Abstract
Notch pathway plays diverse and fundamental roles during animal development. One of the most relevant, which arises directly from its unique mode of activation, is the specification of cell fates and tissue boundaries. The development of the leg of Drosophila melanogaster is a fine example of this Notch function, as it is required to specify the fate of the cells that will eventually form the leg joints, the flexible structures that separate the different segments of the adult leg. Notch activity is accurately activated and maintained at the distal end of each segment in response to the proximo-distal patterning gene network of the developing leg. Region-specific downstream targets of Notch in turn regulate the formation of the different types of joints. We discuss recent findings that shed light on the molecular and cellular mechanisms that are ultimately governed by Notch to achieve epithelial fold and joint morphogenesis. Finally, we briefly summarize the role that Notch plays in inducing the nonautonomous growth of the leg. Overall, this book chapter aims to highlight leg development as a useful model to study how patterning information is translated into specific cell behaviors that shape the final form of an adult organ.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abu-Shaar M, Mann RS (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125:3821–3830
Affolter M, Pyrowolakis G, Weiss A, Basler K (2008) Signal-induced repression: the exception or the rule in developmental signaling? Dev Cell 15:11–22. https://doi.org/10.1016/j.devcel.2008.06.006
Ahn Y, Zou J, Mitchell PJ (2011) Segment-specific regulation of the Drosophila AP-2 gene during leg and antennal development. Dev Biol 355:336–348. https://doi.org/10.1016/j.ydbio.2011.04.032
Aldaz S, Escudero LM, Freeman M (2010) Live imaging of Drosophila imaginal disc development. Proc Natl Acad Sci U S A 107:14217–14222. https://doi.org/10.1073/pnas.1008623107
Ambrosini A, Rayer M, Monier B, Suzanne M (2019) Mechanical function of the nucleus in force generation during epithelial morphogenesis. Dev Cell 50:197. https://doi.org/10.1016/j.devcel.2019.05.027
An Y et al (2017) Apical constriction is driven by a pulsatile apical myosin network in delaminating Drosophila neuroblasts. Development 144:2153–2164. https://doi.org/10.1242/dev.150763
Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138:3593–3612. https://doi.org/10.1242/dev.063610
Angelini DR, Smith FW, Jockusch EL (2012) Extent with modification: leg patterning in the beetle tribolium castaneum and the evolution of serial homologs. G3 (Bethesda) 2:235–248. https://doi.org/10.1534/g3.111.001537
Awasaki T, Kimura K (2001) Multiple function of poxn gene in larval PNS development and in adult appendage formation of Drosophila. Dev Genes Evol 211:20–29
Axelrod JD, Matsuno K, Artavanis-Tsakonas S, Perrimon N (1996) Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science 271:1826–1832. https://doi.org/10.1126/science.271.5257.1826
Baanannou A et al (2013) Drosophila distal-less and Rotund bind a single enhancer ensuring reliable and robust bric-a-brac2 expression in distinct limb morphogenetic fields. PLoS Genet 9:e1003581. https://doi.org/10.1371/journal.pgen.1003581
Bando T et al (2009) Regulation of leg size and shape by the Dachsous/Fat signalling pathway during regeneration. Development 136:2235–2245. https://doi.org/10.1242/dev.035204
Barolo S, Stone T, Bang AG, Posakony JW (2002) Default repression and Notch signaling: hairless acts as an adaptor to recruit the corepressors Groucho and dCtBP to Suppressor of Hairless. Genes Dev 16:1964–1976. https://doi.org/10.1101/gad.987402
Bate M, Arias AM (1991) The embryonic origin of imaginal discs in Drosophila. Development 112:755–761
