Skip to main content

Centriole Duplication and Inheritance in Drosophila melanogaster

  • Chapter
  • First Online:
The Centrosome

Abstract

Centrosomes are conserved microtubule-based organelles that are essential for animal development. In this chapter, we highlight key centrosomal proteins and describe the centrosome in the context of several developmental processes in Drosophila melanogaster. These processes include fertilization, during which the centrosome mediates the fusion of male and female pronuclei; development of the embryonic syncytium, where centrosomes act as microtubule-organizing centers and participate in nuclear division; and the formation of sensory and motile cilia in the adult, where the centrosome's centrioles template axoneme assembly. The study of these processes in Drosophila provides a unique experimental system where classical approaches in genetics and biochemistry can be used to dissect centrosome biology.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Al-Dosari MS, Shaheen R, Colak D, Alkuraya FS (2010) Novel CENPJ mutation causes Seckel syndrome. J Med Genet 47:411–414

    PubMed  CAS  Google Scholar 

  • Alieva IB, Uzbekov RE (2008) The centrosome is a polyfunctional multiprotein cell complex. Biochemistry (Mosc) 73:626–643

    CAS  Google Scholar 

  • Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426:570–574

    PubMed  CAS  Google Scholar 

  • Anderson RG, Brenner RM (1971) The formation of basal bodies (centrioles) in the Rhesus monkey oviduct. J Cell Biol 50:10–34

    PubMed  CAS  Google Scholar 

  • Avidor-Reiss T (2010) The cellular and developmental program connecting the centrosome and cilium duplication cycle. Semin Cell Dev Biol 21:139–141

    PubMed  Google Scholar 

  • Avidor-Reiss T, Maer AM, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S, Zuker CS (2004) Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117:527–539

    PubMed  CAS  Google Scholar 

  • Azimzadeh J, Marshall WF (2010) Building the Centriole. Curr Biol 20:R816–R825

    PubMed  CAS  Google Scholar 

  • Baker JD, Adhikarakunnathu S, Kernan MJ (2004) Mechanosensory-defective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila. Development 131:3411–3422

    PubMed  CAS  Google Scholar 

  • Basto R, Brunk K, Vinadogrova T, Peel N, Franz A, Khodjakov A, Raff JW (2008) Centrosome amplification can initiate tumorigenesis in flies. Cell 133:1032–1042

    PubMed  CAS  Google Scholar 

  • Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW (2006) Flies without Centrioles. Cell 125:1375–1386

    PubMed  CAS  Google Scholar 

  • Betleja E, Cole DG (2010) Ciliary trafficking: CEP290 guards a gated community. Curr Biol 20:R928–R931

    PubMed  CAS  Google Scholar 

  • Bettencourt-Dias M, Rodrigues-Martins A, Carpenter L, Riparbelli M, Lehmann L, Gatt MK, Carmo N, Balloux F, Callaini G, Glover DM (2005) SAK/PLK4 is required for centriole duplication and flagella development. Curr Biol 15:2199–2207

    PubMed  CAS  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 182:133–144

    PubMed  CAS  Google Scholar 

  • Blachon S, Gopalakrishnan J, Omori Y, Polyanovsky A, Church A, Nicastro D, Malicki J, Avidor-Reiss T (2008) Drosophila asterless and vertebrate Cep152 Are orthologs essential for centriole duplication. Genetics 180:2081–2094

    PubMed  CAS  Google Scholar 

  • Bonaccorsi S, Giansanti MG, Gatti M (1998) Spindle self-organization and cytokinesis during male meiosis in asterless mutants of Drosophila melanogaster. J Cell Biol 142:751–761

    PubMed  CAS  Google Scholar 

  • Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, Higgins J, Hampshire DJ, Morrison EE, Leal GF, Silva EO et al (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37:353–355

    PubMed  CAS  Google Scholar 

  • Butcher RD, Chodagam S, Basto R, Wakefield JG, Henderson DS, Raff JW, Whitfield WG (2004) The Drosophila centrosome-associated protein CP190 is essential for viability but not for cell division. J Cell Sci 117:1191–1199

    PubMed  CAS  Google Scholar 

  • Callaini G, Marchini D (1989) Abnormal centrosomes in cold-treated Drosophila embryos. Exp Cell Res 184:367–374

    PubMed  CAS  Google Scholar 

  • Callaini G, Riparbelli MG (1990) Centriole and centrosome cycle in the early Drosophila embryo. J Cell Sci 97(Pt 3):539–543

