The elegans of spindle assembly

Cellular and Molecular Life Sciences

Volumn 67, Issue 13, 2010, Pages 2195-2213

  Müller Reichert, Thomas ^d   Greenan, Garrett ^a   O'Toole, Eileen ^b   Srayko, Martin ^c  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d NONE

Author keywords

3D; Caenorhabditis elegans; Electron tomography; Meiosis; Microtubules; Mitosis; Spindle

Indexed keywords

DNA; GAMMA TUBULIN; ADENOSINE TRIPHOSPHATASE; KATANIN;

ANAPHASE; CAENORHABDITIS ELEGANS; CENTRIOLE; CENTROMERE; CENTROSOME; CHROMOSOME REPLICATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPLASM; DIPLOIDY; ELECTRON TOMOGRAPHY; EMBRYO; FEMALE; FERTILIZATION; HAPLOIDY; IMAGING; LIVE CELL IMAGING; MALE; MEIOSIS; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; NONHUMAN; PROTEIN STRUCTURE; REVIEW; ZYGOTE; ANIMAL; METABOLISM; MICROTUBULE; MITOSIS; PHYSIOLOGY; PRENATAL DEVELOPMENT;

CAENORHABDITIS ELEGANS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CAENORHABDITIS ELEGANS; CENTRIOLES; CENTROSOME; MEIOSIS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS;

EID: 77954051915     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0324-8     Document Type: Review

References (195)

1. Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81:208-219
2. Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, Caprioli RM, Greenstein D (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291:2144-2147
3. Miller MA, Ruest PJ, Kosinski M, Hanks SK, Greenstein D (2003) An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev 17:187-200
4. Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73:304-321
5. Yang HY, McNally K, McNally FJ (2003) MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Dev Biol 260:245-259
6. McNally KL, McNally FJ (2005) Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282:218-230
7. Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1:15-26
8. McNally K, Audhya A, Oegema K, McNally FJ (2006) Katanin controls mitotic and meiotic spindle length. J Cell Biol 175:881-891
9. O'Connell KF, Maxwell KN, White JG (2000) The spd-2 gene is required for polarization of the anteroposterior axis and formation of the sperm asters in the Caenorhabditis elegans zygote. Dev Biol 222:55-70
10. Hamill DR, Severson AF, Carter JC, Bowerman B (2002) Centrosome maturation and mitotic spindle assembly in C. elegans require SPD-5, a protein with multiple coiled-coil domains. Dev Cell 3:673-684
11. Cuenca AA, Schetter A, Aceto D, Kemphues K, Seydoux G (2003) Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130:1255-1265
12. Cowan CR, Hyman AA (2004) Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 431:92-96
13. Sadler PL, Shakes DC (2000) Anucleate Caenorhabditis elegans sperm can crawl, fertilize oocytes and direct anteriorposterior polarization of the 1-cell embryo. Development 127:355-366
14. Gonczy P, Schnabel H, Kaletta T, Amores AD, Hyman T, Schnabel R (1999) Dissection of cell division processes in the one cell stage Caenorhabditis elegans embryo by mutational analysis. J Cell Biol 144:927-946
15. Schmidt DJ, Rose DJ, Saxton WM, Strome S (2005) Functional analysis of cytoplasmic dynein heavy chain in Caenorhabditis elegans with fast-acting temperature-sensitive mutations. Mol Biol Cell 16:1200-1212
16. 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 115:825-836
17. Albertson DG (1984) Formation of the first cleavage spindle in nematode embryos. Dev Biol 101:61-72
18. Galli M, van den Heuvel S (2008) Determination of the cleavage plane in early C. elegans embryos. Annu Rev Genet 42:389-411
19. Merdes A, Cleveland DW (1997) Pathways of spindle pole formation: different mechanisms; conserved components. J Cell Biol 138:953-956
