Skip to main content
SpringerLink
Log in

Coordination of Embryogenesis by the Centrosome in Drosophila melanogaster

  • Chapter
  • First Online:
The Golgi Apparatus and Centriole

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 67))

Abstract

The first 3 h of Drosophila melanogaster embryo development are exemplified by rapid nuclear divisions within a large syncytium, transforming the zygote to the cellular blastoderm after 13 successive cleavage divisions. As the syncytial embryo develops, it relies on centrosomes and cytoskeletal dynamics to transport nuclei, maintain uniform nuclear distribution throughout cleavage cycles, ensure generation of germ cells, and coordinate cellularization. For the sake of this review, we classify six early embryo stages that rely on processes coordinated by the centrosome and its regulation of the cytoskeleton. The first stage features migration of one of the female pronuclei toward the male pronucleus following maturation of the first embryonic centrosomes. Two subsequent stages distribute the nuclei first axially and then radially in the embryo. The remaining three stages involve centrosome-actin dynamics that control cortical plasma membrane morphogenesis. In this review, we highlight the dynamics of the centrosome and its role in controlling the six stages that culminate in the cellularization of the blastoderm embryo.

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 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
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

  • Acharya S, Laupsien P, Wenzl C, Yan S, Großhans J (2014) Function and dynamics of slam in furrow formation in early Drosophila embryo. Dev Biol 386(2):371–384

    Article  CAS  PubMed  Google Scholar 

  • Afshar K, Stuart B, Wasserman SA (2000) Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 127(9):1887–1897

    CAS  PubMed  Google Scholar 

  • Al-Hakim AK, Bashkurov M, Gingras AC, Durocher D, Pelletier L (2012) Interaction proteomics identify NEURL4 and the HECT E3 ligase HERC2 as novel modulators of centrosome architecture. Mol Cell Proteomics 11(6):M111.014233

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Archambault V, Pinson X (2010) Free centrosomes: where do they all come from? Fly 4(2):172–177

    Article  CAS  PubMed  Google Scholar 

  • Archambault V, Zhao X, White-Cooper H, Carpenter AT, Glover DM (2007) Mutations in Drosophila Greatwall/Scant reveal its roles in mitosis and meiosis and interdependence with polo kinase. PLoS Genet 3(11):e200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Archambault V, D’Avino PP, Deery MJ, Lilley KS, Glover DM (2008) Sequestration of polo kinase to microtubules by phosphopriming-independent binding to map 205 is relieved by phosphorylation at a CDK site in mitosis. Genes Dev 22(19):2707–2720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker J, Theurkauf WE, Schubiger G (1993) Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo. J Cell Biol 122(1):113–121

    Article  CAS  PubMed  Google Scholar 

  • Barros TP, Kinoshita K, Hyman AA, Raff JW (2005) Aurora a activates D-TACC-Msps complexes exclusively at centrosomes to stabilize centrosomal microtubules. J Cell Biol 170(7):1039–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belecz I, Gonzalez C, Puro J, Szabad J (2001) Dominant-negative mutant dynein allows spontaneous centrosome assembly, uncouples chromosome and centrosome cycles. Curr Biol 11(2):136–140

    Article  CAS  PubMed  Google Scholar 

  • Blachon S, Cai X, Roberts KA, Yang K, Polyanovsky A, Church A, Avidor-Reiss T (2009) A proximal centriole-like structure is present in Drosophila spermatids and can serve as a model to study centriole duplication. Genetics 182(1):133–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blachon S, Khire A, Avidor-Reiss T (2014) The origin of the second centriole in the zygote of Drosophila melanogaster. Genetics 197(1):199–205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bownes M (1982) Embryogenesis. A handbook of Drosophila. Elsevier, Amsterdam

    Google Scholar 

  • Brandt A, Papagiannouli F, Wagner N, Wilsch-Bräuninger M, Braun M, Furlong EE, Loserth S, Wenzl C, Pilot F, Vogt N, Lecuit T, Krohne G, Grosshans J (2006) Developmental control of nuclear size and shape by Kugelkern and Kurzkern. Curr Biol 16(6):543–552

    Article  CAS  PubMed  Google Scholar 

  • Brent AE, MacQueen A, Hazelrigg T (2000) The Drosophila wispy gene is required for RNA localization and other microtubule-based events of meiosis and early embryogenesis. Genetics 154(4):1649–1662

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brunk K, Vernay B, Griffith E, Reynolds NL, Strutt D, Ingham PW, Jackson AP (2007) Microcephalin coordinates mitosis in the syncytial Drosophila embryo. J Cell Sci 120. (Pt 20:3578–3588

    Article  CAS  PubMed  Google Scholar 

  • Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139(2):469–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buttrick GJ, Beaumont LM, Leitch J, Yau C, Hughes JR, Wakefield JG (2008) Akt regulates centrosome migration and spindle orientation in the early Drosophila melanogaster embryo. J Cell Biol 180(3):537–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Callaini G, Anselmi F (1988) Centrosome splitting during nuclear elongation in the Drosophila embryo. Exp Cell Res 178(2):415–425

    Article  CAS  PubMed  Google Scholar 

  • Callaini G, Dallai R (1991) Abnormal behavior of the yolk centrosomes during early embryogenesis of Drosophila melanogaster. Exp Cell Res 192(1):16–21

    Article  CAS  PubMed  Google Scholar 

  • Callaini G, Riparbelli MG (1996) Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev Biol 176(2):199–208

    Article  CAS  PubMed  Google Scholar 

  • Callaini G, Dallai R, Riparbelli MG (1992) Cytochalasin induces spindle fusion in the syncytial blastoderm of the early Drosophila embryo. Biol Cell 74(3):249–254

    Article  CAS  PubMed  Google Scholar 

  • Callaini G, Whitfield WG, Riparbelli MG (1997) Centriole and centrosome dynamics during the embryonic cell cycles that follow the formation of the cellular blastoderm in Drosophila. Exp Cell Res 234(1):183–190

    Article  CAS  PubMed  Google Scholar 

  • Callaini G, Riparbelli MG, Dallai R (1999) Centrosome inheritance in insects: fertilization and parthenogenesis. Biol Cell 91(4–5):355–366

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Albertson R, Riggs B, Field CM, Sullivan W (2008) Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J Cell Biol 182(2):301–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao J, Crest J, Fasulo B, Sullivan W (2010) Cortical actin dynamics facilitate early-stage centrosome separation. Curr Biol 20(8):770–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cesario JM, Jang JK, Redding B, Shah N, Rahman T, McKim KS (2006) Kinesin 6 family member Subito participates in mitotic spindle assembly and interacts with mitotic regulators. J Cell Sci 119(Pt 22):4770–4780