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Carvalho-Santos Z, Machado P, Branco P, Tavares-Cadete F, Rodrigues-Martins A, Pereira-Leal JB, Bettencourt-Dias M (2010) Stepwise evolution of the centriole-assembly pathway. J Cell Sci 123:1414–1426

    PubMed  CAS  Google Scholar 

  • Chou TB, Perrimon N (1996) The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144:1673–1679

    PubMed  CAS  Google Scholar 

  • Chung YD, Zhu J, Han Y, Kernan MJ (2001) nompA encodes a PNS-specific, ZP domain protein required to connect mechanosensory dendrites to sensory structures. Neuron 29:415–428

    PubMed  CAS  Google Scholar 

  • Conduit PT, Brunk K, Dobbelaere J, Dix CI, Lucas EP, Raff JW (2010) Centrioles regulate centrosome size by controlling the rate of Cnn incorporation into the PCM. Curr Biol 20:2178–2186

    PubMed  CAS  Google Scholar 

  • Craige B, Tsao CC, Diener DR, Hou Y, Lechtreck KF, Rosenbaum JL, Witman GB (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190:927–940

    PubMed  CAS  Google Scholar 

  • Cunha-Ferreira I, Bento I, Bettencourt-Dias M (2009) From zero to many: control of centriole number in development and disease. Traffic 10:482–498

    PubMed  CAS  Google Scholar 

  • Dammermann A, Muller-Reichert T, Pelletier L, Habermann B, Desai A, Oegema K (2004) Centriole assembly requires both centriolar and pericentriolar material proteins. Dev Cell 7:815–829

    PubMed  CAS  Google Scholar 

  • Delattre M, Gonczy P (2004) The arithmetic of centrosome biogenesis. J Cell Sci 117:1619–1630

    PubMed  CAS  Google Scholar 

  • Dix CI, Raff JW (2007) Drosophila Spd-2 Recruits PCM to the Sperm Centriole, but Is Dispensable for Centriole Duplication. Curr Biol.

    Google Scholar 

  • Dzhindzhev NS, Yu QD, Weiskopf K, Tzolovsky G, Cunha-Ferreira I, Riparbelli M, Rodrigues-Martins A, Bettencourt-Dias M, Callaini G, Glover DM (2010) Asterless is a scaffold for the onset of centriole assembly. Nature 467:714–718

    PubMed  CAS  Google Scholar 

  • Ferree PM, McDonald K, Fasulo B, Sullivan W (2006) The origin of centrosomes in parthenogenetic hymenopteran insects. Curr Biol 16:801–807

    PubMed  CAS  Google Scholar 

  • Fitch KR, Wakimoto BT (1998) The paternal effect gene ms(3)sneaky is required for sperm activation and the initiation of embryogenesis in Drosophila melanogaster. Dev Biol 197:270–282

    PubMed  CAS  Google Scholar 

  • Friedlander M, Wahrman J (1966) Giant centrioles in neuropteran meiosis. J Cell Sci 1:129–144

    PubMed  CAS  Google Scholar 

  • Fritz-Laylin LK, Cande WZ (2010) Ancestral centriole and flagella proteins identified by analysis of Naegleria differentiation. J Cell Sci 123:4024–4031

    PubMed  CAS  Google Scholar 

  • Fukasawa K (2007) Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7:911–924

    PubMed  CAS  Google Scholar 

  • Fuller MT (1993) Spermatogenesis. In: Bate M and Martinez-Arias A (eds) The development of Drosophila melanogaster, Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press), pp. 71–174

    Google Scholar 

  • Fulton C, Dingle AD (1971) Basal bodies, but not centrioles, in Naegleria. J Cell Biol 51:826–836

    PubMed  CAS  Google Scholar 

  • Ganem NJ, Godinho SA, Pellman D (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460:278–282

    PubMed  CAS  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

    Google Scholar 

  • Giansanti MG, Gatti M, Bonaccorsi S (2001) The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development 128:1137–1145

    PubMed  CAS  Google Scholar 

  • Gomes JE, Corado M, Schweisguth F (2009) Van Gogh and Frizzled act redundantly in the Drosophila sensory organ precursor cell to orient its asymmetric division. PLoS ONE 4:e4485

    PubMed  Google Scholar 

  • Gonczy P, Echeverri C, Oegema K, Coulson A, Jones SJ, Copley RR, Duperon J, Oegema J, Brehm M, Cassin E et al (2000) Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408:331–336

    PubMed  CAS  Google Scholar 

  • Gopalakrishnan J, Guichard P, Smith AH, Schwarz H, Agard DA, Marco S, Avidor-Reiss T (2010) Self-assembling SAS-6 multimer is a core centriole building block. J Biol Chem 285:8759–8770

    PubMed  CAS  Google Scholar 

  • Gopalakrishnan J, Mennella V, Blachon S, Zhai B, Smith AH, Megraw TL, Nicastro D, Gygi SP, Agard DA, Avidor-Reiss T (2011) Sas-4 Scaffolds cytoplasmic complexes and tethers them in a centrosome. Nat Commun 2, 359, doi:ncomms1367 [pii] 10.1038/ncomms1367.

  • Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, Vale RD, Stuurman N (2007) Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316:417–421

    PubMed  CAS  Google Scholar 

  • Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7:1140–1146

    PubMed  CAS  Google Scholar 

  • Han YG, Kwok BH, Kernan MJ (2003) Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr Biol 13:1679–1686

    PubMed  CAS  Google Scholar 

  • Heuer JG, Li K, Kaufman TC (1995) The Drosophila homeotic target gene centrosomin (cnn) encodes a novel centrosomal protein with leucine zippers and maps to a genomic region required for midgut morphogenesis. Development 121:3861–3876

    PubMed  CAS  Google Scholar 

  • Hodges ME, Scheumann N, Wickstead B, Langdale JA, Gull K (2010) Reconstructing the evolutionary history of the centriole from protein components. J Cell Sci 123:1407–1413

    PubMed  CAS  Google Scholar 

  • Jaspersen SL, Winey M (2004) The budding yeast spindle pole body: structure, duplication, and function. Annu Rev Cell Dev Biol 20:1–28

    PubMed  CAS  Google Scholar 

  • Jones MH, Winey M (2006) Centrosome duplication: is asymmetry the clue? Curr Biol 16:R808–R810

    PubMed  CAS  Google Scholar 

  • Kalay E, Yigit G, Aslan Y, Brown KE, Pohl E, Bicknell LS, Kayserili H, Li Y, Tuysuz B, Nurnberg G et al (2011) CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat Genet 43:23–26

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Keil TA (1997) Functional morphology of insect mechanoreceptors. Microsc Res Tech 39:506–531

    PubMed  CAS  Google Scholar 

  • Keller LC, Geimer S, Romijn E, Yates J 3rd, Zamora I, Marshall WF (2009) Molecular architecture of the centriole proteome: the conserved WD40 domain protein POC1 is required for centriole duplication and length control. Mol Biol Cell 20:1150–1166

    PubMed  CAS  Google Scholar 

  • Keller LC, Romijn EP, Zamora I, Yates JR 3rd, Marshall WF (2005) Proteomic analysis of isolated chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr Biol 15:1090–1098

    PubMed  CAS  Google Scholar 

  • Kellogg DR, Alberts BM (1992) Purification of a multiprotein complex containing centrosomal proteins from the Drosophila embryo by chromatography with low-affinity polyclonal antibodies. Mol Biol Cell 3:1–11

    PubMed  CAS  Google Scholar 

  • Kellogg DR, Oegema K, Raff J, Schneider K, Alberts BM (1995) CP60: a microtubule-associated protein that is localized to the centrosome in a cell cycle-specific manner. Mol Biol Cell 6:1673–1684

    PubMed  CAS  Google Scholar 

  • Kemp CA, Kopish KR, Zipperlen P, Ahringer J, O’Connell KF (2004) Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2. Dev Cell 6:511–523

    PubMed  CAS  Google Scholar 

  • Kernan M, Cowan D, Zuker C (1994) Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:1195–1206

    PubMed  CAS  Google Scholar 

  • Kilburn CL, Pearson CG, Romijn EP, Meehl JB, Giddings TH Jr, Culver BP, Yates JR 3rd, Winey M (2007) New Tetrahymena basal body protein components identify basal body domain structure. J Cell Biol 178:905–912

    PubMed  CAS  Google Scholar 

  • Kirkham M, Muller-Reichert T, Oegema K, Grill S, Hyman AA (2003) SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112:575–587

    PubMed  CAS  Google Scholar 

  • Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, Bortfeld M, Erat MC, Fluckiger I (2011) Structural basis of the 9-fold summetry of centroiles. Cell 144(3):364–375

    PubMed  CAS  Google Scholar 

  • Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, Nigg EA (2007) Plk4-induced centriole biogenesis in human cells. Dev Cell 13:190–202

    PubMed  CAS  Google Scholar 

  • Krioutchkova MM, Onishchenko GE (1999) Structural and functional characteristics of the centrosome in gametogenesis and early embryogenesis of animals. Int Rev Cytol 185:107–156