20. Scholey JM, Brust-Mascher I, Mogilner A (2003) Cell division. Nature 422:746-752
21. Lloyd C, Chan J (2006) Not so divided: the common basis of plant and animal cell division. Nat Rev Mol Cell Biol 7:147-152
22. Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237-242
23. Kirschner MW, Mitchison T (1986) Microtubule dynamics. Nature 324:621
24. Howard J, Hyman AA (2009) Growth, fluctuation and switching at microtubule plus ends. Nat Rev Mol Cell Biol 10:569-574
25. Chretien D, Fuller SD, Karsenti E (1995) Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J Cell Biol 129:1311-1328
26. Arnal I, Karsenti E, Hyman AA (2000) Structural transitions at microtubule ends correlate with their dynamic properties in Xenopus egg extracts. J Cell Biol 149:767-774
27. Mandelkow EM, Mandelkow E, Milligan RA (1991) Microtubule dynamics and microtubule caps: a time-resolved cryoelectron microscopy study. J Cell Biol 114:977-991
28. Muller-Reichert T, Chretien D, Severin F, Hyman AA (1998) Structural changes at microtubule ends accompanying GTP hydrolysis: information from a slowly hydrolyzable analogue of GTP, guanylyl (a,b)methylenediphosphonate. Proc Natl Acad Sci USA 95:3661-3666
29. Nogales E, Wolf SG, Downing KH (1997) Visualizing the secondary structure of tubulin: three-dimensional map at 4 A. J Struct Biol 118:119-127
30. Bringmann H, Hyman AA (2005) A cytokinesis furrow is positioned by two consecutive signals. Nature 436:731-734
31. Glotzer M (2005) The molecular requirements for cytokinesis. Science 307:1735-1739
32. Howard J, Hyman AA (2007) Microtubule polymerases and depolymerases. Curr Opin Cell Biol 19:31-35
33. 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 109:2977-2991
34. Shiina N, Moriguchi T, Ohta K, Gotoh Y, Nishida E (1992) Regulation of a major microtubule-associated protein by MPF and MAP kinase. EMBO J 11:3977-3984
35. Gard DL, Kirschner MW (1987) A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105:2203-2215
36. Faruki S, Karsenti E (1994) Purification of microtubule proteins from Xenopus egg extracts: identification of a 230 K MAP4-like protein. Cell Motil Cytoskeleton 28:108-118
37. Andersen SS, Buendia B, Dominguez JE, Sawyer A, Karsenti E (1994) Effect on microtubule dynamics of XMAP230, a microtubule-associated protein present in Xenopus laevis eggs and dividing cells. J Cell Biol 127:1289-1299
38. Andersen SS, Karsenti E (1997) XMAP310: a Xenopus rescuepromoting factor localized to the mitotic spindle. J Cell Biol 139:975-983
39. Hughes JR, Meireles AM, Fisher KH, Garcia A, Antrobus PR, Wainman A, Zitzmann N, Deane C, Ohkura H, Wakefield JG (2008) A microtubule interactome: complexes with roles in cell cycle and mitosis. PLoS Biol 6:e98
40. Amos LA, Schlieper D (2005) Microtubules and maps. Adv Protein Chem 71:257-298
41. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, Howard J, Hyman AA (2008) XMAP215 is a processive microtubule polymerase. Cell 132:79-88
42. Kerssemakers JW, Munteanu EL, Laan L, Noetzel TL, Janson ME, Dogterom M (2006) Assembly dynamics of microtubules at molecular resolution. Nature 442:709-712
43. Slep KC, Vale RD (2007) Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol Cell 27:976-991
44. Matthews LR, Carter P, Thierry-Mieg D, Kemphues K (1998) ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J Cell Biol 141:1159-1168
45. Srayko M, Kaya A, Stamford J, Hyman AA (2005) Identification and characterization of factors required for microtubule growth and nucleation in the early C elegans embryo. Dev Cell 9:223-236
46. Desai A, Verma S, Mitchison TJ, Walczak CE (1999) Kin I kinesins are microtubule-destabilizing enzymes. Cell 96:69-78