    Article  CAS  PubMed  Google Scholar 

  • Chen JV, Buchwalter RA, Kao LR, Megraw TL (2017) A splice variant of centrosomin converts mitochondria to microtubule-organizing centers. Curr Biol 27(13):1928–1940.e1926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chodagam S, Royou A, Whitfield W, Karess R, Raff JW (2005) The centrosomal protein CP190 regulates myosin function during early Drosophila development. Curr Biol 15(14):1308–1313

    Article  CAS  PubMed  Google Scholar 

  • Cinalli RM, Lehmann R (2013) A spindle-independent cleavage pathway controls germ cell formation in Drosophila. Nat Cell Biol 15(7):839–845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford JM, Harden N, Leung T, Lim L, Kiehart DP (1998) Cellularization in Drosophila melanogaster is disrupted by the inhibition of rho activity and the activation of Cdc42 function. Dev Biol 204(1):151–164

    Article  CAS  PubMed  Google Scholar 

  • Crest J, Concha-Moore K, Sullivan W (2012) RhoGEF and positioning of rappaport-like furrows in the early Drosophila embryo. Curr Biol 22(21):2037–2041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cullen CF, Ohkura H (2001) Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat Cell Biol 3(7):637–642

    Article  CAS  PubMed  Google Scholar 

  • Dävring L, Sunner M (1973) Female meiosis and embryonic mitosis in Drosophila melanogaster. I. Meiosis and fertilization. Hereditas 73(1):51–64

    Article  PubMed  Google Scholar 

  • Dawes-Hoang RE, Parmar KM, Christiansen AE, Phelps CB, Brand AH, Wieschaus EF (2005) folded gastrulation, cell shape change and the control of myosin localization. Development 132(18):4165–4178

    Article  CAS  PubMed  Google Scholar 

  • Debec A, Kalpin RF, Daily DR, McCallum PD, Rothwell WF, Sullivan W (1996) Live analysis of free centrosomes in normal and aphidicolin-treated Drosophila embryos. J Cell Biol 134(1):103–115

    Article  CAS  PubMed  Google Scholar 

  • Debec A, Marcaillou C, Bobinnec Y, Borot C (1999) The centrosome cycle in syncytial Drosophila embryos analyzed by energy filtering transmission electron microscopy. Biol Cell 91(4–5):379–391

    Article  CAS  PubMed  Google Scholar 

  • Debec A, Grammont M, Berson G, Dastugue B, Sullivan W, Couderc JL (2001) Toucan protein is essential for the assembly of syncytial mitotic spindles in Drosophila melanogaster. Genesis 31(4):167–175

    Article  CAS  PubMed  Google Scholar 

  • Deneke VE, Melbinger A, Vergassola M, Di Talia S (2016) Waves of Cdk1 activity in S phase synchronize the cell cycle in Drosophila embryos. Dev Cell 38(4):399–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dix CI, Raff JW (2007) Drosophila Spd-2 recruits PCM to the sperm centriole, but is dispensable for centriole duplication. Curr Biol 17(20):1759–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ede DA, Counce SJ (1956) A cinematographic study of the embryology of Drosophila melanogaster. Roux Arch Dev Biol 148(4):402–415

    Article  CAS  Google Scholar 

  • Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44(6):871–877

    Article  CAS  PubMed  Google Scholar 

  • Edgar BA, Kiehle CP, Schubiger G (1986) Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 44(2):365–372

    Article  CAS  PubMed  Google Scholar 

  • Edgar BA, Odell GM, Schubiger G (1987) Cytoarchitecture and the patterning of fushi tarazu expression in the Drosophila blastoderm. Genes Dev 1(10):1226–1237

    Article  CAS  PubMed  Google Scholar 

  • Edgar BA, Sprenger F, Duronio RJ, Leopold P, O’Farrell PH (1994) Distinct molecular mechanism regulate cell cycle timing at successive stages of Drosophila embryogenesis. Genes Dev 8(4):440–452

    Article  CAS  PubMed  Google Scholar 

  • Elfring LK, Axton JM, Fenger DD, Page AW, Carminati JL, Orr-Weaver TL (1997) Drosophila PLUTONIUM protein is a specialized cell cycle regulator required at the onset of embryogenesis. Mol Biol Cell 8(4):583–593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358(6385):387–392

    Article  CAS  PubMed  Google Scholar 

  • Fabrowski P, Necakov AS, Mumbauer S, Loeser E, Reversi A, Streichan S, Briggs JA, De Renzis S (2013) Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila. Nat Commun 4:2244

    Article  PubMed  CAS  Google Scholar 

  • Farache D, Emorine L, Haren L, Merdes A (2018) Assembly and regulation of γ-tubulin complexes. Open Biol 8(3)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farina F, Gaillard J, Guérin C, Couté Y, Sillibourne J, Blanchoin L, Théry M (2016) The centrosome is an actin-organizing centre. Nat Cell Biol 18(1):65–75

    Article  CAS  PubMed  Google Scholar 

  • Fenger DD, Carminati JL, Burney-Sigman DL, Kashevsky H, Dines JL, Elfring LK, Orr-Weaver TL (2000) PAN GU: a protein kinase that inhibits S phase and promotes mitosis in early Drosophila development. Development 127(22):4763–4774

    CAS  PubMed  Google Scholar 

  • Field CM, Alberts BM (1995) Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 131(1):165–178

    Article  CAS  PubMed  Google Scholar 

  • Field CM, Coughlin M, Doberstein S, Marty T, Sullivan W (2005) Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 132(12):2849–2860

    Article  CAS  PubMed  Google Scholar 

  • Figard L, Xu H, Garcia HG, Golding I, Sokac AM (2013) The plasma membrane flattens out to fuel cell-surface growth during Drosophila cellularization. Dev Cell 27(6):648–655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flor-Parra I, Iglesias-Romero AB, Chang F (2018) The XMAP215 ortholog Alp14 promotes microtubule nucleation in fission yeast. Curr Biol 28(11):1681–1691.e1684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foe VE, Alberts BM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61:31–70

    CAS  PubMed  Google Scholar 

  • Foe VE, Odell GM, Edgar BA (1993) Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In: Bate M, Martinez Arias A (eds) The Development of Drosophila melanogaster, vol 1. Cold Spring Harbor Press, Cold Spring Harbor, NY

    Google Scholar 

  • Foe VE, Field CM, Odell GM (2000) Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development 127(9):1767–1787