Bausek N, Zeidler MP (2014) Galpha73B is a downstream effector of JAK/STAT signalling and a regulator of Rho1 in Drosophila haematopoiesis. J Cell Sci 127:101–110. https://doi.org/10.1242/jcs.132852
Beira JV, Paro R (2016) The legacy of Drosophila imaginal discs. Chromosoma 125:573–592. https://doi.org/10.1007/s00412-016-0595-4
Bigas A, Espinosa L (2018) The multiple usages of Notch signaling in development, cell differentiation and cancer. Curr Opin Cell Biol 55:1–7. https://doi.org/10.1016/j.ceb.2018.06.010
Bishop SA, Klein T, Arias AM, Couso JP (1999) Composite signalling from Serrate and Delta establishes leg segments in Drosophila through Notch. Development 126:2993–3003
Boettner B, Van Aelst L (2002) The role of Rho GTPases in disease development. Gene 286:155–174
Bray S (1998) Notch signalling in Drosophila: three ways to use a pathway. Semin Cell Dev Biol 9:591–597. https://doi.org/10.1006/scdb.1998.0262
Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678–689. https://doi.org/10.1038/nrm2009
Bray S, Bernard F (2010) Chapter eight – Notch targets and their regulation, Elsevier Inc. Curr Top Dev Biol. 92:253–275. https://doi.org/10.1016/S0070-2153(10)92008-5
Bray S, Furriols M (2001) Notch pathway: making sense of suppressor of hairless. Curr Biol 11:R217–R221
Buckles GR, Rauskolb C, Villano JL, Katz FN (2001) Four-jointed interacts with dachs, abelson and enabled and feeds back onto the Notch pathway to affect growth and segmentation in the Drosophila leg. Development 128:3533–3542
Campbell G (2002) Distalization of the Drosophila leg by graded EGF-receptor activity. Nature 418:781–785
Campbell G, Weaver T, Tomlinson A (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74:1113–1123
Capilla A et al (2012) Planar cell polarity controls directional Notch signaling in the Drosophila leg. Development 139:2584–2593. https://doi.org/10.1242/dev.077446
Casares F, Mann RS (2001) The ground state of the ventral appendage in Drosophila. Science 293:1477–1480. https://doi.org/10.1126/science.1062542
Chu J, Dong PD, Panganiban G (2002) Limb type-specific regulation of bric a brac contributes to morphological diversity. Development 129:695–704
Ciechanska E, Dansereau DA, Svendsen PC, Heslip TR, Brook WJ (2007) dAP-2 and defective proventriculus regulate Serrate and Delta expression in the tarsus of Drosophila melanogaster. Genome 50:693–705. https://doi.org/10.1139/g07-043
Cifuentes FJ, Garcia-Bellido A (1997) Proximo-distal specification in the wing disc of Drosophila by the nubbin gene. Proc Natl Acad Sci U S A 94:11405–11410. https://doi.org/10.1073/pnas.94.21.11405
Citi S, Guerrera D, Spadaro D, Shah J (2014) Epithelial junctions and Rho family GTPases: the zonular signalosome. Small GTPases 5:1–15. https://doi.org/10.4161/21541248.2014.973760
Clark HF et al (1995) Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev 9:1530–1542. https://doi.org/10.1101/gad.9.12.1530
Cohen B, Simcox AA, Cohen SM (1993) Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117:597–608
Cordoba S, Estella C (2014) The bHLH-PAS transcription factor dysfusion regulates tarsal joint formation in response to Notch activity during drosophila leg development. PLoS Genet 10:e1004621. https://doi.org/10.1371/journal.pgen.1004621
Cordoba S, Estella C (2018) The transcription factor Dysfusion promotes fold and joint morphogenesis through regulation of Rho1. PLoS Genet 14:e1007584. https://doi.org/10.1371/journal.pgen.1007584
Cordoba S, Requena D, Jory A, Saiz A, Estella C (2016) The evolutionarily conserved transcription factor Sp1 controls appendage growth through Notch signaling. Development 143:3623–3631. https://doi.org/10.1242/dev.138735
Dahmann C, Oates AC, Brand M (2011) Boundary formation and maintenance in tissue development. Nat Rev Genet 12:43–55. https://doi.org/10.1038/nrg2902
