Skip to main content
SpringerLink
Log in

The Five Faces of Notch Signalling During Drosophila melanogaster Embryonic CNS Development

  • Chapter
  • First Online:
Book cover Notch Signaling in Embryology and Cancer

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1218))

Abstract

During central nervous system (CNS) development, a complex series of events play out, starting with the establishment of neural progenitor cells, followed by their asymmetric division and formation of lineages and the differentiation of neurons and glia. Studies in the Drosophila melanogaster embryonic CNS have revealed that the Notch signal transduction pathway plays at least five different and distinct roles during these events. Herein, we review these many faces of Notch signalling and discuss the mechanisms that ensure context-dependent and compartment-dependent signalling. We conclude by discussing some outstanding issues regarding Notch signalling in this system, which likely have bearing on Notch signalling in many species.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Acar M, Jafar-Nejad H, Takeuchi H, Rajan A, Ibrani D, Rana NA, Pan H, Haltiwanger RS, Bellen HJ (2008) Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132:247–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allan DW, Thor S (2015) Transcriptional selectors, masters, and combinatorial codes: regulatory principles of neural subtype specification. Wiley Interdiscip Rev Dev Biol 4:505–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Artavanis-Tsakonas S, Muskavitch MA, Yedvobnick B (1983) Molecular cloning of Notch, a locus affecting neurogenesis in Drosophila melanogaster. Proc Natl Acad Sci U S A 80:1977–1981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babaoglan AB, O’Connor-Giles KM, Mistry H, Schickedanz A, Wilson BA, Skeath JB (2009) Sanpodo: a context-dependent activator and inhibitor of Notch signaling during asymmetric divisions. Development 136:4089–4098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachmann A, Knust E (1998) Dissection of cis-regulatory elements of the Drosophila gene Serrate. Dev Genes Evol 208:346–351

    Article  CAS  PubMed  Google Scholar 

  • Bahrampour S, Thor S (2016) Ctr9, a key component of the Paf1 complex, affects proliferation and terminal differentiation in the developing Drosophila nervous system. G3 (Bethesda) 6:3229–3239

    Article  CAS  PubMed Central  Google Scholar 

  • Bailey AM, Posakony JW (1995) Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9:2609–2622

    Article  CAS  PubMed  Google Scholar 

  • Baumgardt M, Karlsson D, Terriente J, Diaz-Benjumea FJ, Thor S (2009) Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell 139:969–982

    Article  CAS  PubMed  Google Scholar 

  • Baumgardt M, Karlsson D, Salmani BY, Bivik C, Macdonald RB, Gunnar E, Thor S (2014) Global programmed switch in neural daughter cell proliferation mode triggered by a temporal gene cascade. Dev Cell 30:192–208

    Article  CAS  PubMed  Google Scholar 

  • Bender LB, Kooh PJ, Muskavitch MA (1993) Complex function and expression of Delta during Drosophila oogenesis. Genetics 133:967–978

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhat KM (1999) Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. Bioessays 21:472–485

    Article  CAS  PubMed  Google Scholar 

  • Bhat KM, Gaziova I, Katipalla S (2011) Neuralized mediates asymmetric division of neural precursors by two distinct and sequential events: promoting asymmetric localization of Numb and enhancing activation of Notch-signaling. Dev Biol 351:186–198

    Article  CAS  PubMed  Google Scholar 

  • Birkholz O, Rickert C, Berger C, Urbach R, Technau GM (2013) Neuroblast pattern and identity in the Drosophila tail region and role of double sex in the survival of sex-specific precursors. Development 140:1830–1842

    Article  CAS  PubMed  Google Scholar 

  • Bivik Stadler C, Arefin B, Ekman H, Thor S (2019) PIP degron-stabilized Dacapo/p21(Cip1) and mutations in ago act in an anti- versus pro-proliferative manner, yet both trigger an increase in Cyclin E levels. Development 146(13):dev175927