47. Moores CA, Milligan RA (2006) Lucky 13-microtubule depolymerisation by kinesin-13 motors. J Cell Sci 119:3905-3913
48. Helenius J, Brouhard G, Kalaidzidis Y, Diez S, Howard J (2006) The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 441:115-119
49. Hunter AW, Caplow M, Coy DL, Hancock WO, Diez S, Wordeman L, Howard J (2003) The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATPhydrolyzing complex at microtubule ends. Mol Cell 11:445-457
50. Mulder AM, Glavis-Bloom A, Moores CA, Wagenbach M, Carragher B, Wordeman L, Milligan RA (2009) A new model for binding of kinesin 13 to curved microtubule protofilaments. J Cell Biol 185:51-57
51. Kline-Smith SL, Khodjakov A, Hergert P, Walczak CE (2004) Depletion of centromeric MCAK leads to chromosome congression and segregation defects due to improper kinetochore attachments. Mol Biol Cell 15:1146-1159
52. Andrews PD, Ovechkina Y, Morrice N, Wagenbach M, Duncan K, Wordeman L, Swedlow JR (2004) Aurora B regulates MCAK at the mitotic centromere. Dev Cell 6:253-268
53. Lan W, Zhang X, Kline-Smith SL, Rosasco SE, Barrett-Wilt GA, Shabanowitz J, Hunt DF, Walczak CE, Stukenberg PT (2004) Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr Biol 14:273-286
54. Knowlton AL, Lan W, Stukenberg PT (2006) Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Curr Biol 16:1705-1710
55. Huang H, Feng J, Famulski J, Rattner JB, Liu ST, Kao GD, Muschel R, Chan GK, Yen TJ (2007) Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. J Cell Biol 177:413-424
56. Bakhoum SF, Genovese G, Compton DA (2009) Deviant kinetochore microtubule dynamics underlie chromosomal instability. Curr Biol 19:1937-1942
57. Schlaitz AL, Srayko M, Dammermann A, Quintin S, Wielsch N, MacLeod I, de Robillard Q, Zinke A, Yates JR III, Muller-Reichert T, Shevchenko A, Oegema K, Hyman AA (2007) The C. elegans RSA complex localizes protein phosphatase 2A to centrosomes and regulates mitotic spindle assembly. Cell 128:115-127
58. Zhang X, Ems-McClung SC, Walczak CE (2008) Aurora A phosphorylates MCAK to control ran-dependent spindle bipolarity. Mol Biol Cell 19:2752-2765
59. Rogers GC, Rogers SL, Schwimmer TA, Ems-McClung SC, Walczak CE, Vale RD, Scholey JM, Sharp DJ (2004) Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature 427:364-370
60. Kinoshita K, Arnal I, Desai A, Drechsel DN, Hyman AA (2001) Reconstitution of physiological microtubule dynamics using purified components. Science 294:1340-1343
61. Bre MH, Kreis TE, Karsenti E (1987) Control of microtubule nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable detyrosinated microtubules. J Cell Biol 105:1283-1296
62. Jaspersen SL, Winey M (2004) The budding yeast spindle pole body: structure, duplication, and function. Annu Rev Cell Dev Biol 20:1-28
63. O'Toole ET, Winey M, McIntosh JR (1999) High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell 10:2017-2031
64. Marshall WF (2007) What is the function of centrioles? J Cell Biochem 100:916-922
65. Azimzadeh J, Bornens M (2007) Structure and duplication of the centrosome. J Cell Sci 120:2139-2142
66. Wolf N, Hirsh D, McIntosh JR (1978) Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63:155-169
67. O'Connell KF, Caron C, Kopish KR, Hurd DD, Kemphues KJ, Li Y, White JG (2001) The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105:547-558
68. Pelletier L, O'Toole E, Schwager A, Hyman AA, Muller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444:619-623
69. Kochanski RS, Borisy GG (1990) Mode of centriole duplication and distribution. J Cell Biol 110:1599-1605
70. Dutcher SK (2003) Long-lost relatives reappear: identification of new members of the tubulin superfamily. Curr Opin Microbiol 6:634-640