Dawes-Hoang RE et al (2005) folded gastrulation, cell shape change and the control of myosin localization. Development 132:4165–4178. https://doi.org/10.1242/dev.01938
de Celis Ibeas JM, Bray SJ (2003) Bowl is required downstream of Notch for elaboration of distal limb patterning. Development 130:5943–5952. https://doi.org/10.1242/dev.00833
de Celis JF, Tyler DM, de Celis J, Bray SJ (1998) Notch signalling mediates segmentation of the Drosophila leg. Development 125:4617–4626
de Madrid BH, Greenberg L, Hatini V (2015) RhoGAP68F controls transport of adhesion proteins in Rab4 endosomes to modulate epithelial morphogenesis of Drosophila leg discs. Dev Biol 399:283–295. https://doi.org/10.1016/j.ydbio.2015.01.004
del Valle Rodriguez A, Didiano D, Desplan C (2012) Power tools for gene expression and clonal analysis in Drosophila. Nature methods 9:47–55. https://doi.org/10.1038/nmeth.1800
Devenport D (2014) The cell biology of planar cell polarity. J Cell Biol 207:171–179. https://doi.org/10.1083/jcb.201408039
Dexter JS (1914) The analysis of a case of continuous variation in Drosophila by a study of its linkage relations. Am Nat 48:712–758. https://doi.org/10.1086/279446
Diaz-Benjumea FJ, Cohen B, Cohen SM (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372:175–179. https://doi.org/10.1038/372175a0
Duncan DM, Burgess EA, Duncan I (1998) Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev 12:1290–1303
Estella C, Mann RS (2008) Logic of Wg and Dpp induction of distal and medial fates in the Drosophila leg. Development 135:627–636. https://doi.org/10.1242/dev.014670
Estella C, McKay DJ, Mann RS (2008) Molecular integration of wingless, decapentaplegic, and autoregulatory inputs into Distalless during Drosophila leg development. Dev Cell 14:86–96. https://doi.org/10.1016/j.devcel.2007.11.002
Estella C, Voutev R, Mann RS (2012) A dynamic network of morphogens and transcription factors patterns the fly leg. Curr Top Dev Biol 98:173–198. https://doi.org/10.1016/B978-0-12-386499-4.00007-0
Fox DT, Peifer M (2007) Abelson kinase (Abl) and RhoGEF2 regulate actin organization during cell constriction in Drosophila. Development 134:567–578. https://doi.org/10.1242/dev.02748
Fristrom D, Fristrom JW (1993) The metamorphic development of the adult epidermis. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Plainview, NY. vol II, pp 843–897
Galindo MI, Bishop SA, Greig S, Couso JP (2002) Leg patterning driven by proximal-distal interactions and EGFR signaling. Science 297:256–259. https://doi.org/10.1126/science.1072311
Galindo MI, Bishop SA, Couso JP (2005) Dynamic EGFR-Ras signalling in Drosophila leg development. Dev Dyn 233:1496–1508. https://doi.org/10.1002/dvdy.20452
Gilmour D, Rembold M, Leptin M (2017) From morphogen to morphogenesis and back. Nature 541:311–320. https://doi.org/10.1038/nature21348
Giorgianni MW, Mann RS (2011) Establishment of medial fates along the proximodistal axis of the Drosophila leg through direct activation of dachshund by Distalless. Dev Cell 20:455–468. https://doi.org/10.1016/j.devcel.2011.03.017
Godt D, Couderc JL, Cramton SE, Laski FA (1993) Pattern formation in the limbs of Drosophila: bric a brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus. Development 119:799–812
González-Crespo S, Morata G (1996) Genetic evidence for the subdivision of the arthropod limb into coxopodite and telopodite. Development 122:3921–3928
Gonzalez-Crespo S et al (1998) Antagonism between extradenticle function and Hedgehog signalling in the developing limb. Nature 394:196–200. https://doi.org/10.1038/28197
Greenberg L, Hatini V (2009) Essential roles for lines in mediating leg and antennal proximodistal patterning and generating a stable Notch signaling interface at segment borders. Dev Biol 330:93–104. https://doi.org/10.1016/j.ydbio.2009.03.014