    Article  PubMed  CAS  Google Scholar 

  • Bivik C, Macdonald RB, Gunnar E, Mazouni K, Schweisguth F, Thor S (2016) Control of neural daughter cell proliferation by multi-level Notch/Su(H)/E(spl)-HLH signaling. PLoS Genet 12:e1005984

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boone JQ, Doe CQ (2008) Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev Neurobiol 68:1185–1195

    Article  PubMed  PubMed Central  Google Scholar 

  • Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678–689

    Article  CAS  PubMed  Google Scholar 

  • Cau E, Blader P (2009) Notch activity in the nervous system: to switch or not switch? Neural Dev 4:36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choksi SP, Southall TD, Bossing T, Edoff K, de Wit E, Fischer BE, van Steensel B, Micklem G, Brand AH (2006) Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell 11:775–789

    Article  CAS  PubMed  Google Scholar 

  • Cohen SM, Jurgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482–485

    Article  CAS  PubMed  Google Scholar 

  • Crowner D, Le Gall M, Gates MA, Giniger E (2003) Notch steers Drosophila ISNb motor axons by regulating the Abl signaling pathway. Curr Biol 13:967–972

    Article  CAS  PubMed  Google Scholar 

  • Deblandre GA, Lai EC, Kintner C (2001) Xenopus neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev Cell 1:795–806

    Article  CAS  PubMed  Google Scholar 

  • Delidakis C, Preiss A, Hartley DA, Artavanistsakonas S (1991) 2 genetically and molecularly distinct functions involved in early neurogenesis reside within the enhancer of split locus of Drosophila-melanogaster. Genetics 129:803–823

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doe CQ (1996) Asymmetric cell division and neurogenesis. Curr Opin Genet Dev 6:562–566

    Article  CAS  PubMed  Google Scholar 

  • Doe CQ, Bowerman B (2001) Asymmetric cell division: fly neuroblast meets worm zygote. Curr Opin Cell Biol 13:68–75

    Article  CAS  PubMed  Google Scholar 

  • Doe CQ, Technau GM (1993) Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci 16:510–514

    Article  CAS  PubMed  Google Scholar 

  • Fleming RJ, Scottgale TN, Diederich RJ, Artavanis-Tsakonas S (1990) The gene Serrate encodes a putative EGF-like transmembrane protein essential for proper ectodermal development in Drosophila melanogaster. Genes Dev 4:2188–2201

    Article  CAS  PubMed  Google Scholar 

  • Fortini ME (2009) Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 16:633–647

    Article  CAS  PubMed  Google Scholar 

  • Fortini ME, Artavanis-Tsakonas S (1994) The suppressor of hairless protein participates in notch receptor signaling. Cell 79:273–282

    Article  CAS  PubMed  Google Scholar 

  • Fuerstenberg S, Broadus J, Doe CQ (1998) Asymmetry and cell fate in the Drosophila embryonic CNS. Int J Dev Biol 42:379–383

    CAS  PubMed  Google Scholar 

  • Garces A, Thor S (2006) Specification of Drosophila aCC motoneuron identity by a genetic cascade involving even-skipped, grain and zfh1. Development 133:1445–1455

    Article  CAS  PubMed  Google Scholar 

  • Giniger E (1998) A role for Abl in Notch signaling. Neuron 20:667–681

    Article  CAS  PubMed  Google Scholar 

  • Giniger E (2012) Notch signaling and neural connectivity. Curr Opin Genet Dev 22:339–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giniger E, Jan LY, Jan YN (1993) Specifying the path of the intersegmental nerve of the Drosophila embryo: a role for Delta and Notch. Development 117:431–440

    CAS  PubMed  Google Scholar 

  • Griffiths RL, Hidalgo A (2004) Prospero maintains the mitotic potential of glial precursors enabling them to respond to neurons. EMBO J 23:2440–2450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffiths RC, Benito-Sipos J, Fenton JC, Torroja L, Hidalgo A (2007) Two distinct mechanisms segregate Prospero in the longitudinal glia underlying the timing of interactions with axons. Neuron Glia Biol 3:75–88