    CAS  PubMed  Google Scholar 

  • Fogarty P, Kalpin RF, Sullivan W (1994) The Drosophila maternal-effect mutation grapes causes a metaphase arrest at nuclear cycle 13. Development 120(8):2131–2142

    CAS  PubMed  Google Scholar 

  • Fogarty P, Campbell SD, Abu-Shumays R, Phalle BS, Yu KR, Uy GL, Goldberg ML, Sullivan W (1997) The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr Biol 7(6):418–426

    Article  CAS  PubMed  Google Scholar 

  • Franz A, Roque H, Saurya S, Dobbelaere J, Raff JW (2013) CP110 exhibits novel regulatory activities during centriole assembly in Drosophila. J Cell Biol 203(5):785–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman M, Glover DM (1987) The gnu mutation of Drosophila causes inappropriate DNA synthesis in unfertilized and fertilized eggs. Genes Dev 1(9):924–930

    Article  CAS  PubMed  Google Scholar 

  • Freeman M, Nüsslein-Volhard C, Glover DM (1986) The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell 46(3):457–468

    Article  CAS  PubMed  Google Scholar 

  • Frescas D, Mavrakis M, Lorenz H, Delotto R, Lippincott-Schwartz J (2006) The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J Cell Biol 173(2):219–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fullilove SL, Jacobson AG (1971) Nuclear elongation and cytokinesis in Drosophila montana. Dev Biol 26(4):560–577

    Article  CAS  PubMed  Google Scholar 

  • Gergely F, Karlsson C, Still I, Cowell J, Kilmartin J, Raff JW (2000a) The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc Natl Acad Sci U S A 97(26):14352–14357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gergely F, Kidd D, Jeffers K, Wakefield JG, Raff JW (2000b) D-TACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J 19(2):241–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giansanti MG, Bucciarelli E, Bonaccorsi S, Gatti M (2008) Drosophila SPD-2 is an essential centriole component required for PCM recruitment and astral-microtubule nucleation. Curr Biol 18(4):303–309

    Article  CAS  PubMed  Google Scholar 

  • Giet R, McLean D, Descamps S, Lee MJ, Raff JW, Prigent C, Glover DM (2002) Drosophila Aurora a kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J Cell Biol 156(3):437–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giunta KL, Jang JK, Manheim EA, Subramanian G, McKim KS (2002) subito encodes a kinesin-like protein required for meiotic spindle pole formation in Drosophila melanogaster. Genetics 160(4):1489–1501

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glover DM (2005) Polo kinase and progression through M phase in Drosophila: a perspective from the spindle poles. Oncogene 24(2):230–237

    Article  CAS  PubMed  Google Scholar 

  • Glover DM, Alphey L, Axton JM, Cheshire A, Dalby B, Freeman M, Girdham C, Gonzalez C, Karess RE, Leibowitz MH (1989) Mitosis in Drosophila development. J Cell Sci Suppl 12:277–291

    Article  CAS  PubMed  Google Scholar 

  • González C, Saunders RD, Casal J, Molina I, Carmena M, Ripoll P, Glover DM (1990) Mutations at the asp locus of Drosophila lead to multiple free centrosomes in syncytial embryos, but restrict centrosome duplication in larval neuroblasts. J Cell Sci 96(Pt 4):605–616

    PubMed  Google Scholar 

  • González C, Tavosanis G, Mollinari C (1998) Centrosomes and microtubule organisation during Drosophila development. J Cell Sci 111(Pt 18):2697–2706

    PubMed  Google Scholar 

  • Gottardo M, Callaini G, Riparbelli MG (2015) The Drosophila centriole—conversion of doublets into triplets within the stem cell niche. J Cell Sci 128(14):2437–2442

    Article  CAS  PubMed  Google Scholar 

  • Grevengoed EE, Fox DT, Gates J, Peifer M (2003) Balancing different types of actin polymerization at distinct sites: roles for Abelson kinase and enabled. J Cell Biol 163(6):1267–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Großhans J, Wenzl C, Herz HM, Bartoszewski S, Schnorrer F, Vogt N, Schwarz H, Müller HA (2005) RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 132(5):1009–1020

    Article  PubMed  CAS  Google Scholar 

  • Gunawardane RN, Lizarraga SB, Wiese C, Wilde A, Zheng Y (2000) γ-tubulin complexes and their role in microtubule nucleation. Curr Top Dev Biol 49:55–73

    Article  CAS  PubMed  Google Scholar 

  • Gunzelmann J, Rüthnick D, Lin TC, Zhang W, Neuner A, Jäkle U, Schiebel E (2018) The microtubule polymerase Stu2 promotes oligomerization of the γ-TuSC for cytoplasmic microtubule nucleation. elife 7

    Google Scholar 

  • Hatanaka K, Okada M (1991) Retarded nuclear migration in Drosophila embryos with aberrant F-actin reorganization caused by maternal mutations and by cytochalasin treatment. Development 111(4):909–920

    CAS  PubMed  Google Scholar 

  • Heck MM, Pereira A, Pesavento P, Yannoni Y, Spradling AC, Goldstein LS (1993) The kinesin-like protein KLP61F is essential for mitosis in Drosophila. J Cell Biol 123(3):665–679

    Article  CAS  PubMed  Google Scholar 

  • Hieda M (2017) Implications for diverse functions of the LINC complexes based on the structure. Cell 6(1)

    Article  PubMed Central  CAS  Google Scholar 

  • Huang J, Raff JW (1999) The disappearance of cyclin B at the end of mitosis is regulated spatially in Drosophila cells. EMBO J 18(8):2184–2195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter C, Wieschaus E (2000) Regulated expression of nullo is required for the formation of distinct apical and basal adherens junctions in the Drosophila blastoderm. J Cell Biol 150(2):391–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iampietro C, Bergalet J, Wang X, Cody NA, Chin A, Lefebvre FA, Douziech M, Krause HM, Lécuyer E (2014) Developmentally regulated elimination of damaged nuclei involves a Chk2-dependent mechanism of mRNA nuclear retention. Dev Cell 29(4):468–481

    Article  CAS  PubMed  Google Scholar 

  • Iida T, Kobayashi S (2000) Delocalization of polar plasm components caused by grandchildless mutations, gs(1)N26 and gs(1)N441, in Drosophila melanogaster. Develop Growth Differ 42(1):53–60

    Article  CAS  Google Scholar 

  • Illmensee K, Mahowald AP (1974) Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci U S A 71(4):1016–1020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones J, Macdonald PM (2015) Neurl4 contributes to germ cell formation and integrity in Drosophila. Biol Open 4(8):937–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jongens TA, Hay B, Jan LY, Jan YN (1992) The germ cell-less gene product: a posteriorly localized component necessary for germ cell development in Drosophila. Cell 70(4):569–584