71. O'Toole ET, McDonald KL, Mantler J, McIntosh JR, Hyman AA, Muller-Reichert T (2003) Morphologically distinct microtubule ends in the mitotic centrosome of Caenorhabditis elegans. J Cell Biol 163:451-456
72. 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
73. 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
74. 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
75. Leidel S, Gonczy P (2003) SAS-4 is essential for centrosome duplication in C. elegans and is recruited to daughter centrioles once per cell cycle. Dev Cell 4:431-439
76. Delattre M, Leidel S, Wani K, Baumer K, Bamat J, Schnabel H, Feichtinger R, Schnabel R, Gonczy P (2004) Centriolar SAS-5 is required for centrosome duplication in C. elegans. Nat Cell Biol 6:656-664
77. 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
78. 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
79. Dammermann A, Maddox PS, Desai A, Oegema K (2008) SAS-4 is recruited to a dynamic structure in newly forming centrioles that is stabilized by the gamma-tubulin-mediated addition of centriolar microtubules. J Cell Biol 180:771-785
80. Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7:1140-1146
81. 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
82. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW (2006) Flies without centrioles. Cell 125:1375-1386
83. 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
84. Zhu F, Lawo S, Bird A, Pinchev D, Ralph A, Richter C, Muller-Reichert T, Kittler R, Hyman AA, Pelletier L (2008) The mammalian SPD-2 ortholog Cep192 regulates centrosome biogenesis. Curr Biol 18:136-141
85. Rodrigues-Martins A, Bettencourt-Dias M, Riparbelli M, Ferreira C, Ferreira I, Callaini G, Glover DM (2007) DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol 17:1465-1472
86. 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
87. Nakazawa Y, Hiraki M, Kamiya R, Hirono M (2007) SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr Biol 17:2169-2174
88. Yabe T, Ge X, Pelegri F (2007) The zebrafish maternal-effect gene cellular atoll encodes the centriolar component sas-6 and defects in its paternal function promote whole genome duplication. Dev Biol 312:44-60
89. Strnad P, Leidel S, Vinogradova T, Euteneuer U, Khodjakov A, Gonczy P (2007) Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev Cell 13:203-213
90. Tsou MF, Stearns T (2006) Mechanism limiting centrosome duplication to once per cell cycle. Nature 442:947-951
91. Song MH, Aravind L, Muller-Reichert T, O'Connell KF (2008) The conserved protein SZY-20 opposes the Plk4-related kinase ZYG-1 to limit centrosome size. Dev Cell 15:901-912
92. Kemp CA, Song MH, Addepalli MK, Hunter G, O'Connell K (2007) Suppressors of zyg-1 define regulators of centrosome duplication and nuclear association in Caenorhabditis elegans. Genetics 176:95-113
93. Loncarek J, Hergert P, Magidson V, Khodjakov A (2008) Control of daughter centriole formation by the pericentriolar material. Nat Cell Biol 10:322-328
94. Khodjakov A, Rieder CL, Sluder G, Cassels G, Sibon O, Wang CL (2002) De novo formation of centrosomes in vertebrate cells arrested during S phase. J Cell Biol 158:1171-1181
95. Hannak E, Kirkham M, Hyman AA, Oegema K (2001) Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J Cell Biol 155:1109-1116
96. Boxem M, Maliga Z, Klitgord N, Li N, Lemmens I, Mana M, de Lichtervelde L, Mul JD, van de Peut D, Devos M, Simonis N, Yildirim MA, Cokol M, Kao HL, de Smet AS, Wang H, Schlaitz AL, Hao T, Milstein S, Fan C, Tipsword M, Drew K, Galli M, Rhrissorrakrai K, Drechsel D, Koller D, Roth FP, Iakoucheva LM, Dunker AK, Bonneau R, Gunsalus KC, Hill DE, Piano F, Tavernier J, van den Heuvel S, Hyman AA, Vidal M (2008) A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134:534-545