    Article  PubMed  PubMed Central  Google Scholar 

  • Gunnar E, Bivik C, Starkenberg A, Thor S (2016) sequoia controls the type I>0 daughter proliferation switch in the developing Drosophila nervous system. Development 143:3774–3784

    Article  CAS  PubMed  Google Scholar 

  • Handford PA, Korona B, Suckling R, Redfield C, Lea SM (2018) Structural insights into Notch receptor-ligand interactions. Adv Exp Med Biol 1066:33–46

    Article  CAS  PubMed  Google Scholar 

  • Hirata J, Nakagoshi H, Nabeshima Y, Matsuzaki F (1995) Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377:627–630

    Article  CAS  PubMed  Google Scholar 

  • Hirth F, Reichert H (1999) Conserved genetic programs in insect and mammalian brain development. Bioessays 21:677–684

    Article  CAS  PubMed  Google Scholar 

  • Jennings B, Preiss A, Delidakis C, Bray S (1994) The Notch signalling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo. Development 120:3537–3548

    CAS  PubMed  Google Scholar 

  • Johansen KM, Fehon RG, Artavanis-Tsakonas S (1989) The notch gene product is a glycoprotein expressed on the cell surface of both epidermal and neuronal precursor cells during Drosophila development. J Cell Biol 109:2427–2440

    Article  CAS  PubMed  Google Scholar 

  • Kannan R, Song JK, Karpova T, Clarke A, Shivalkar M, Wang B, Kotlyanskaya L, Kuzina I, Gu Q, Giniger E (2017) The Abl pathway bifurcates to balance Enabled and Rac signaling in axon patterning in Drosophila. Development 144:487–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kannan R, Cox E, Wang L, Kuzina I, Gu Q, Giniger E (2018) Tyrosine phosphorylation and proteolytic cleavage of Notch are required for non-canonical Notch/Abl signaling in Drosophila axon guidance. Development 145(2):dev151548

    PubMed  PubMed Central  Google Scholar 

  • Kidd S, Baylies MK, Gasic GP, Young MW (1989) Structure and distribution of the Notch protein in developing Drosophila. Genes Dev 3:1113–1129

    Article  CAS  PubMed  Google Scholar 

  • Klambt C, Knust E, Tietze K, Campos-Ortega JA (1989) Closely related transcripts encoded by the neurogenic gene complex Enhancer of split of Drosophila melanogaster. EMBO J 8:203–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knoblich JA, Jan LY, Jan YN (1995) Asymmetric segregation of Numb and Prospero during cell division. Nature 377:624–627

    Article  CAS  PubMed  Google Scholar 

  • Knust E, Schrons H, Grawe F, Campos-Ortega JA (1992) Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics 132:505–518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kopczynski CC, Muskavitch MA (1989) Complex spatio-temporal accumulation of alternative transcripts from the neurogenic gene Delta during Drosophila embryogenesis. Development 107:623–636

    CAS  PubMed  Google Scholar 

  • Kuzina I, Song JK, Giniger E (2011) How Notch establishes longitudinal axon connections between successive segments of the Drosophila CNS. Development 138:1839–1849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai EC (2002) Protein degradation: four E3s for the notch pathway. Curr Biol 12:R74–R78

    Article  CAS  PubMed  Google Scholar 

  • Lai EC, Deblandre GA, Kintner C, Rubin GM (2001) Drosophila neuralized is a ubiquitin ligase that promotes the internalization and degradation of delta. Dev Cell 1:783–794

    Article  CAS  PubMed  Google Scholar 

  • Landgraf M, Thor S (2006) Development of Drosophila motoneurons: specification and morphology. Semin Cell Dev Biol 17:3–11