    Article  CAS  PubMed  Google Scholar 

  • Jongens TA, Ackerman LD, Swedlow JR, Jan LY, Jan YN (1994) Germ cell-less encodes a cell type-specific nuclear pore-associated protein and functions early in the germ-cell specification pathway of Drosophila. Genes Dev 8(18):2123–2136

    Article  CAS  PubMed  Google Scholar 

  • Jordan P, Karess R (1997) Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J Cell Biol 139(7):1805–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kao LR, Megraw TL (2009) Centrocortin cooperates with centrosomin to organize Drosophila embryonic cleavage furrows. Curr Biol 19(11):937–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karess RE, Chang XJ, Edwards KA, Kulkarni S, Aguilera I, Kiehart DP (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65(7):1177–1189

    Article  CAS  PubMed  Google Scholar 

  • Karr TL (1991) Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech Dev 34(2–3):101–111

    Article  CAS  PubMed  Google Scholar 

  • Karr TL, Alberts BM (1986) Organization of the cytoskeleton in early Drosophila embryos. J Cell Biol 102(4):1494–1509

    Article  CAS  PubMed  Google Scholar 

  • Kellogg DR, Mitchison TJ, Alberts BM (1988) Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103(4):675–686

    CAS  PubMed  Google Scholar 

  • Kellogg DR, Field CM, Alberts BM (1989) Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo. J Cell Biol 109(6 Pt 1):2977–2991

    Article  CAS  PubMed  Google Scholar 

  • Kellogg DR, Sullivan W, Theurkauf W, Oegema K, Raff JW, Alberts BM (1991) Studies on the centrosome and cytoplasmic organization in the early Drosophila embryo. Cold Spring Harb Symp Quant Biol 56:649–662

    Article  CAS  PubMed  Google Scholar 

  • Khire A, Jo KH, Kong D, Akhshi T, Blachon S, Cekic AR, Hynek S, Ha A, Loncarek J, Mennella V, Avidor-Reiss T (2016) Centriole remodeling during spermiogenesis in Drosophila. Curr Biol 26(23):3183–3189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiehart DP, Ketchum A, Young P, Lutz D, Alfenito MR, Chang XJ, Awobuluyi M, Pesacreta TC, Inoué S, Stewart CT (1990) Contractile proteins in Drosophila development. Ann N Y Acad Sci 582:233–251

    Article  CAS  PubMed  Google Scholar 

  • Knoblich JA (2000) Epithelial polarity: the ins and outs of the fly epidermis. Curr Biol 10(21):R791–R794

    Article  CAS  PubMed  Google Scholar 

  • Kollman JM, Greenberg CH, Li S, Moritz M, Zelter A, Fong KK, Fernandez JJ, Sali A, Kilmartin J, Davis TN, Agard DA (2015) Ring closure activates yeast γTuRC for species-specific microtubule nucleation. Nat Struct Mol Biol 22(2):132–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komma DJ, Endow SA (1997) Enhancement of the ncdD microtubule motor mutant by mutants of αTub67C. J Cell Sci 110(Pt 2):229–237

    CAS  PubMed  Google Scholar 

  • Kotadia S, Crest J, Tram U, Riggs B, Sullivan W (2010) Blastoderm formation and cellularisation in Drosophila melanogaster. eLS

    Google Scholar 

  • LaLonde M, Janssens H, Yun S, Crosby J, Redina O, Olive V, Altshuller YM, Choi SY, Du G, Gergen JP, Frohman MA (2006) A role for phospholipase D in Drosophila embryonic cellularization. BMC Dev Biol 6:60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lamb MM, Laird CD (1976) Increase in nuclear poly(A)-containing RNA at syncytial blastoderm in Drosophila melanogaster embryos. Dev Biol 52(1):31–42

    Article  CAS  PubMed  Google Scholar 

  • Lantz VA, Miller KG (1998) A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J Cell Biol 140(4):897–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lantz VA, Clemens SE, Miller KG (1999) The actin cytoskeleton is required for maintenance of posterior pole plasm components in the Drosophila embryo. Mech Dev 85(1–2):111–122

    Article  CAS  PubMed  Google Scholar 

  • Lasko P (2012) mRNA localization and translational control in Drosophila oogenesis. Cold Spring Harb Perspect Biol 4(10)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lattao R, Kovács L, Glover DM (2017) The centrioles, centrosomes, basal bodies, and cilia of Drosophila melanogaster. Genetics 206(1):33–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lecuit T, Wieschaus E (2000) Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J Cell Biol 150(4):849–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee DM, Harris TJ (2014) Coordinating the cytoskeleton and endocytosis for regulated plasma membrane growth in the early Drosophila embryo. BioArchitecture 4(2):68–74

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee MJ, Gergely F, Jeffers K, Peak-Chew SY, Raff JW (2001) Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat Cell Biol 3(7):643–649

    Article  CAS  PubMed  Google Scholar 

  • Lee DM, Wilk R, Hu J, Krause HM, Harris TJ (2015) Germ cell segregation from the Drosophila Soma is controlled by an inhibitory threshold set by the Arf-GEF Steppke. Genetics 200(3):863–872

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lerit DA, Gavis ER (2011) Transport of germ plasm on astral microtubules directs germ cell development in Drosophila. Curr Biol 21(6):439–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lerit DA, Shebelut CW, Lawlor KJ, Rusan NM, Gavis ER, Schedl P, Deshpande G (2017) Germ cell-less promotes centrosome segregation to induce germ cell formation. Cell Rep 18(4):831–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Kim S, Kobayashi T, Liang FX, Korzeniewski N, Duensing S, Dynlacht BD (2012) Neurl4, a novel daughter centriole protein, prevents formation of ectopic microtubule organizing centres. EMBO Rep 13(6):547–553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin TC, Neuner A, Schiebel E (2015) Targeting of γ-tubulin complexes to microtubule organizing centers: conservation and divergence. Trends Cell Biol 25(5):296–307

    Article  CAS  PubMed  Google Scholar 

  • Lindeman RE, Pelegri F (2012) Localized products of futile cycle/lrmp promote centrosome-nucleus attachment in the zebrafish zygote. Curr Biol 22(10):843–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llamazares S, Tavosanis G, Gonzalez C (1999) Cytological characterisation of the mutant phenotypes produced during early embryogenesis by null and loss-of-function alleles of the γTub37C gene in Drosophila. J Cell Sci 112(Pt 5):659–667

    Google Scholar 

  • Loppin B, Dubruille R, Horard B (2015) The intimate genetics of Drosophila fertilization. Open Biol 5(8)