97. Bornens M (2002) Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14:25-34
98. Job D, Valiron O, Oakley B (2003) Microtubule nucleation. Curr Opin Cell Biol 15:111-117
99. Oakley BR (2000) Gamma-tubulin. Curr Top Dev Biol 49:27-54
100. Oakley CE, Oakley BR (1989) Identification of gamma-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338:662-664
101. Gunawardane RN, Martin OC, Cao K, Zhang L, Dej K, Iwamatsu A, Zheng Y (2000) Characterization and reconstitution of Drosophila gamma-tubulin ring complex subunits. J Cell Biol 151:1513-1524
102. Murphy SM, Urbani L, Stearns T (1998) The mammalian gamma-tubulin complex contains homologues of the yeast spindle pole body components spc97p and spc98p. J Cell Biol 141:663-674
103. Hannak E, Oegema K, Kirkham M, Gonczy P, Habermann B, Hyman AA (2002) The kinetically dominant assembly pathway for centrosomal asters in Caenorhabditis elegans is gammatubulin dependent. J Cell Biol 157:591-602
104. 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
105. 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
106. Wiese C, Zheng Y (2000) A new function for the gammatubulin ring complex as a microtubule minus-end cap. Nat Cell Biol 2:358-364
107. Keating TJ, Borisy GG (2000) Immunostructural evidence for the template mechanism of microtubule nucleation. Nat Cell Biol 2:352-357
108. Moritz M, Braunfeld MB, Guenebaut V, Heuser J, Agard DA (2000) Structure of the gamma-tubulin ring complex: a template for microtubule nucleation. Nat Cell Biol 2:365-370
109. Erickson HP, Stoffler D (1996) Protofilaments and rings, two conformations of the tubulin family conserved from bacterial FtsZ to alpha/beta and gamma tubulin. J Cell Biol 135:5-8
110. Zheng Y, Wong ML, Alberts B, Mitchison T (1995) Nucleation of microtubule assembly by a gamma-tubulin-containing ring complex. Nature 378:578-583
111. Byers B, Shriver K, Goetsch L (1978) The role of spindle pole bodies and modified microtubule ends in the initiation of microtubule assembly in Saccharomyces cerevisiae. J Cell Sci 30:331-352
112. Rout MP, Kilmartin JV (1990) Components of the yeast spindle and spindle pole body. J Cell Biol 111:1913-1927
113. Bullitt E, Rout MP, Kilmartin JV, Akey CW (1997) The yeast spindle pole body is assembled around a central crystal of Spc42p. Cell 89:1077-1086
114. 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 130:1149-1159
115. Strome S, Powers J, Dunn M, Reese K, Malone CJ, White J, Seydoux G, Saxton W (2001) Spindle dynamics and the role of gamma-tubulin in early Caenorhabditis elegans embryos. Mol Biol Cell 12:1751-1764
116. Theurkauf WE, Hawley RS (1992) Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J Cell Biol 116:1167-1180
117. Gueth-Hallonet C, Antony C, Aghion J, Santa-Maria A, Lajoie-Mazenc I, Wright M, Maro B (1993) Gamma-Tubulin is present in acentriolar MTOCs during early mouse development. J Cell Sci 105(Pt 1):157-166
118. Sathananthan AH (1997) Mitosis in the human embryo: the vital role of the sperm centrosome (centriole). Histol Histopathol 12:827-856
119. Khodjakov A, Cole RW, Oakley BR, Rieder CL (2000) Centrosome-independent mitotic spindle formation in vertebrates. Curr Biol 10:59-67
120. Tulu US, Rusan NM, Wadsworth P (2003) Peripheral, noncentrosome- associated microtubules contribute to spindle formation in centrosome-containing cells. Curr Biol 13:1894-1899
121. Megraw TL, Kao LR, Kaufman TC (2001) Zygotic development without functional mitotic centrosomes. Curr Biol 11:116-120
122. Rebollo E, Llamazares S, Reina J, Gonzalez C (2004) Contribution of noncentrosomal microtubules to spindle assembly in Drosophila spermatocytes. PLoS Biol 2:E8
