Centriole duplication and inheritance in drosophila melanogaster

The Centrosome: Cell and Molecular Mechanisms of Functions and Dysfunctions in Disease

Volumn , Issue , 2012, Pages 3-31

  Avidor Reiss, T ^a   Gopalakrishnan, J ^a   Blachon, S ^a   Polyanovsky, A ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903385791     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-62703-035-9_1     Document Type: Chapter

References (116)

1. Al-Dosari MS, Shaheen R, Colak D, Alkuraya FS (2010) Novel CENPJ mutation causes Seckel syndrome. J Med Genet 47:411–414
2. Alieva IB, Uzbekov RE (2008) The centrosome is a polyfunctional multiprotein cell complex. Biochemistry (Mosc) 73:626–643
3. 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
4. Anderson RG, Brenner RM (1971) The formation of basal bodies (centrioles) in the Rhesus monkey oviduct. J Cell Biol 50:10–34
5. Avidor-Reiss T (2010) The cellular and developmental program connecting the centrosome and cilium duplication cycle. Semin Cell Dev Biol 21:139–141
6. 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
7. Azimzadeh J, Marshall WF (2010) Building the Centriole. Curr Biol 20:R816–R825
8. 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
9. 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
10. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW (2006) Flies without Centrioles. Cell 125:1375–1386
11. Betleja E, Cole DG (2010) Ciliary trafficking: CEP290 guards a gated community. Curr Biol 20:R928–R931
12. 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
13. 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
14. 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
15. 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
16. 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
17. 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
18. Callaini G, Marchini D (1989) Abnormal centrosomes in cold-treated Drosophila embryos. Exp Cell Res 184:367–374
19. Callaini G, Riparbelli MG (1990) Centriole and centrosome cycle in the early Drosophila embryo. J Cell Sci 97(Pt 3):539–543
20. Callaini G, Riparbelli MG (1996) Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev Biol 176:199–208
21. 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
22. Chou TB, Perrimon N (1996) The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144:1673–1679
23. 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
24. 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
25. 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
26. 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
27. 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
28. Delattre M, Gonczy P (2004) The arithmetic of centrosome biogenesis. J Cell Sci 117:1619–1630
29. Dix CI, Raff JW (2007) Drosophila Spd-2 Recruits PCM to the Sperm Centriole, but Is Dispensable for Centriole Duplication. Curr Biol.
30. 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
31. Ferree PM, McDonald K, Fasulo B, Sullivan W (2006) The origin of centrosomes in parthenogenetic hymenopteran insects. Curr Biol 16:801–807
32. 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
33. Friedlander M, Wahrman J (1966) Giant centrioles in neuropteran meiosis. J Cell Sci 1:129–144
34. Fritz-Laylin LK, Cande WZ (2010) Ancestral centriole and flagella proteins identified by analysis of Naegleria differentiation. J Cell Sci 123:4024–4031
35. Fukasawa K (2007) Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7:911–924
36. 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
37. Fulton C, Dingle AD (1971) Basal bodies, but not centrioles, in Naegleria. J Cell Biol 51:826–836
38. Ganem NJ, Godinho SA, Pellman D (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460:278–282
39. 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
40. Giansanti MG, Gatti M, Bonaccorsi S (2001) The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development 128:1137–1145
41. 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
42. 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
43. 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
44. 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.
45. 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
46. Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7:1140–1146
47. 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
48. 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
49. 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
50. Jaspersen SL, Winey M (2004) The budding yeast spindle pole body: structure, duplication, and function. Annu Rev Cell Dev Biol 20:1–28
51. Jones MH, Winey M (2006) Centrosome duplication: is asymmetry the clue? Curr Biol 16: R808–R810
52. 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
53. Kao LR, Megraw TL (2009) Centrocortin cooperates with centrosomin to organize Drosophila embryonic cleavage furrows. Curr Biol 19:937–942
54. Keil TA (1997) Functional morphology of insect mechanoreceptors. Microsc Res Tech 39:506–531
55. 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