    Google Scholar 

  • Lucas EP, Raff JW (2007) Maintaining the proper connection between the centrioles and the pericentriolar matrix requires Drosophila centrosomin. J Cell Biol 178(5):725–732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahoney NM, Goshima G, Douglass AD, Vale RD (2006) Making microtubules and mitotic spindles in cells without functional centrosomes. Curr Biol 16(6):564–569

    Article  CAS  PubMed  Google Scholar 

  • Mahowald AP (2001) Assembly of the Drosophila germ plasm. Int Rev Cytol 203:187–213

    Article  CAS  PubMed  Google Scholar 

  • Malone CJ, Misner L, Le Bot N, Tsai MC, Campbell JM, Ahringer J, White JG (2003) The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115(7):825–836

    Article  CAS  PubMed  Google Scholar 

  • Mazumdar A, Mazumdar M (2002) How one becomes many: blastoderm cellularization in Drosophila melanogaster. BioEssays 24(11):1012–1022

    Article  CAS  PubMed  Google Scholar 

  • McCartney BM, Peifer M (2000) Teaching tumour suppressors new tricks. Nat Cell Biol 2(4):E58–E60

    Article  CAS  PubMed  Google Scholar 

  • McCartney BM, McEwen DG, Grevengoed E, Maddox P, Bejsovec A, Peifer M (2001) Drosophila APC2 and armadillo participate in tethering mitotic spindles to cortical actin. Nat Cell Biol 3(10):933–938

    Article  CAS  PubMed  Google Scholar 

  • McKnight SL, Bustin M, Miller OL (1977) Electron microscope analysis of chromosome metabolism in Drosophila melanogaster embryo. Cold Spring Harb Symp Quant Biol 41:741–754

    Google Scholar 

  • Megraw TL, Li K, Kao LR, Kaufman TC (1999) The centrosomin protein is required for centrosome assembly and function during cleavage in Drosophila. Development 126(13):2829–2839

    CAS  PubMed  Google Scholar 

  • Megraw TL, Kao LR, Kaufman TC (2001) Zygotic development without functional mitotic centrosomes. Curr Biol 11(2):116–120

    Article  CAS  PubMed  Google Scholar 

  • Mermall V, Miller KG (1995) The 95F unconventional myosin is required for proper organization of the Drosophila syncytial blastoderm. J Cell Biol 129(6):1575–1588

    Article  CAS  PubMed  Google Scholar 

  • Mermall V, McNally JG, Miller KG (1994) Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embryos. Nature 369(6481):560–562

    Article  CAS  PubMed  Google Scholar 

  • Meyerzon M, Gao Z, Liu J, Wu JC, Malone CJ, Starr DA (2009) Centrosome attachment to the C. elegans male pronucleus is dependent on the surface area of the nuclear envelope. Dev Biol 327(2):433–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller KG, Kiehart DP (1995) Fly division. J Cell Biol 131(1):1–5

    Article  CAS  PubMed  Google Scholar 

  • Minestrini G, Harley AS, Glover DM (2003) Localization of Pavarotti-KLP in living Drosophila embryos suggests roles in reorganizing the cortical cytoskeleton during the mitotic cycle. Mol Biol Cell 14(10):4028–4038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirouse V, Dastugue B, Couderc JL (2005) The Drosophila toucan protein is a new mitotic microtubule-associated protein required for spindle microtubule stability. Genes Cells 10(1):37–46

    Article  CAS  PubMed  Google Scholar 

  • Mogensen MM, Tucker JB, Baggaley TB (1993) Multiple plasma membrane-associated MTOC systems in the acentrosomal cone cells of Drosophila ommatidia. Eur J Cell Biol 60(1):67–75

    CAS  PubMed  Google Scholar 

  • Moritz M, Braunfeld MB, Fung JC, Sedat JW, Alberts BM, Agard DA (1995) Three-dimensional structural characterization of centrosomes from early Drosophila embryos. J Cell Biol 130(5):1149–1159

    Article  CAS  PubMed  Google Scholar 

  • Müller HA, Wieschaus E (1996) armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J Cell Biol 134(1):149–163

    Article  PubMed  Google Scholar 

  • Niki Y (1984) Developmental analysis of the grandchildless (gs(1)N26) mutation in Drosophila melanogaster: abnormal cleavage patterns and defects in pole cell formation. Dev Biol 103(1):182–189

    Article  CAS  PubMed  Google Scholar 

  • Niki Y, Okada M (1981) Isolation and characterization of grandchildless-like mutants in Drosophila melanogaster. Roux Arch Dev Biol 190(1):1–10

    Article  Google Scholar 

  • Nithianantham S, Cook BD, Beans M, Guo F, Chang F, Al-Bassam J (2018) Structural basis of tubulin recruitment and assembly by microtubule polymerases with tumor overexpressed gene (TOG) domain arrays. elife 7

    Google Scholar 

  • O’Farrell PH (2015) Growing an embryo from a single cell: a hurdle in animal life. Cold Spring Harb Perspect Biol 7(11)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Farrell PH, Stumpff J, Su TT (2004) Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol 14(1):R35–R45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oakley BR (2000) γ-Tubulin. Curr Top Dev Biol 49:27–54

    Article  CAS  PubMed  Google Scholar 

  • Oakley BR, Paolillo V, Zheng Y (2015) γ-Tubulin complexes in microtubule nucleation and beyond. Mol Biol Cell 26(17):2957–2962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okada M (1982) Loss of the ability to form pole cells in Drosophila embryos with artificially delayed nuclear arrival at the posterior pole. Prog Clin Biol Res 85(Pt A):363–372

    PubMed  Google Scholar 

  • Padash Barmchi M, Rogers S, Häcker U (2005) DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo. J Cell Biol 168(4):575–585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paddy MR, Saumweber H, Agard DA, Sedat JW (1996) Time-resolved, in vivo studies of mitotic spindle formation and nuclear lamina breakdown in Drosophila early embryos. J Cell Sci 109(Pt 3):591–607

    CAS  PubMed  Google Scholar 

  • Pai CY, Lei EP, Ghosh D, Corces VG (2004) The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol Cell 16(5):737–748

    Article  CAS  PubMed  Google Scholar 

  • Papoulas O, Hays TS, Sisson JC (2005) The golgin lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat Cell Biol 7(6):612–618

    Article  CAS  PubMed  Google Scholar 

  • Peel N, Stevens NR, Basto R, Raff JW (2007) Overexpressing centriole-replication proteins in vivo induces centriole overduplication and de novo formation. Curr Biol 17(10):834–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelissier A, Chauvin JP, Lecuit T (2003) Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 13(21):1848–1857