Greenberg L, Hatini V (2011) Systematic expression and loss-of-function analysis defines spatially restricted requirements for Drosophila RhoGEFs and RhoGAPs in leg morphogenesis. Mech Dev 128:5–17. https://doi.org/10.1016/j.mod.2010.09.001
Greenwald I (2012) Notch and the awesome power of genetics. Genetics 191:655–669. https://doi.org/10.1534/genetics.112.141812
Grimaldi D, Engel M (2005) Evolution of the insects. Cambridge University Press, New York
Guarner A et al (2014) The zinc finger homeodomain-2 gene of Drosophila controls Notch targets and regulates apoptosis in the tarsal segments. Dev Biol 385:350–365. https://doi.org/10.1016/j.ydbio.2013.10.011
Halder G, Johnson RL (2011) Hippo signaling: growth control and beyond. Development 138:9–22. https://doi.org/10.1242/dev.045500
Hao I, Green RB, Dunaevsky O, Lengyel JA, Rauskolb C (2003) The odd-skipped family of zinc finger genes promotes Drosophila leg segmentation. Dev Biol 263:282–295
Harvey BM, Haltiwanger RS (2018) Regulation of Notch function by O-glycosylation. Adv Exp Med Biol 1066:59–78. https://doi.org/10.1007/978-3-319-89512-3_4
Henrique D, Schweisguth F (2019) Mechanisms of Notch signaling: a simple logic deployed in time and space. Development 146(3):dev172148. https://doi.org/10.1242/dev.172148
Hernandez-Martinez R, Covarrubias L (2011) Interdigital cell death function and regulation: new insights on an old programmed cell death model. Dev Growth Differ 53:245–258. https://doi.org/10.1111/j.1440-169X.2010.01246.x
Homem CC, Peifer M (2008) Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis. Development 135:1005–1018. https://doi.org/10.1242/dev.016337
Hori K, Sen A, Artavanis-Tsakonas S (2013) Notch signaling at a glance. J Cell Sci 126:2135–2140. https://doi.org/10.1242/jcs.127308
Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269. https://doi.org/10.1146/annurev.cellbio.21.020604.150721
Johnston LA, Schubiger G (1996) Ectopic expression of wingless in imaginal discs interferes with decapentaplegic expression and alters cell determination. Development 122:3519–3529
Karess RE et al (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65:1177–1189
Kerber B, Monge I, Mueller M, Mitchell PJ, Cohen SM (2001) The AP-2 transcription factor is required for joint formation and cell survival in Drosophila leg. Development 128:1231–1238
Kojima T (2017) Developmental mechanism of the tarsus in insect legs. Curr Opin Insect Sci 19:36–42. https://doi.org/10.1016/j.cois.2016.11.002
Kolsch V, Seher T, Fernandez-Ballester GJ, Serrano L, Leptin M (2007) Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315:384–386. https://doi.org/10.1126/science.1134833
Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233. https://doi.org/10.1016/j.cell.2009.03.045
Kozu S et al (2006) Temporal regulation of late expression of Bar homeobox genes during Drosophila leg development by Spineless, a homolog of the mammalian dioxin receptor. Dev Biol 294:497–508. https://doi.org/10.1016/j.ydbio.2006.03.015
Kuhn S, Geyer M (2014) Formins as effector proteins of Rho GTPases. Small GTPases 5:e29513. https://doi.org/10.4161/sgtp.29513
Lai EC (2002) Keeping a good pathway down: transcriptional repression of Notch pathway target genes by CSL proteins. EMBO Rep 3:840–845. https://doi.org/10.1093/embo-reports/kvf170
Lecuit T, Cohen SM (1997) Proximal-distal axis formation in the Drosophila leg. Nature 388:139–145. https://doi.org/10.1038/40563
Leptin M, Grunewald B (1990) Cell shape changes during gastrulation in Drosophila. Development 110:73–84
Liu R, Linardopoulou EV, Osborn GE, Parkhurst SM (2010) Formins in development: orchestrating body plan origami. Biochim Biophys Acta 1803:207–225. https://doi.org/10.1016/j.bbamcr.2008.09.016