    Article  CAS  PubMed  Google Scholar 

  • Landgraf M, Bossing T, Technau GM, Bate M (1997) The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J Neurosci 17:9642–9655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrence PA, Sanson B, Vincent JP (1996) Compartments, wingless and engrailed: patterning the ventral epidermis of Drosophila embryos. Development 122:4095–4103

    CAS  PubMed  Google Scholar 

  • Le Gall M, de Mattei C, Giniger E (2008) Molecular separation of two signaling pathways for the receptor, Notch. Dev Biol 313:556–567

    Article  CAS  PubMed  Google Scholar 

  • Lecourtois M, Schweisguth F (1995) The neurogenic suppressor of hairless DNA-binding protein mediates the transcriptional activation of the enhancer of split complex genes triggered by Notch signaling. Genes Dev 9:2598–2608

    Article  CAS  PubMed  Google Scholar 

  • Li L, Vaessin H (2000) Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis. Genes Dev 14:147–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lieber T, Kidd S, Young MW (2002) kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev 16:209–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lundell MJ, Lee HK, Perez E, Chadwell L (2003) The regulation of apoptosis by Numb/Notch signaling in the serotonin lineage of Drosophila. Development 130:4109–4121

    Article  CAS  PubMed  Google Scholar 

  • Miguel-Aliaga I, Thor S (2004) Segment-specific prevention of pioneer neuron apoptosis by cell-autonomous, postmitotic Hox gene activity. Development 131:6093–6105

    Article  CAS  PubMed  Google Scholar 

  • Miguel-Aliaga I, Thor S (2009) Programmed cell death in the nervous system–a programmed cell fate? Curr Opin Neurobiol 19:127–133

    Article  CAS  PubMed  Google Scholar 

  • Miller AC, Lyons EL, Herman TG (2009) cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr Biol 19:1378–1383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moloney DJ, Panin VM, Johnston SH, Chen J, Shao L, Wilson R, Wang Y, Stanley P, Irvine KD, Haltiwanger RS, Vogt TF (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406:369–375

    Article  CAS  PubMed  Google Scholar 

  • Monastirioti M, Giagtzoglou N, Koumbanakis KA, Zacharioudaki E, Deligiannaki M, Wech I, Almeida M, Preiss A, Bray S, Delidakis C (2010) Drosophila Hey is a target of Notch in asymmetric divisions during embryonic and larval neurogenesis. Development 137:191–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakao K, Campos-Ortega JA (1996) Persistent expression of genes of the enhancer of split complex suppresses neural development in Drosophila. Neuron 16:275–286

    Article  CAS  PubMed  Google Scholar 

  • Nam Y, Sliz P, Song L, Aster JC, Blacklow SC (2006) Structural basis for cooperativity in recruitment of MAML coactivators to Notch transcription complexes. Cell 124:973–983

    Article  CAS  PubMed  Google Scholar 

  • Newsome TP, Schmidt S, Dietzl G, Keleman K, Asling B, Debant A, Dickson BJ (2000) Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101:283–294

    Article  CAS  PubMed  Google Scholar 

  • Nicholson SC, Nicolay BN, Frolov MV, Moberg KH (2011) Notch-dependent expression of the archipelago ubiquitin ligase subunit in the Drosophila eye. Development 138:251–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Connor-Giles KM, Skeath JB (2003) Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev Cell 5:231–243

    Article  PubMed  Google Scholar 

  • Oellers N, Dehio M, Knust E (1994) bHLH proteins encoded by the Enhancer of split complex of Drosophila negatively interfere with transcriptional activation mediated by proneural genes. Mol Gen Genet 244:465–473

    Article  CAS  PubMed  Google Scholar 

  • Okajima T, Xu A, Irvine KD (2003) Modulation of notch-ligand binding by protein O-fucosyltransferase 1 and fringe. J Biol Chem 278:42340–42345

    Article  CAS  PubMed  Google Scholar 

  • Pan D, Rubin GM (1997) Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90:271–280