    Article  CAS  PubMed  Google Scholar 

  • Piekny AJ, Glotzer M (2008) Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr Biol 18(1):30–36

    Article  CAS  PubMed  Google Scholar 

  • Pollitt AY, Insall RH (2009) WASP and SCAR/WAVE proteins: the drivers of actin assembly. J Cell Sci 122(Pt 15):2575–2578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Postner MA, Miller KG, Wieschaus EF (1992) Maternal effect mutations of the sponge locus affect actin cytoskeletal rearrangements in Drosophila melanogaster embryos. J Cell Biol 119(5):1205–1218

    Article  CAS  PubMed  Google Scholar 

  • Raff JW, Glover DM (1988) Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J Cell Biol 107(6 Pt 1):2009–2019

    Article  CAS  PubMed  Google Scholar 

  • Raff JW, Glover DM (1989) Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell 57(4):611–619

    Article  CAS  PubMed  Google Scholar 

  • Raff JW, Jeffers K, Huang JY (2002) The roles of Fzy/Cdc20 and Fzr/Cdh1 in regulating the destruction of cyclin B in space and time. J Cell Biol 157(7):1139–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rappaport R (1961) Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool 148:81–89

    Article  CAS  PubMed  Google Scholar 

  • Riggs B, Rothwell W, Mische S, Hickson GR, Matheson J, Hays TS, Gould GW, Sullivan W (2003) Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components nuclear-fallout and Rab11. J Cell Biol 163(1):143–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riggs B, Fasulo B, Royou A, Mische S, Cao J, Hays TS, Sullivan W (2007) The concentration of Nuf, a Rab11 effector, at the microtubule-organizing center is cell cycle regulated, dynein-dependent, and coincides with furrow formation. Mol Biol Cell 18(9):3313–3322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rikhy R, Mavrakis M, Lippincott-Schwartz J (2015) Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo. Biol Open 4(3):301–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riparbelli MG, Callaini G (2003) Assembly of yolk spindles in the early Drosophila embryo. Mech Dev 120(4):441–454

    Article  CAS  PubMed  Google Scholar 

  • Riparbelli MG, Callaini G, Glover DM (2000) Failure of pronuclear migration and repeated divisions of polar body nuclei associated with MTOC defects in polo eggs of Drosophila. J Cell Sci 113(Pt 18):3341–3350

    CAS  PubMed  Google Scholar 

  • Riparbelli MG, Callaini G, Glover DM, Avides MC (2002) A requirement for the abnormal spindle protein to organise microtubules of the central spindle for cytokinesis in Drosophila. J Cell Sci 115(Pt 5):913–922

    CAS  PubMed  Google Scholar 

  • Riparbelli MG, Callaini G, Schejter ED (2007) Microtubule-dependent organization of subcortical microfilaments in the early Drosophila embryo. Dev Dyn 236(3):662–670

    Article  CAS  PubMed  Google Scholar 

  • Ripoche J, Link B, Yucel JK, Tokuyasu K, Malhotra V (1994) Location of Golgi membranes with reference to dividing nuclei in syncytial Drosophila embryos. Proc Natl Acad Sci U S A 91(5):1878–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson SE, Dockendorff TC, Leatherman JL, Faulkner DL, Jongens TA (1999) germ cell-less is required only during the establishment of the germ cell lineage of Drosophila and has activities which are dependent and independent of its localization to the nuclear envelope. Dev Biol 215(2):288–297

    Article  CAS  PubMed  Google Scholar 

  • Robinson JT, Wojcik EJ, Sanders MA, McGrail M, Hays TS (1999) Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J Cell Biol 146(3):597–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues-Martins A, Bettencourt-Dias M, Riparbelli M, Ferreira C, Ferreira I, Callaini G, Glover DM (2007a) DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol 17(17):1465–1472

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues-Martins A, Riparbelli M, Callaini G, Glover DM, Bettencourt-Dias M (2007b) Revisiting the role of the mother centriole in centriole biogenesis. Science 316(5827):1046–1050

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues-Martins A, Riparbelli M, Callaini G, Glover DM, Bettencourt-Dias M (2008) From centriole biogenesis to cellular function: centrioles are essential for cell division at critical developmental stages. Cell Cycle 7(1):11–16

    Article  CAS  PubMed  Google Scholar 

  • Rogers SL, Rogers GC, Sharp DJ, Vale RD (2002) Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J Cell Biol 158(5):873–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rothwell WF, Fogarty P, Field CM, Sullivan W (1998) Nuclear-fallout, a drosophila protein that cycles from the cytoplasm to the centrosomes, regulates cortical microfilament organization. Development 125(7):1295–1303

    CAS  PubMed  Google Scholar 

  • Rothwell WF, Sullivan W (2000) The centrosome in early Drosophila embryogenesis. Curr Top Dev Biol 49:409–447

    Article  CAS  PubMed  Google Scholar 

  • Rothwell WF, Zhang CX, Zelano C, Hsieh TS, Sullivan W (1999) The Drosophila centrosomal protein Nuf is required for recruiting Dah, a membrane associated protein, to furrows in the early embryo. J Cell Sci 112(Pt 17):2885–2893

    Google Scholar 

  • Royou A, Sullivan W, Karess R (2002) Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J Cell Biol 158(1):127–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schejter ED, Wieschaus E (1993) bottleneck acts as a regulator of the microfilament network governing cellularization of the Drosophila embryo. Cell 75(2):373–385

    Article  CAS  PubMed  Google Scholar 

  • Shamanski FL, Orr-Weaver TL (1991) The Drosophila plutonium and pan gu genes regulate entry into S phase at fertilization. Cell 66(6):1289–1300

    Article  CAS  PubMed  Google Scholar 

  • Sharp DJ, Yu KR, Sisson JC, Sullivan W, Scholey JM (1999) Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat Cell Biol 1(1):51–54

    Article  CAS  PubMed  Google Scholar 

  • Shaw M, Cohen P, Alessi DR (1997) Further evidence that the inhibition of glycogen synthase kinase-3beta by IGF-1 is mediated by PDK1/PKB-induced phosphorylation of Ser-9 and not by dephosphorylation of Tyr-216. FEBS Lett 416(3):307–311

    Article  CAS  PubMed  Google Scholar 

  • Sherlekar A, Rikhy R (2016) Syndapin promotes pseudocleavage furrow formation by actin organization in the syncytial Drosophila embryo. Mol Biol Cell 27(13):2064–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Shermoen AW, McCleland ML, O’Farrell PH (2010) Developmental control of late replication and S phase length. Curr Biol 20(23):2067–2077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sibon OC, Stevenson VA, Theurkauf WE (1997) DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388(6637):93–97

