Dissociation of the Nuf2-Ndc80 complex releases centromeres from the spindle-pole body during meiotic prophase in fission yeast.
In the fission yeast Schizosaccharomyces pombe, centromeres remain clustered at the spindle-pole body (SPB) during mitotic interphase. In contrast, during meiotic prophase centromeres dissociate from the SPB. Here we examined the behavior of centromere proteins in living meiotic cells of S. pombe. We show that the Nuf2-Ndc80 complex proteins (Nuf2, Ndc80, Spc24, and Spc25) disappear from the centromere in meiotic prophase when the centromeres are separated from the SPB. The centromere protein Mis12 also dissociates during meiotic prophase; however, Mis6 remains throughout meiosis. When cells are induced to meiosis by inactivation of Pat1 kinase (a key negative regulator of meiosis), centromeres remain associated with the SPB during meiotic prophase. However, inactivation of Nuf2 by a mutation causes the release of centromeres from the SPB in pat1 mutant cells, suggesting that the Nuf2-Ndc80 complex connects centromeres to the SPB. We further found that removal of the Nuf2-Ndc80 complex from the centromere and centromere-SPB dissociation are caused by mating pheromone signaling. Because pat1 mutant cells also show aberrant chromosome segregation in the first meiotic division and this aberration is compensated by mating pheromone signaling, dissociation of the Nuf2-Ndc80 complex may be associated with remodeling of the kinetochore for meiotic chromosome segregation.
Asakawa
Haruhiko
H
Cell Biology Group and CREST Research Project, Kansai Advanced Research Center, National Institute of Information and Communications Technology, Kobe 651-2492, Japan.
Hayashi
Aki
A
Haraguchi
Tokuko
T
Hiraoka
Yasushi
Y
D001483:Base Sequence; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism; D002503:Centromere / Q000378:metabolism; D004271:DNA, Fungal / Q000235:genetics; D004268:DNA-Binding Proteins; D005800:Genes, Fungal; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D018386:Kinetochores / Q000378:metabolism; D008540:Meiosis; D008954:Models, Biological; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism*; D010455:Peptides / Q000378:metabolism; D011418:Prophase; D011993:Recombinant Fusion Proteins / Q000235:genetics / Q000378:metabolism; D012568:Schizosaccharomyces / Q000166:cytology* / Q000235:genetics / Q000378:metabolism*; D029702:Schizosaccharomyces pombe Proteins / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction
D018797:Cell Cycle Proteins; D004271:DNA, Fungal; D004268:DNA-Binding Proteins; C089516:Mating Factor, S pombe; C107314:Mis6 protein, S pombe; D009687:Nuclear Proteins; D010455:Peptides; D011993:Recombinant Fusion Proteins; D029702:Schizosaccharomyces pombe Proteins; C492315:mis12 protein, S pombe; C490196:nuf2 protein, S pombe; D049452:Green Fluorescent Proteins
Mol Biol Cell. 2001 Dec;12(12):3955-72
11739793
Cell. 2004 Sep 17;118(6):715-29
15369671
Genes Dev. 1999 Jul 1;13(13):1664-77
10398680
J Cell Biol. 2004 Feb 16;164(4):535-46
14769859
Cell. 1997 Jul 11;90(1):131-43
9230309
Nat Cell Biol. 2004 Nov;6(11):1135-41
15502821
Dev Cell. 2004 Mar;6(3):329-41
15030757
Mol Biol Cell. 1998 Nov;9(11):3211-25
9802907
Science. 1994 Apr 8;264(5156):270-3
8146661
Curr Biol. 2004 Jan 20;14(2):131-7
14738735
J Biol Chem. 2004 Mar 26;279(13):13076-85
14699129
Chromosoma. 2001 Sep;110(5):322-34
11685532
Science. 2003 Apr 18;300(5618):482-6
12663816
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3752-7
9520439
J Cell Sci. 2004 Aug 1;117(Pt 17):3875-86
15265989
Mol Gen Genet. 1985;198(3):416-21
25864229
Nat Cell Biol. 2003 May;5(5):480-5
12717442
J Cell Biol. 1998 Apr 6;141(1):21-9
9531545
EMBO J. 2003 Jun 2;22(11):2752-63
12773390
Cell Struct Funct. 1999 Oct;24(5):291-8
15216885
J Cell Sci. 2003 Aug 15;116(Pt 16):3347-62
12829748
Genes Cells. 1998 Sep;3(9):587-601
9813109
Nat Cell Biol. 2001 May;3(5):522-6
11331883
Genes Cells. 2004 Aug;9(8):671-84
15298676
J Cell Sci. 2003 Oct 1;116(Pt 19):4035-42
12928332
Curr Biol. 2001 Oct 16;11(20):1618-23
11676924
Cell. 2001 Jul 27;106(2):195-206
11511347
EMBO J. 2003 May 1;22(9):2284-96
12727894
Genes Dev. 2003 Jan 1;17(1):101-14
12514103
EMBO J. 1995 Jul 3;14(13):3094-104
7621824
Nature. 2004 Feb 5;427(6974):510-7
14730319
J Cell Sci. 1988 Mar;89 ( Pt 3):343-57
3198697
J Cell Biol. 2001 Jun 11;153(6):1227-38
11402066
EMBO J. 2001 Feb 15;20(4):777-91
11179222
Curr Genet. 1985;10(4):297-311
3870979
Gene. 1993 Jan 15;123(1):127-30
8422996
Science. 2000 Jun 23;288(5474):2215-9
10864871
J Cell Biol. 2002 Nov 25;159(4):549-55
12438418
Science. 2002 Sep 27;297(5590):2267-70
12351790
Methods Enzymol. 1991;194:795-823
2005825
Nature. 1997 Mar 13;386(6621):187-90
9062192
J Cell Sci. 1998 Mar;111 ( Pt 6):701-12
9471999
J Cell Biol. 2001 Jan 22;152(2):349-60
11266451
Mol Biol Cell. 2001 Sep;12(9):2767-75
11553715
Genes Dev. 2003 Dec 1;17(23):2902-21
14633972
Curr Biol. 2003 Dec 2;13(23):2103-9
14654001