Lohmann I, McGinnis N, Bodmer M, McGinnis W (2002) The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110:457–466
Mack NA, Georgiou M (2014) The interdependence of the Rho GTPases and apicobasal cell polarity. Small GTPases 5:10. https://doi.org/10.4161/21541248.2014.973768
Manjon C, Sanchez-Herrero E, Suzanne M (2007) Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9:57–63. https://doi.org/10.1038/ncb1518
Mao Y et al (2006) Dachs: an unconventional myosin that functions downstream of Fat to regulate growth, affinity and gene expression in Drosophila. Development 133:2539–2551. https://doi.org/10.1242/dev.02427
Marston DJ et al (2016) MRCK-1 drives apical constriction in C. elegans by linking developmental patterning to force generation. Curr Biol 26:2079–2089. https://doi.org/10.1016/j.cub.2016.06.010
Martin AC, Goldstein B (2014) Apical constriction: themes and variations on a cellular mechanism driving morphogenesis. Development 141:1987–1998. https://doi.org/10.1242/dev.102228
Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495–499. https://doi.org/10.1038/nature07522
Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF (2010) Integration of contractile forces during tissue invagination. J Cell Biol 188:735–749. https://doi.org/10.1083/jcb.200910099
Mason FM, Tworoger M, Martin AC (2013) Apical domain polarization localizes actin-myosin activity to drive ratchet-like apical constriction. Nat Cell Biol 15:926–936. https://doi.org/10.1038/ncb2796
Mason FM, Xie S, Vasquez CG, Tworoger M, Martin AC (2016) RhoA GTPase inhibition organizes contraction during epithelial morphogenesis. J Cell Biol 214:603–617. https://doi.org/10.1083/jcb.201603077
McKay DJ, Estella C, Mann RS (2009) The origins of the Drosophila leg revealed by the cis-regulatory architecture of the Distalless gene. Development 136:61–71. https://doi.org/10.1242/dev.029975
Mirth C, Akam M (2002) Joint development in the Drosophila leg: cell movements and cell populations. Dev Biol 246:391–406. https://doi.org/10.1006/dbio.2002.0593
Monge I et al (2001) Drosophila transcription factor AP-2 in proboscis, leg and brain central complex development. Development 128:1239–1252
Monier B, Suzanne M (2015) The morphogenetic role of apoptosis. Curr Top Dev Biol 114:335–362. https://doi.org/10.1016/bs.ctdb.2015.07.027
Monier B et al (2015) Apico-basal forces exerted by apoptotic cells drive epithelium folding. Nature 518:245–248. https://doi.org/10.1038/nature14152
Morgan TH (1917) The theory of the gene. Am Nat 51:513–544. https://doi.org/10.1086/279629
Morimura S, Maves L, Chen Y, Hoffmann FM (1996) decapentaplegic overexpression affects Drosophila wing and leg imaginal disc development and wingless expression. Dev Biol 177:136–151. https://doi.org/10.1006/dbio.1996.0151
Mulinari S, Barmchi MP, Hacker U (2008) DRhoGEF2 and diaphanous regulate contractile force during segmental groove morphogenesis in the Drosophila embryo. Mol Biol Cell 19:1883–1892. https://doi.org/10.1091/mbc.E07-12-1230
Munoz-Descalzo S et al (2010) Wingless modulates the ligand independent traffic of Notch through Dishevelled. Fly (Austin) 4:182–193. https://doi.org/10.4161/fly.4.3.11998
Natori K, Tajiri R, Furukawa S, Kojima T (2012) Progressive tarsal patterning in the Drosophila by temporally dynamic regulation of transcription factor genes. Dev Biol 361:450–462. https://doi.org/10.1016/j.ydbio.2011.10.031
Neisch AL, Speck O, Stronach B, Fehon RG (2010) Rho1 regulates apoptosis via activation of the JNK signaling pathway at the plasma membrane. J Cell Biol 189:311–323. https://doi.org/10.1083/jcb.200912010