    Article  CAS  PubMed  Google Scholar 

  • Sibon OC, Laurençon A, Hawley R, Theurkauf WE (1999) The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr Biol 9(6):302–312

    Article  CAS  PubMed  Google Scholar 

  • Sibon OC, Kelkar A, Lemstra W, Theurkauf WE (2000) DNA-replication/DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat Cell Biol 2(2):90–95

    Article  CAS  PubMed  Google Scholar 

  • Sigrist S, Jacobs H, Stratmann R, Lehner CF (1995) Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. EMBO J 14(19):4827–4838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sisson JC, Field C, Ventura R, Royou A, Sullivan W (2000) Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol 151(4):905–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokac AM, Wieschaus E (2008a) Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell 14(5):775–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokac AM, Wieschaus E (2008b) Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization. J Cell Sci 121(11):1815–1824

    Article  CAS  PubMed  Google Scholar 

  • Stafstrom JP, Staehelin LA (1984) Dynamics of the nuclear envelope and of nuclear pore complexes during mitosis in the Drosophila embryo. Eur J Cell Biol 34(1):179–189

    CAS  PubMed  Google Scholar 

  • Stanley H, Botas J, Malhotra V (1997) The mechanism of Golgi segregation during mitosis is cell type-specific. Proc Natl Acad Sci U S A 94(26):14467–14470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevens NR, Raposo AA, Basto R, St Johnston D, Raff JW (2007) From stem cell to embryo without centrioles. Curr Biol 17(17):1498–1503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevens NR, Dobbelaere J, Brunk K, Franz A, Raff JW (2010) Drosophila Ana2 is a conserved centriole duplication factor. J Cell Biol 188(3):313–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson VA, Kramer J, Kuhn J, Theurkauf WE (2001) Centrosomes and the scrambled protein coordinate microtubule-independent actin reorganization. Nat Cell Biol 3(1):68–75

    Article  CAS  PubMed  Google Scholar 

  • Stevenson V, Hudson A, Cooley L, Theurkauf WE (2002) Arp2/3-dependent pseudocleavage [correction of psuedocleavage] furrow assembly in syncytial Drosophila embryos. Curr Biol 12(9):705–711

    Article  CAS  PubMed  Google Scholar 

  • Stiffler LA, Ji JY, Trautmann S, Trusty C, Schubiger G (1999) Cyclin A and B functions in the early Drosophila embryo. Development 126(23):5505–5513

    CAS  PubMed  Google Scholar 

  • Su TT, Sprenger F, DiGregorio PJ, Campbell SD, O’Farrell PH (1998) Exit from mitosis in Drosophila syncytial embryos requires proteolysis and cyclin degradation, and is associated with localized dephosphorylation. Genes Dev 12(10):1495–1503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Chow B, Boulianne GL, Wilde A (2013) The BAR domain of amphiphysin is required for cleavage furrow tip-tubule formation during cellularization in Drosophila embryos. Mol Biol Cell 24(9):1444–1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan W, Minden JS, Alberts BM (1990) daughterless-abo-like, a Drosophila maternal-effect mutation that exhibits abnormal centrosome separation during the late blastoderm divisions. Development 110(2):311–323

    CAS  PubMed  Google Scholar 

  • Sullivan W, Daily DR, Fogarty P, Yook KJ, Pimpinelli S (1993a) Delays in anaphase initiation occur in individual nuclei of the syncytial Drosophila embryo. Mol Biol Cell 4(9):885–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan W, Fogarty P, Theurkauf W (1993b) Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development 118(4):1245–1254

    CAS  PubMed  Google Scholar 

  • Swanson MM, Poodry CA (1981) The shibire(ts) mutant of Drosophila: a probe for the study of embryonic development. Dev Biol 84(2):465–470

    Article  CAS  PubMed  Google Scholar 

  • Takada S, Kelkar A, Theurkauf WE (2003) Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113(1):87–99

    Article  CAS  PubMed  Google Scholar 

  • Tavosanis G, Llamazares S, Goulielmos G, Gonzalez C (1997) Essential role for γ-tubulin in the acentriolar female meiotic spindle of Drosophila. EMBO J 16(8):1809–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Technau M, Roth S (2008) The Drosophila KASH domain proteins Msp-300 and Klarsicht and the SUN domain protein Klaroid have no essential function during oogenesis. Fly (Austin) 2(2):82–91

    Article  Google Scholar 

  • Theurkauf WE (1994) Actin cytoskeleton. Through the bottleneck. Curr Biol 4(1):76–78

    Article  CAS  PubMed  Google Scholar 

  • Thomas JH, Wieschaus E (2004) src64 and tec29 are required for microfilament contraction during Drosophila cellularization. Development 131(4):863–871

    Article  CAS  PubMed  Google Scholar 

  • Tillery MML, Blake-Hedges C, Zheng Y, Buchwalter RA, Megraw TL (2018) Centrosomal and non-centrosomal microtubule-organizing centers (MTOCs) in Drosophila melanogaster. Cell 7(9)

    Article  PubMed Central  Google Scholar 

  • Tucker JB, Milner MJ, Currie DA, Muir JW, Forrest DA, Spencer MJ (1986) Centrosomal microtubule-organizing centers and a switch in the control of protofilament number for cell surfacing-associated microtubules during Drosophila wing morphogenesis. Eur J Cell Biol 41:279–289

    Google Scholar 

  • Turner FR, Mahowald AP (1976) Scanning electron microscopy of Drosophila embryogenesis. 1. The structure of the egg envelopes and the formation of the cellular blastoderm. Dev Biol 50(1):95–108

    Article  CAS  PubMed  Google Scholar 

  • Turner FR, Mahowald AP (1979) Scanning electron microscopy of Drosophila embryogenesis. III. Formation of the head and caudal segments. Dev Biol 68(1):96–109

    Article  CAS  PubMed  Google Scholar 

  • Vaizel-Ohayon D, Schejter ED (1999) Mutations in centrosomin reveal requirements for centrosomal function during early Drosophila embryogenesis. Curr Biol 9(16):889–898

    Article  CAS  PubMed  Google Scholar 

  • van Ijzendoorn SC (2006) Recycling endosomes. J Cell Sci 119(Pt 9):1679–1681

    Article  PubMed  CAS  Google Scholar 

  • Varmark H, Llamazares S, Rebollo E, Lange B, Reina J, Schwarz H, Gonzalez C (2007) Asterless is a centriolar protein required for centrosome function and embryo development in Drosophila. Curr Biol 17(20):1735–1745