    PubMed  CAS  Google Scholar 

  • Leidel S, Delattre M, Cerutti L, Baumer K, Gonczy P (2005) SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat Cell Biol 7:115–125

    PubMed  CAS  Google Scholar 

  • Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, Li H, Blacque OE, Li L, Leitch CC et al (2004) Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117:541–552

    PubMed  CAS  Google Scholar 

  • Li K, Kaufman TC (1996) The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85:585–596

    PubMed  CAS  Google Scholar 

  • Li K, Xu EY, Cecil JK, Turner FR, Megraw TL, Kaufman TC (1998) Drosophila centrosomin protein is required for male meiosis and assembly of the flagellar axoneme. J Cell Biol 141:455–467

    PubMed  CAS  Google Scholar 

  • Loncarek J, Khodjakov A (2009) Ab ovo or de novo? Mechanisms of centriole duplication. Mol Cells 27:135–142

    PubMed  CAS  Google Scholar 

  • Loncarek J, Sluder G, Khodjakov A (2007) Centriole biogenesis: a tale of two pathways. Nat Cell Biol 9:736–738

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Manandhar G, Schatten H, Sutovsky P (2005) Centrosome reduction during gametogenesis and its significance. Biol Reprod 72:2–13

    PubMed  CAS  Google Scholar 

  • Martinez-Campos M, Basto R, Baker J, Kernan M, Raff JW (2004) The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J Cell Biol 165:673–683

    PubMed  CAS  Google Scholar 

  • Matsuura K, Lefebvre PA, Kamiya R, Hirono M (2004) Bld10p, a novel protein essential for basal body assembly in Chlamydomonas: localization to the cartwheel, the first ninefold symmetrical structure appearing during assembly. J Cell Biol 165:663–671

    PubMed  Google Scholar 

  • Megraw TL, Kaufman TC (2000) The centrosome in Drosophila oocyte development. Curr Top Dev Biol 49:385–407

    PubMed  CAS  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 126:2829–2839

    PubMed  CAS  Google Scholar 

  • Moritz M, Braunfeld MB, Sedat JW, Alberts B, Agard DA (1995) Microtubule nucleation by gamma-tubulin-containing rings in the centrosome. Nature 378:638–640

    PubMed  CAS  Google Scholar 

  • Moritz M, Zheng Y, Alberts BM, Oegema K (1998) Recruitment of the gamma-tubulin ring complex to Drosophila salt-stripped centrosome scaffolds. J Cell Biol 142:775–786

    PubMed  CAS  Google Scholar 

  • Mottier-Pavie V, Megraw TL (2009) Drosophila Bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol Biol Cell

    Google Scholar 

  • Nigg EA, Raff JW (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139:663–678

    PubMed  CAS  Google Scholar 

  • Oegema K, Wiese C, Martin OC, Milligan RA, Iwamatsu A, Mitchison TJ, Zheng Y (1999) Characterization of two related Drosophila gamma-tubulin complexes that differ in their ability to nucleate microtubules. J Cell Biol 144:721–733

    PubMed  CAS  Google Scholar 

  • Okada M (1998) Germline cell formation in Drosophila embryogenesis. Genes Genet Syst 73:1–8

    PubMed  CAS  Google Scholar 

  • Oliferenko S, Balasubramanian MK (2002) Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol 4:816–820

    PubMed  CAS  Google Scholar 

  • Omran H (2010) NPHP proteins: gatekeepers of the ciliary compartment. J Cell Biol 190:715–717

    PubMed  CAS  Google Scholar 

  • Pearson CG, Osborn DP, Giddings TH Jr, Beales PL, Winey M (2009) Basal body stability and ciliogenesis requires the conserved component Poc1. J Cell Biol 187:905–920

    PubMed  CAS  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 17:834–843

    PubMed  CAS  Google Scholar 

  • Pelletier L, Ozlu N, Hannak E, Cowan C, Habermann B, Ruer M, Muller-Reichert T, Hyman AA (2004) The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr Biol 14:863–873

    PubMed  CAS  Google Scholar 

  • Phillips DM (1967) Giant centriole formation in Sciara. J Cell Biol 33:73–92

    PubMed  CAS  Google Scholar 

  • Riparbelli MG, Callaini G (2003) Drosophila parthenogenesis: a model for de novo centrosome assembly. Dev Biol 260:298–313