Neubueser D, Hipfner DR (2010) Overlapping roles of Drosophila Drak and Rok kinases in epithelial tissue morphogenesis. Mol Biol Cell 21:2869–2879. https://doi.org/10.1091/mbc.E10-04-0328
Newcomb S et al (2018) cis-regulatory architecture of a short-range EGFR organizing center in the Drosophila melanogaster leg. PLoS Genet 14:e1007568. https://doi.org/10.1371/journal.pgen.1007568
Ng M, Diaz-Benjumea FJ, Cohen SM (1995) Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development 121:589–599
Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801
Okajima T, Irvine KD (2002) Regulation of notch signaling by O-linked fucose. Cell 111:893–904. https://doi.org/10.1016/S0092-8674(02)01114-5
Panin VM, Papayannopoulos V, Wilson R, Irvine KD (1997) Fringe modulates Notch-ligand interactions. Nature 387:908–912. https://doi.org/10.1038/43191
Pastor-Pareja JC, Grawe F, Martin-Blanco E, Garcia-Bellido A (2004) Invasive cell behavior during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev Cell 7:387–399. https://doi.org/10.1016/j.devcel.2004.07.022
Penton AL, Leonard LD, Spinner NB (2012) Notch signaling in human development and disease. Semin Cell Dev Biol 23:450–457. https://doi.org/10.1016/j.semcdb.2012.01.010
Pueyo JI, Couso JP (2008) The 11-aminoacid long Tarsal-less peptides trigger a cell signal in Drosophila leg development. Dev Biol 324:192–201. https://doi.org/10.1016/j.ydbio.2008.08.025
Pueyo JI, Couso JP (2011) Tarsal-less peptides control Notch signalling through the Shavenbaby transcription factor. Dev Biol 355:183–193. https://doi.org/10.1016/j.ydbio.2011.03.033
Pueyo JI, Galindo MI, Bishop SA, Couso JP (2000) Proximal-distal leg development in Drosophila requires the apterous gene and the Lim1 homologue dlim1. Development 127:5391–5402
Rauskolb C (2001) The establishment of segmentation in the Drosophila leg. Development 128:4511–4521
Rauskolb C, Irvine KD (1999) Notch-mediated segmentation and growth control of the Drosophila leg. Dev Biol 210:339–350. https://doi.org/10.1006/dbio.1999.9273
Rauskolb C, Correia T, Irvine KD (1999) Fringe-dependent separation of dorsal and ventral cells in the Drosophila wing. Nature 401:476–480. https://doi.org/10.1038/46786
Reeves GT, Stathopoulos A (2009) Graded dorsal and differential gene regulation in the Drosophila embryo. Cold Spring Harb Perspect Biol 1:a000836. https://doi.org/10.1101/cshperspect.a000836
Riento K, Ridley AJ (2003) Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4:446–456. https://doi.org/10.1038/nrm1128
Robertson F, Pinal N, Fichelson P, Pichaud F (2012) Atonal and EGFR signalling orchestrate rok- and Drak-dependent adherens junction remodelling during ommatidia morphogenesis. Development 139:3432–3441. https://doi.org/10.1242/dev.080762
Roh-Johnson M et al (2012) Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 335:1232–1235. https://doi.org/10.1126/science.1217869
Rosenblatt J, Raff MC, Cramer LP (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11:1847–1857
Ruiz-Losada M, Blom-Dahl D, Cordoba S, Estella C (2018) Specification and patterning of drosophila appendages. J Dev Biol 6(3):17. https://doi.org/10.3390/jdb6030017
Sawyer JM et al (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341:5–19. https://doi.org/10.1016/j.ydbio.2009.09.009
Shirai T, Yorimitsu T, Kiritooshi N, Matsuzaki F, Nakagoshi H (2007) Notch signaling relieves the joint-suppressive activity of Defective proventriculus in the Drosophila leg. Dev Biol 312:147–156. https://doi.org/10.1016/j.ydbio.2007.09.003
Shubin N, Tabin C, Carroll S (1997) Fossils, genes and the evolution of animal limbs. Nature 388:639–648. https://doi.org/10.1038/41710
Simoes S et al (2006) Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133:4257–4267. https://doi.org/10.1242/dev.02588
Slattum G, McGee KM, Rosenblatt J (2009) P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J Cell Biol 186:693–702. https://doi.org/10.1083/jcb.200903079