123. Moutinho-Pereira S, Debec A, Maiato H (2009) Microtubule cytoskeleton remodeling by acentriolar microtubule-organizing centers at the entry and exit from mitosis in Drosophila somatic cells. Mol Biol Cell 20:2796-2808
124. Hoyer-Fender S (2009) Centriole maturation and transformation to basal body. Semin Cell Dev Biol doi:10.1016/j.semcdb.2009.07.002
125. Ward S, Klass M (1982) The location of the major protein in Caenorhabditis elegans sperm and spermatocytes. Dev Biol 92:203-208
126. Kim DY, Roy R (2006) Cell cycle regulators control centrosome elimination during oogenesis in Caenorhabditis elegans. J Cell Biol 174:751-757
127. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382:420-425
128. Kalab P, Heald R (2008) The RanGTP gradient-a GPS for the mitotic spindle. J Cell Sci 121:1577-1586
129. Bischoff FR, Ponstingl H (1991) Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354:80-82
130. Askjaer P, Galy V, Hannak E, Mattaj IW (2002) Ran GTPase cycle and importins alpha and beta are essential for spindle formation and nuclear envelope assembly in living Caenorhabditis elegans embryos. Mol Biol Cell 13:4355-4370
131. Bamba C, Bobinnec Y, Fukuda M, Nishida E (2002) The GTPase Ran regulates chromosome positioning and nuclear envelope assembly in vivo. Curr Biol 12:503-507
132. Srayko M, O'Toole ET, Hyman AA, Muller-Reichert T (2006) Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr Biol 16:1944-1949
133. Vale RD (1991) Severing of stable microtubules by a mitotically activated protein in Xenopus egg extracts. Cell 64:827-839
134. McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75:419-429
135. Hartman JJ, Mahr J, McNally K, Okawa K, Iwamatsu A, Thomas S, Cheesman S, Heuser J, Vale RD, McNally FJ (1998) Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 93:277-287
136. Clark-Maguire S, Mains PE (1994) mei-1, a gene required for meiotic spindle formation in Caenorhabditis elegans, is a member of a family of ATPases. Genetics 136:533-546
137. Srayko M, Buster DW, Bazirgan OA, McNally FJ, Mains PE (2000) MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev 14:1072-1084
138. Bowerman B, Kurz T (2006) Degrade to create: developmental requirements for ubiquitin-mediated proteolysis during early C. elegans embryogenesis. Development 133:773-784
139. Clark-Maguire S, Mains PE (1994) Localization of the mei-1 gene product of Caenorhaditis elegans, a meiotic-specific spindle component. J Cell Biol 126:199-209
140. Yang G, Houghtaling BR, Gaetz J, Liu JZ, Danuser G, KapoorTM (2007) Architectural dynamics of the meiotic spindle revealed by single-fluorophore imaging. Nat Cell Biol 9:1233-1242
141. Liang ZY, Hallen MA, Endow SA (2009) Mature Drosophila meiosis I spindles comprise microtubules of mixed polarity. Curr Biol 19:163-168
142. Segbert C, Barkus R, Powers J, Strome S, Saxton WM, Bossinger O (2003) KLP-18, a Klp2 kinesin, is required for assembly of acentrosomal meiotic spindles in Caenorhabditis elegans. Mol Biol Cell 14:4458-4469
143. Tournebize R, Andersen SS, Verde F, Doree M, Karsenti E, Hyman AA (1997) Distinct roles of PP1 and PP2A-like phosphatases in control of microtubule dynamics during mitosis. EMBO J 16:5537-5549
144. Gard DL (1992) Microtubule organization during maturation of Xenopus oocytes: assembly and rotation of the meiotic spindles. Dev Biol 151:516-530
145. Walczak CE, Vernos I, Mitchison TJ, Karsenti E, Heald R (1998) A model for the proposed roles of different microtubulebased motor proteins in establishing spindle bipolarity. Curr Biol 8:903-913
146. Walczak CE (2000) Microtubule dynamics and tubulin interacting proteins. Curr Opin Cell Biol 12:52-56