    Article  CAS  PubMed  Google Scholar 

  • Venkei Z, Gáspár I, Tóth G, Szabad J (2006) alpha4-tubulin is involved in rapid formation of long microtubules to push apart the daughter centrosomes during early Drosophila embryogenesis. J Cell Sci 119(Pt 15):3238–3248

    Article  CAS  PubMed  Google Scholar 

  • von Dassow G, Schubiger G (1994) How an actin network might cause fountain streaming and nuclear migration in the syncytial Drosophila embryo. J Cell Biol 127(6 Pt 1):1637–1653

    Article  Google Scholar 

  • Von Stetina JR, Orr-Weaver TL (2011) Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol 3(10):a005553

    Google Scholar 

  • Wakefield JG, Huang JY, Raff JW (2000) Centrosomes have a role in regulating the destruction of cyclin B in early Drosophila embryos. Curr Biol 10(21):1367–1370

    Article  CAS  PubMed  Google Scholar 

  • Walker JJ, Lee KK, Desai RN, Erickson JW (2000) The Drosophila melanogaster sex determination gene sisA is required in yolk nuclei for midgut formation. Genetics 155(1):191–202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Pinson X, Archambault V (2011) PP2A-twins is antagonized by greatwall and collaborates with polo for cell cycle progression and centrosome attachment to nuclei in Drosophila embryos. PLoS Genet 7(8):e1002227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warn RM, Robert-Nicoud M (1990) F-actin organization during the cellularization of the Drosophila embryo as revealed with a confocal laser scanning microscope. J Cell Sci 96(Pt 1):35–42

    PubMed  Google Scholar 

  • Warn RM, Magrath R, Webb S (1984) Distribution of F-actin during cleavage of the Drosophila syncytial blastoderm. J Cell Biol 98(1):156–162

    Article  CAS  PubMed  Google Scholar 

  • Warn RM, Smith L, Warn A (1985) Three distinct distributions of F-actin occur during the divisions of polar surface caps to produce pole cells in Drosophila embryos. J Cell Biol 100(4):1010–1015

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16(11):3044–3056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webb RL, Zhou MN, McCartney BM (2009) A novel role for an APC2-diaphanous complex in regulating actin organization in Drosophila. Development 136(8):1283–1293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG (2004) EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 6(9):820–830

    Article  CAS  PubMed  Google Scholar 

  • Wenzl C, Yan S, Laupsien P, Grosshans J (2010) Localization of RhoGEF2 during Drosophila cellularization is developmentally controlled by Slam. Mech Dev 127(7–8):371–384

    Article  CAS  PubMed  Google Scholar 

  • Wheatley S, Kulkarni S, Karess R (1995) Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121(6):1937–1946

    CAS  PubMed  Google Scholar 

  • Williams BC, Dernburg AF, Puro J, Nokkala S, Goldberg ML (1997) The Drosophila kinesin-like protein KLP3A is required for proper behavior of male and female pronuclei at fertilization. Development 124(12):2365–2376

    CAS  PubMed  Google Scholar 

  • Wilson PG, Borisy GG (1998) Maternally expressed γTub37CD in Drosophila is differentially required for female meiosis and embryonic mitosis. Dev Biol 199(2):273–290

    Article  CAS  PubMed  Google Scholar 

  • Wilson PG, Zheng Y, Oakley CE, Oakley BR, Borisy GG, Fuller MT (1997) Differential expression of two gamma-tubulin isoforms during gametogenesis and development in Drosophila. Dev Biol 184(2):207–221

    Article  CAS  PubMed  Google Scholar 

  • Wolf R (1980) Migration and division of cleavage nuclei in the gall midge, Wachtliella persicariae: II. Origin and ultrastructure of the migration cytaster. Roux Arch Dev Biol 188(1):65–73

    Article  Google Scholar 

  • Xue Z, Sokac AM (2016) Back-to-back mechanisms drive actomyosin ring closure during Drosophila embryo cleavage. J Cell Biol 215(3):335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuda GK, Baker J, Schubiger G (1991) Independent roles of centrosomes and DNA in organizing the Drosophila cytoskeleton. Development 111(2):379–391

    CAS  PubMed  Google Scholar 

  • Yohn CB, Pusateri L, Barbosa V, Lehmann R (2003) l(3)malignant brain tumor and three novel genes are required for Drosophila germ-cell formation. Genetics 165(4):1889–1900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young PE, Pesacreta TC, Kiehart DP (1991) Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development 111(1):1–14

    CAS  PubMed  Google Scholar 

  • Zallen JA, Cohen Y, Hudson AM, Cooley L, Wieschaus E, Schejter ED (2002) SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J Cell Biol 156(4):689–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalokar M (1976) Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev Biol 49(2):425–437

    Article  CAS  PubMed  Google Scholar 

  • Zalokar M, Erk I (1976) Division and migration of nuclei during early embryogenesis of Drosophila melanogaster. J Microsc Biol Cell 25:97–106

    Google Scholar 

  • Zhang J, Megraw TL (2007) Proper recruitment of γ-tubulin and D-TACC/Msps to embryonic Drosophila centrosomes requires Centrosomin Motif 1. Mol Biol Cell 18(10):4037–4049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang CX, Rothwell WF, Sullivan W, Hsieh TS (2000) Discontinuous actin hexagon, a protein essential for cortical furrow formation in Drosophila, is membrane associated and hyperphosphorylated. Mol Biol Cell 11(3):1011–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Breuer M, Förster A, Egger-Adam D, Wodarz A (2009) Mars, a Drosophila protein related to vertebrate HURP, is required for the attachment of centrosomes to the mitotic spindle during syncytial nuclear divisions. J Cell Sci 122(Pt 4):535–545

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, College of Medicine, Florida State University, Tallahassee, FL, USA

    Caitlyn Blake-Hedges & Timothy L. Megraw

Authors
  1. Caitlyn Blake-Hedges
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy L. Megraw
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Caitlyn Blake-Hedges .

Editor information

Editors and Affiliations

  1. Department of Surgery, Houston Methodist Hospital, Houston, TX, USA

    Malgorzata Kloc

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Blake-Hedges, C., Megraw, T.L. (2019). Coordination of Embryogenesis by the Centrosome in Drosophila melanogaster . In: Kloc, M. (eds) The Golgi Apparatus and Centriole. Results and Problems in Cell Differentiation, vol 67. Springer, Cham. https://doi.org/10.1007/978-3-030-23173-6_12

Download citation

Publish with us

Policies and ethics

Search

Navigation