Snodgrass RE (1935) Principles of insect morphology. McGraw Hill, New York, 667 pp
Soler C, Daczewska M, Da Ponte JP, Dastugue B, Jagla K (2004) Coordinated development of muscles and tendons of the Drosophila leg. Development 131:6041–6051. https://doi.org/10.1242/dev.01527
Struhl G, Basler K (1993) Organizing activity of wingless protein in Drosophila. Cell 72:527–540
Suzanne M (2016) Molecular and cellular mechanisms involved in leg joint morphogenesis. Semin Cell Dev Biol 55:131–138. https://doi.org/10.1016/j.semcdb.2016.01.032
Suzanne M, Steller H (2013) Shaping organisms with apoptosis. Cell Death Differ 20:669–675. https://doi.org/10.1038/cdd.2013.11
Suzanne M et al (2010) Coupling of apoptosis and L/R patterning controls stepwise organ looping. Curr Biol 20:1773–1778. https://doi.org/10.1016/j.cub.2010.08.056
Svendsen PC, Ryu JR, Brook WJ (2015) The expression of the T-box selector gene midline in the leg imaginal disc is controlled by both transcriptional regulation and cell lineage. Biol Open 4:1707–1714. https://doi.org/10.1242/bio.013565
Tajiri R, Misaki K, Yonemura S, Hayashi S (2010) Dynamic shape changes of ECM-producing cells drive morphogenesis of ball-and-socket joints in the fly leg. Development 137:2055–2063. https://doi.org/10.1242/dev.047175
Tajiri R, Misaki K, Yonemura S, Hayashi S (2011) Joint morphology in the insect leg: evolutionary history inferred from Notch loss-of-function phenotypes in Drosophila. Development 138:4621–4626. https://doi.org/10.1242/dev.067330
Tan JL, Ravid S, Spudich JA (1992) Control of nonmuscle myosins by phosphorylation. Annu Rev Biochem 61:721–759. https://doi.org/10.1146/annurev.bi.61.070192.003445
Theisen H, Haerry TE, O’Connor MB, Marsh JL (1996) Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122:3939–3948
Vasquez CG, Martin AC (2016) Force transmission in epithelial tissues. Dev Dyn 245:361–371. https://doi.org/10.1002/dvdy.24384
Vidal M, Larson DE, Cagan RL (2006) Csk-deficient boundary cells are eliminated from normal Drosophila epithelia by exclusion, migration, and apoptosis. Dev Cell 10:33–44. https://doi.org/10.1016/j.devcel.2005.11.007
Villano JL, Katz FN (1995) 4-jointed is required for intermediate growth in the proximal-distal Axis in Drosophila. Development 121:2767–2777
von Kalm L, Fristrom D, Fristrom J (1995) The making of a fly leg: a model for epithelial morphogenesis. BioEssays 17:693–702. https://doi.org/10.1002/bies.950170806
Weng M, Wieschaus E (2016) Myosin-dependent remodeling of adherens junctions protects junctions from Snail-dependent disassembly. J Cell Biol 212:219–229. https://doi.org/10.1083/jcb.201508056
Wilder EL, Perrimon N (1995) Dual functions of wingless in the Drosophila leg imaginal disc. Development 121:477–488
Winter CG et al (2001) Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105:81–91
Xu N, Keung B, Myat MM (2008) Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rho-kinase. Dev Biol 321:88–100. https://doi.org/10.1016/j.ydbio.2008.06.007
Yamaguchi Y et al (2011) Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure. J Cell Biol 195:1047–1060. https://doi.org/10.1083/jcb.201104057
Zegers MM, Friedl P (2014) Rho GTPases in collective cell migration. Small GTPases 5:e28997. https://doi.org/10.4161/sgtp.28997
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Córdoba, S., Estella, C. (2020). Role of Notch Signaling in Leg Development in Drosophila melanogaster. 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_7
Download citation
DOI: https://doi.org/10.1007/978-3-030-34436-8_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-34435-1
Online ISBN: 978-3-030-34436-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)