147. Afshar K, Barton NR, Hawley RS, Goldstein LS (1995) DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell 81:129-138
148. Vernos I, Raats J, Hirano T, Heasman J, Karsenti E, Wylie C (1995) Xklp1, a chromosomal Xenopus kinesin-like protein essential for spindle organization and chromosome positioning. Cell 81:117-127
149. Wang SZ, Adler R (1995) Chromokinesin: a DNA-binding, kinesin-like nuclear protein. J Cell Biol 128:761-768
150. Akhmanova A, Hoogenraad CC (2005) Microtubule plus-endtracking proteins: mechanisms and functions. Curr Opin Cell Biol 17:47-54
151. Matthies HJ, McDonald HB, Goldstein LS, Theurkauf WE (1996) Anastral meiotic spindle morphogenesis: role of the nonclaret disjunctional kinesin-like protein. J Cell Biol 134:455-464
152. Herman RK, Madl JE, Kari CK (1979) Duplications in Caenorhabditis elegans. Genetics 92:419-435
153. Monen J, Maddox PS, Hyndman F, Oegema K, Desai A (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7:1248-1255
154. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153:1209-1226
155. Powers J, Rose DJ, Saunders A, Dunkelbarger S, Strome S, Saxton WM (2004) Loss of KLP-19 polar ejection force causes misorientation and missegregation of holocentric chromosomes. J Cell Biol 166:991-1001
156. Wignall SM, Villeneuve AM (2009) Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11:839-844
157. Kashina AS, Baskin RJ, Cole DG, Wedaman KP, Saxton WM, Scholey JM (1996) A bipolar kinesin. Nature 379:270-272
158. Kashina AS, Scholey JM, Leszyk JD, Saxton WM (1996) An essential bipolar mitotic motor. Nature 384:225
159. Saunders AM, Powers J, Strome S, Saxton WM (2007) Kinesin-5 acts as a brake in anaphase spindle elongation. Curr Biol 17:R453-R454
160. Bishop JD, Han Z, Schumacher JM (2005) The Caenorhabditis elegans Aurora B kinase AIR-2 phosphorylates and is required for the localization of a BimC kinesin to meiotic and mitotic spindles. Mol Biol Cell 16:742-756
161. Yang HY, Mains PE, McNally FJ (2005) Kinesin-1 mediates translocation of the meiotic spindle to the oocyte cortex through KCA-1, a novel cargo adapter. J Cell Biol 169:447-457
162. Ellefson ML, McNally FJ (2009) Kinesin-1 and cytoplasmic dynein act sequentially to move the meiotic spindle to the oocyte cortex in Caenorhabditis elegans. Mol Biol Cell 20:2722-2730
163. van der Voet M, Berends CW, Perreault A, Nguyen-Ngoc T, Gonczy P, Vidal M, Boxem M, van den Heuvel S (2009) NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/Galpha. Nat Cell Biol 11:269-277
164. Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484-498
165. Gopalan G, Chan CS, Donovan PJ (1997) A novel mammalian, mitotic spindle-associated kinase is related to yeast and fly chromosome segregation regulators. J Cell Biol 138:643-656
166. Glover DM, Leibowitz MH, McLean DA, Parry H (1995) Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 81:95-105
167. Chan CS, Botstein D (1993) Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics 135:677-691
168. Andrews PD, Knatko E, Moore WJ, Swedlow JR (2003) Mitotic mechanics: the auroras come into view. Curr Opin Cell Biol 15:672-683
169. Schumacher JM, Ashcroft N, Donovan PJ, Golden A (1998) A highly conserved centrosomal kinase, AIR-1, is required for accurate cell cycle progression and segregation of developmental factors in Caenorhabditis elegans embryos. Development 125:4391-4402
170. Schumacher JM, Golden A, Donovan PJ (1998) AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol 143:1635-1646
171. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8:798-812
172. Ozlu N, Srayko M, Kinoshita K, Habermann B, O'Toole ET, Muller-Reichert T, Schmalz N, Desai A, Hyman AA (2005) An essential function of the C. elegans ortholog of TPX2 is to localize activated aurora A kinase to mitotic spindles. Dev Cell 9:237-248