    Article  CAS  PubMed  Google Scholar 

  • Panin VM, Papayannopoulos V, Wilson R, Irvine KD (1997) Fringe modulates Notch-ligand interactions. Nature 387:908–912

    Article  CAS  PubMed  Google Scholar 

  • Pavlopoulos E, Pitsouli C, Klueg KM, Muskavitch MA, Moschonas NK, Delidakis C (2001) neuralized Encodes a peripheral membrane protein involved in delta signaling and endocytosis. Dev Cell 1:807–816

    Article  CAS  PubMed  Google Scholar 

  • Petcherski AG, Kimble J (2000) Mastermind is a putative activator for Notch. Curr Biol 10:R471–R473

    Article  CAS  PubMed  Google Scholar 

  • Pitsouli C, Delidakis C (2005) The interplay between DSL proteins and ubiquitin ligases in Notch signaling. Development 132:4041–4050

    Article  CAS  PubMed  Google Scholar 

  • Poulson DF (1937) Chromosomal deficiencies and the embryonic development of Drosophila Melanogaster. Proc Natl Acad Sci U S A 23:133–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi H, Rand MD, Wu X, Sestan N, Wang W, Rakic P, Xu T, Artavanis-Tsakonas S (1999) Processing of the notch ligand delta by the metalloprotease Kuzbanian. Science 283:91–94

    Article  CAS  PubMed  Google Scholar 

  • Rogulja-Ortmann A, Luer K, Seibert J, Rickert C, Technau GM (2007) Programmed cell death in the embryonic central nervous system of Drosophila melanogaster. Development 134:105–116

    Article  CAS  PubMed  Google Scholar 

  • Schmid A, Chiba A, Doe CQ (1999) Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653–4689

    CAS  PubMed  Google Scholar 

  • Schweisguth F, Posakony JW (1994) Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development 120:1433–1441

    CAS  PubMed  Google Scholar 

  • Simoes S, Oh Y, Wang MFZ, Fernandez-Gonzalez R, Tepass U (2017) Myosin II promotes the anisotropic loss of the apical domain during Drosophila neuroblast ingression. J Cell Biol 216:1387–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skeath JB (1999) At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. Bioessays 21:922–931

    Article  CAS  PubMed  Google Scholar 

  • Skeath JB, Doe CQ (1998) Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development 125:1857–1865

    CAS  PubMed  Google Scholar 

  • Skeath JB, Thor S (2003) Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol 13:8–15

    Article  CAS  PubMed  Google Scholar 

  • Song JK, Giniger E (2011) Noncanonical Notch function in motor axon guidance is mediated by Rac GTPase and the GEF1 domain of Trio. Dev Dyn 240:324–332

    Article  PubMed  PubMed Central  Google Scholar 

  • Spana EP, Doe CQ (1995) The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121:3187–3195

    CAS  PubMed  Google Scholar 

  • Spana EP, Doe CQ (1996) Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17:21–26

    Article  CAS  PubMed  Google Scholar 

  • Stacey SM, Muraro NI, Peco E, Labbe A, Thomas GB, Baines RA, van Meyel DJ (2010) Drosophila glial glutamate transporter Eaat1 is regulated by fringe-mediated notch signaling and is essential for larval locomotion. J Neurosci 30:14446–14457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas GB, van Meyel DJ (2007) The glycosyltransferase Fringe promotes Delta-Notch signaling between neurons and glia, and is required for subtype-specific glial gene expression. Development 134:591–600

    Article  CAS  PubMed  Google Scholar 

  • Thomas U, Speicher SA, Knust E (1991) The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs. Development 111:749–761

    CAS  PubMed  Google Scholar 

  • Thor S (1995) The genetics of brain-development – conserved programs in flies and mice. Neuron 15:975–977

    Article  CAS  PubMed  Google Scholar 

  • Thor S, Thomas J (2002) Motor neuron specification in worms, flies and mice: conserved and ‘lost’ mechanisms. Curr Opin Genet Dev 12:558–564