56. 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
57. 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
58. 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
59. 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
60. Kernan M, Cowan D, Zuker C (1994) Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:1195–1206
61. 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
62. 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
63. 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
64. 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
65. 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
66. 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
67. 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
68. Li K, Kaufman TC (1996) The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85:585–596
69. 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
70. Loncarek J, Khodjakov A (2009) Ab ovo or de novo? Mechanisms of centriole duplication. Mol Cells 27:135–142
71. Loncarek J, Sluder G, Khodjakov A (2007) Centriole biogenesis: a tale of two pathways. Nat Cell Biol 9:736–738
72. Mahoney NM, Goshima G, Douglass AD, Vale RD (2006) Making microtubules and mitotic spindles in cells without functional centrosomes. Curr Biol 16:564–569
73. Manandhar G, Schatten H, Sutovsky P (2005) Centrosome reduction during gametogenesis and its significance. Biol Reprod 72:2–13
74. Martinez-Campos M, Basto R, Baker J, Kernan M, Raff JW (2004) The Drosophila pericentrinlike protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J Cell Biol 165:673–683
75. 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
76. Megraw TL, Kaufman TC (2000) The centrosome in Drosophila oocyte development. Curr Top Dev Biol 49:385–407
77. 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
78. 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
79. 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
80. Mottier-Pavie V, Megraw TL (2009) Drosophila Bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol Biol Cell
81. Nigg EA, Raff JW (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139:663–678
82. 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
83. Okada M (1998) Germline cell formation in Drosophila embryogenesis. Genes Genet Syst 73:1–8
84. Oliferenko S, Balasubramanian MK (2002) Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol 4:816–820
85. Omran H (2010) NPHP proteins: gatekeepers of the ciliary compartment. J Cell Biol 190:715–717
86. 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
87. 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
88. 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
89. Phillips DM (1967) Giant centriole formation in Sciara. J Cell Biol 33:73–92
90. Riparbelli MG, Callaini G (2003) Drosophila parthenogenesis: a model for de novo centrosome assembly. Dev Biol 260:298–313
91. Riparbelli MG, Whitfield WG, Dallai R, Callaini G (1997) Assembly of the zygotic centrosome in the fertilized Drosophila egg. Mech Dev 65:135–144
92. 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
93. 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
94. Rosenbaum J (2002) Intraflagellar transport. Curr Biol 12:R125
95. Scholey JM, Anderson KV (2006) Intraflagellar transport and cilium-based signaling. Cell 125:439–442
96. 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
97. Sluder G, Khodjakov A (2010) Centriole duplication: analogue control in a digital age. Cell Biol Int 34:1239–1245
98. 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
99. 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
100. Stevens NR, Raposo AA, Basto R, St Johnston D, Raff JW (2007) From stem cell to embryo without centrioles. Curr Biol 17, 1498–1503
101. 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
102. Sun QY, Schatten H (2007) Centrosome inheritance after fertilization and nuclear transfer in mammals. Adv Exp Med Biol 591:58–71
103. 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
104. Tates AD (1971) Cytodifferentiation during Spermatogenesis in Drosophila melanogaster: An Electron Microscope Study. Rijksuniversiteit de Leiden, Leiden
105. Thornton GK, Woods CG (2009) Primary microcephaly: do all roads lead to Rome? Trends Genet 25:501–510
106. Tokuyasu KT (1975) Dynamics of spermiogenesis in Drosophila melanogaster. V. Head-tail alignment. J Ultrastruct Res 50:117–129
107. Vaizel-Ohayon D, Schejter ED (1999) Mutations in centrosomin reveal requirements for centrosomal function during early Drosophila embryogenesis. Curr Biol 9:889–898
108. 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
109. 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
110. 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
111. Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234
112. 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
113. 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
114. 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
115. 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
116. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521