    PubMed  CAS  Google Scholar 

  • Riparbelli MG, Whitfield WG, Dallai R, Callaini G (1997) Assembly of the zygotic centrosome in the fertilized Drosophila egg. Mech Dev 65:135–144

    PubMed  CAS  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 17:1465–1472

    PubMed  CAS  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 316:1046–1050

    PubMed  CAS  Google Scholar 

  • Rosenbaum J (2002) Intraflagellar transport. Curr Biol 12:R125

    PubMed  CAS  Google Scholar 

  • Scholey JM, Anderson KV (2006) Intraflagellar transport and cilium-based signaling. Cell 125:439–442

    PubMed  CAS  Google Scholar 

  • Seidl S (1991) Structure and differentiation of the sensilla of the ventral sensory field on the maxillary palps ofPeriplaneta americana (Insecta, Blattodea), paying special attention to the ciliogenesis of the sensory cells. Zoomorphology 111:35–47

    Google Scholar 

  • Sluder G, Khodjakov A (2010) Centriole duplication: analogue control in a digital age. Cell Biol Int 34:1239–1245

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Stevens NR, Dobbelaere J, Wainman A, Gergely F, Raff JW (2009) Ana3 is a conserved protein required for the structural integrity of centrioles and basal bodies. J Cell Biol 187:355–363

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Stevens NR, Roque H, Raff JW (2010b) DSas-6 and Ana2 Coassemble into Tubules to Promote Centriole Duplication and Engagement. Dev Cell 19:913–919

    PubMed  CAS  Google Scholar 

  • Sun QY, Schatten H (2007) Centrosome inheritance after fertilization and nuclear transfer in mammals. Adv Exp Med Biol 591:58–71

    PubMed  Google Scholar 

  • Tang CJ, Fu RH, Wu KS, Hsu WB, Tang TK (2009) CPAP is a cell-cycle regulated protein that controls centriole length. Nat Cell Biol 11:825–831

    PubMed  CAS  Google Scholar 

  • Tates AD (1971) Cytodifferentiation during Spermatogenesis in Drosophila melanogaster: An Electron Microscope Study. Rijksuniversiteit de Leiden, Leiden

    Google Scholar 

  • Thornton GK, Woods CG (2009) Primary microcephaly: do all roads lead to Rome? Trends Genet 25:501–510

    PubMed  CAS  Google Scholar 

  • Tokuyasu KT (1975) Dynamics of spermiogenesis in Drosophila melanogaster. V. Head-tail alignment. J Ultrastruct Res 50:117–129

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • van Breugel M, Hirono M, Andreeva A, Yanagisawa HA, Yamaguchi S, Nakazawa Y, Morgner N, Petrovich M, Ebong IO, Robinson CV et al (2011) Structures of SAS-6 suggest its organization in centrioles. Science 331:1196–1199

    PubMed  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 17:1735–1745

    PubMed  CAS  Google Scholar 

  • Wakefield JG, Bonaccorsi S, Gatti M (2001) The drosophila protein asp is involved in microtubule organization during spindle formation and cytokinesis. J Cell Biol 153:637–648

    PubMed  CAS  Google Scholar 

  • Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234

    CAS  Google Scholar 

  • Wang Y, Ji P, Liu J, Broaddus RR, Xue F, Zhang W (2009) Centrosome-associated regulators of the G(2)/M checkpoint as targets for cancer therapy. Mol Cancer 8:8

    PubMed  Google Scholar 

  • Whitfield WG, Millar SE, Saumweber H, Frasch M, Glover DM (1988) Cloning of a gene encoding an antigen associated with the centrosome in Drosophila. J Cell Sci 89(Pt 4):467–480

    PubMed  CAS  Google Scholar 

  • Williams CL, Li C, Kida K, Inglis PN, Mohan S, Semenec L, Bialas NJ, Stupay RM, Chen N, Blacque OE et al (2011) MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 192:1023–1041

    PubMed  CAS  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 184:207–221

    PubMed  CAS  Google Scholar 

  • Yamashita YM, Mahowald AP, Perlin JR, Fuller MT (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This material is based upon work supported by the National Science Foundation under Grant No. MCB-1121176. Andrey Polyanovsky was supported by RFBR grant 10-04-01027

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomer Avidor-Reiss .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Humana Press, a part of Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Avidor-Reiss, T., Gopalakrishnan, J., Blachon, S., Polyanovsky, A. (2012). Centriole Duplication and Inheritance in Drosophila melanogaster . In: Schatten, H. (eds) The Centrosome. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-035-9_1

Download citation

Publish with us

Policies and ethics