    Article  CAS  PubMed  Google Scholar 

  • Ulvklo C, Macdonald R, Bivik C, Baumgardt M, Karlsson D, Thor S (2012) Control of neuronal cell fate and number by integration of distinct daughter cell proliferation modes with temporal progression. Development 139:678–689

    Article  CAS  PubMed  Google Scholar 

  • Urbach R, Schnabel R, Technau GM (2003) The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130:3589–3606

    Article  CAS  PubMed  Google Scholar 

  • Urbach R, Jussen D, Technau GM (2016) Gene expression profiles uncover individual identities of gnathal neuroblasts and serial homologies in the embryonic CNS of Drosophila. Development 143:1290–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varshney S, Stanley P (2018) Multiple roles for O-glycans in Notch signalling. FEBS Lett 592:3819–3834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vassin H, Bremer KA, Knust E, Campos-Ortega JA (1987) The neurogenic gene Delta of Drosophila melanogaster is expressed in neurogenic territories and encodes a putative transmembrane protein with EGF-like repeats. EMBO J 6:3431–3440

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Shao L, Shi S, Harris RJ, Spellman MW, Stanley P, Haltiwanger RS (2001) Modification of epidermal growth factor-like repeats with O-fucose. Molecular cloning and expression of a novel GDP-fucose protein O-fucosyltransferase. J Biol Chem 276:40338–40345

    Article  CAS  PubMed  Google Scholar 

  • Wharton KA, Johansen KM, Xu T, Artavanis-Tsakonas S (1985) Nucleotide sequence from the neurogenic locus Notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 43:567–581

    Article  CAS  PubMed  Google Scholar 

  • Wheeler SR, Stagg SB, Crews ST (2009) MidExDB: a database of Drosophila CNS midline cell gene expression. BMC Dev Biol 9:56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilson JJ, Kovall RA (2006) Crystal structure of the CSL-Notch-Mastermind ternary complex bound to DNA. Cell 124:985–996

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, Griffin JD (2000) MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet 26:484–489

    Article  CAS  PubMed  Google Scholar 

  • Yeh CH, Bellon M, Nicot C (2018) FBXW7: a critical tumor suppressor of human cancers. Mol Cancer 17:115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zweifel ME, Leahy DJ, Hughson FM, Barrick D (2003) Structure and stability of the ankyrin domain of the Drosophila Notch receptor. Protein Sci 12:2622–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author Contributions

SB and ST generated the figures and wrote the manuscript.

Competing Interests

No competing interests declared.

Funding

Funding was provided by the Swedish Research Council (2018-00694) to SB and by support from the University of Queensland to ST.

Author information

Authors and Affiliations

  1. The Hospital for Sick Children, Peter Gilgan Center for Research and Learning, Toronto, ON, Canada

    Shahrzad Bahrampour

  2. Karolinska Institutet, Department of Cell and Molecular Biology (CMB), Stockholm, Sweden

    Shahrzad Bahrampour

  3. School of Biomedical Sciences, University of Queensland, St Lucia, QLD, Australia

    Stefan Thor

Authors
  1. Shahrzad Bahrampour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Thor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shahrzad Bahrampour or Stefan Thor .

Editor information

Editors and Affiliations

  1. Department of Dermatology, The Saarland University Hospital, Homburg, Saarland, Germany

    Jörg Reichrath

  2. Department of Dermatology, The Saarland University Hospital, Homburg, Saarland, Germany

    Sandra Reichrath

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bahrampour, S., Thor, S. (2020). The Five Faces of Notch Signalling During Drosophila melanogaster Embryonic CNS Development. In: Reichrath, J., Reichrath, S. (eds) Notch Signaling in Embryology and Cancer. Advances in Experimental Medicine and Biology, vol 1218. Springer, Cham. https://doi.org/10.1007/978-3-030-34436-8_3

Download citation

Publish with us

Policies and ethics

Search

Navigation