Subdivision and developmental fate of the head mesoderm in Drosophila melanogaster. Dev Genes Evol 216 39 51
11. WangSTulinaNCarlinDLRulifsonEJ 2007 The origin of islet-like cells in Drosophila identifies parallels to the vertebrate endocrine axis. Proc Natl Acad Sci U S A 104 19873 19878
12. RyderEAshburnerMBautista-LlacerRDrummondJWebsterJ 2007 The DrosDel deletion collection: a Drosophila genomewide chromosomal deficiency resource. Genetics 177 615 629
13. Ochoa-EspinosaAYucelGKaplanLPareAPuraN 2005 The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila. Proc Natl Acad Sci U S A 102 4960 4965
14. JiangJLevineM 1993 Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72 741 752
15. RanganayakuluGSchulzRAOlsonEN 1996 Wingless signaling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev Bio 176 143 148
16. LieberTKiddSAlcamoECorbinVYoungMW 1993 Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev 7 1949 1965
17. LeptinM 1991 twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev 5 1568 1576
18. BayliesMKBateM 1996 twist: a myogenic switch in Drosophila. Science 272 1481 1484
19. CastanonIVon StetinaSKassJBayliesMK 2001 Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128 3145 3159
20. LaiZCFortiniMERubinGM 1991 The embryonic expression patterns of zfh-1 and zfh-2, two Drosophila genes encoding novel zinc-finger homeodomain proteins. Mech Dev 34 123 134
21. LillyBGalewskySFirulliABSchulzRAOlsonEN 1994 D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc Natl Acad Sci U S A 91 5662 5666
22. TaylorMVBeattyKEHunterHKBayliesMK 1995 Drosophila MEF2 is regulated by twist and is expressed in both the primordia and differentiated cells of the embryonic somatic, visceral and heart musculature. Mech Dev 50 29 41
23. ZaffranSAstierMGratecosDSemerivaM 1997 The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity. Development 124 2087 2098
24. YinZXuXLFraschM 1997 Regulation of the twist target gene tinman by modular cis-regulatory elements during early mesoderm development. Development 124 4971 4982
25. LeeYMParkTSchulzRAKimY 1997 Twist-mediated activation of the NK-4 homeobox gene in the visceral mesoderm of Drosophila requires two distinct clusters of E-box regulatory elements. J Biol Chem 272 17531 17541
26. CarmenaABateMJimenezF 1995 lethal of scute, a proneural gene participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev 9 2373 2383
27. Tapanes-CastilloABayliesMK 2004 Notch signaling patterns Drosophila mesodermal segments by regulating the bHLH transcription factor twist. Development 131 2359 2372
28. WongMCastanonWBayliesMK 2008 Daughterless dictates Twist activity in a context-dependent manner during somatic myogenesis. Dev Biol 317 417 429
29. HewesRSParkDGauthierSASchaeferAMTaghertPH 2003 The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130 1771 1781
30. HartensteinVTepassUGruszynski-deFeoE 1996 Proneural and neurogenic genes control specification and morphogenesis of stomatogastric nerve cell precursors in Drosophila. Dev Bio 173 213 227
31. Gonzalez-GaitanMJackleH 2000 Tip cell-derived RTK signaling initiates cell movement in the Drosophila stomatogastric nervous system anlage. EMBO Rep 1 366 371
32. HwangHJRulifsonE 2011 Serial specification of diverse neuroblast identities from a neurogenic placode by Notch and Egfr signaling. Development 138 2883 2893
33. ApelqvistALiHSommerLBeatusPAndersonDJ 1999 Notch signalling controls pancreatic cell differentiation. Nature 400 877 881
34. JensenJPedersenEEGalantePHaldJHellerRS 2000 Control of endodermal endocrine development by Hes-1. Nat Genet 24 36 44
35. KelbermanDRizzotiKLovell-BadgeRRobinsonICAFDattaniMT 2009 Genetic regulation of pituitary gland development in human and mouse. Endocr Rev 30 790 829
36. DuttaSDietrichJEWesterfieldMVargaZM 2008 Notch signaling regulates endocrine cell specification in the zebrafish anterior pituitary. Dev Biol 319 248 257
37. FoeVEAlbertsBM 1983 Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61 31 70
38. De VelascoBErclikTShyDSclafaniJLipshitzH 2007 Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev Biol 302 309 323
39. LammertECleaverOMeltonD 2001 Induction of pancreatic differentiation by signals from blood vessels. Science 294 564 567
40. MandalLBanerjeeUHartensteinV 2004 Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat Genet 36 1019 1023
41. QianLBodmerR 2009 Partial loss of GATA factor Pannier imparis adult heart function in Drosophila. Hum Mol Genet 19 3153 3163
42. Torres-VazquezJParkSWarriorRAroraK 2001 The transcription factor Schnurri plays a dual role in mediating Dpp signaling during embryogenesis. Development 128 1657 1670
43. Campos-OrtegaJAHartensteinV 1985 The embryonic development of Drosophila melanogaster Berlin Springer-Verlag
44. EllisMCO'NeillEMRubinGM 1993 Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 119 855 865
45. BaroloSCastroBPosakonyJW 2004 New Drosophila transgenic reporters: insulated P-element vectors expressing fast-maturing RFP. Biotechniques 36 436 440, 442
46. LiuHMaCMosesK 1996 Identification and functional characterization of conserved promoter elements from glass: a retinal development gene of Drosophila. Mech Dev 56 73 82
47. DolezalTDolezelovaEZurovecMBryantPJ 2005 A role for adenosine deaminase in Drosophila larval development. PLoS Biol 3 e201 doi:10.1371/journal.pbio.0030201
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