173. Portier N, Audhya A, Maddox PS, Green RA, Dammermann A, Desai A, Oegema K (2007) A microtubule-independent role for centrosomes and aurora a in nuclear envelope breakdown. Dev Cell 12:515-529
174. Barr AR, Gergely F (2007) Aurora-A: the maker and breaker of spindle poles. J Cell Sci 120:2987-2996
175. Groen AC, Cameron LA, Coughlin M, Miyamoto DT, Mitchison TJ, Ohi R (2004) XRHAMM functions in ran-dependent microtubule nucleation and pole formation during anastral spindle assembly. Curr Biol 14:1801-1811
176. Gruss OJ, Carazo-Salas RE, Schatz CA, Guarguaglini G, Kast J, Wilm M, Le Bot N, Vernos I, Karsenti E, Mattaj IW (2001) Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 104:83-93
177. Schatz CA, Santarella R, Hoenger A, Karsenti E, Mattaj IW, Gruss OJ, Carazo-Salas RE (2003) Importin alpha-regulated nucleation of microtubules by TPX2. EMBO J 22:2060-2070
178. Srayko M, Quintin S, Schwager A, Hyman AA (2003) Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Curr Biol 13:1506-1511
179. 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 3:643-649
180. Le Bot N, Tsai MC, Andrews RK, Ahringer J (2003) TAC-1, a regulator of microtubule length in the C. elegans embryo. Curr Biol 13:1499-1505
181. Bellanger JM, Gonczy P (2003) TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr Biol 13:1488-1498
182. 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 156:437-451
183. Wittmann T, Wilm M, Karsenti E, Vernos I (2000) TPX2, A novel Xenopus MAP involved in spindle pole organization. J Cell Biol 149:1405-1418
184. Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD (2008) Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 181:421-429
185. Lawo S, Bashkurov M, Mullin M, Ferreria MG, Kittler R, Habermann B, Tagliaferro A, Poser I, Hutchins JR, Hegemann B, Pinchev D, Buchholz F, Peters JM, Hyman AA, Gingras AC, Pelletier L (2009) HAUS, the 8-subunit human Augmin complex, regulates centrosome and spindle integrity. Curr Biol 19:816-826
186. Dammermann A, Desai A, Oegema K (2003) The minus end in sight. Curr Biol 13:R614-R624
187. Rath U, Rogers GC, Tan D, Gomez-Ferreria MA, Buster DW, Sosa HJ, Sharp DJ (2009) The Drosophila kinesin-13, KLP59D, impacts pacman and flux-based chromosome movement. Mol Biol Cell 20:4696-4705
188. Buster DW, Zhang D, Sharp DJ (2007) Poleward tubulin flux in spindles: regulation and function in mitotic cells. Mol Biol Cell 18:3094-3104
189. Labbe JC, McCarthy EK, Goldstein B (2004) The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J Cell Biol 167:245-256
190. Grill SW, Howard J, Schaffer E, Stelzer EH, Hyman AA (2003) The distribution of active force generators controls mitotic spindle position. Science 301:518-521
191. Kozlowski C, Srayko M, Nedelec F (2007) Cortical microtubule contacts position the spindle in C. elegans embryos. Cell 129:499-510
192. Grill SW, Gonczy P, Stelzer EH, Hyman AA (2001) Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630-633
193. Pecreaux J, Roper JC, Kruse K, Julicher F, Hyman AA, Grill SW, Howard J (2006) Spindle oscillations during asymmetric cell division require a threshold number of active cortical force generators. Curr Biol 16:2111-2122
194. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110-156
195. Sonnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, Alleaume AM, Artelt J, Bettencourt P, Cassin E, Hewitson M, Holz C, Khan M, Lazik S, Martin C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Roder M, Finell J, Hantsch H, Jones SJ, Jones M, Piano F, Gunsalus KC, Oegema K, Gonczy P, Coulson A, Hyman AA, Echeverri CJ (2005) Fullgenome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434:462-469