Dividing the spoils of growth and the cell cycle: The fission yeast as a model for the study of cytokinesis.
Cytokinesis is the final stage of the cell cycle, and ensures completion of both genome segregation and organelle distribution to the daughter cells. Cytokinesis requires the cell to solve a spatial problem (to divide in the correct place, orthogonally to the plane of chromosome segregation) and a temporal problem (to coordinate cytokinesis with mitosis). Defects in the spatiotemporal control of cytokinesis may cause cell death, or increase the risk of tumor formation [Fujiwara et al., 2005 (Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. 2005. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437:1043–1047); reviewed by Ganem et al., 2007 (Ganem NJ, Storchova Z, Pellman D. 2007. Tetraploidy, aneuploidy and cancer. Curr Opin Genet Dev 17:157–162.)]. Asymmetric cytokinesis, which permits the generation of two daughter cells that differ in their shape, size and properties, is important both during development, and for cellular homeostasis in multicellular organisms [reviewed by Li, 2007 (Li R. 2007. Cytokinesis in development and disease: variations on a common theme. Cell Mol Life Sci 64:3044–3058)]. The principal focus of this review will be the mechanisms of cytokinesis in the mitotic cycle of the yeast Schizosaccharomyces pombe. This simple model has contributed significantly to our understanding of how the cell cycle is regulated, and serves as an excellent model for studying aspects of cytokinesis. Here we will discuss the state of our knowledge of how the contractile ring is assembled and disassembled, how it contracts, and what we know of the regulatory mechanisms that control these events and assure their coordination with chromosome segregation.
EPFL SV ISREC UPSIM, SV2.1830, Station 19, CH 1015 Lausanne, Switzerland.
Anupama
A
Goyal
Masak
M
Takaine
Viesturs
V
Simanis
Kentaro
K
Nakano
D020090:Chromosome Segregation / Q000502:physiology*; D015825:Chromosomes, Fungal / Q000502:physiology*; D048749:Cytokinesis / Q000502:physiology*; D008938:Mitosis / Q000502:physiology*; D008954:Models, Biological; D012568:Schizosaccharomyces / Q000502:physiology*
Mol Biol Cell. 2008 Apr;19(4):1727-38
18256290
EMBO J. 2001 Mar 15;20(6):1259-70
11250892
J Cell Biol. 1994 Jun;125(6):1289-301
8207058
PLoS One. 2007 Aug 08;2(8):e696
17684545
J Cell Biol. 1995 Oct;131(1):165-78
7559773
EMBO J. 2009 Oct 21;28(20):3117-31
19713940
Nature. 2005 Oct 13;437(7061):1043-7
16222300
EMBO J. 1996 Dec 2;15(23):6605-16
8978687
J Cell Sci. 2005 Dec 15;118(Pt 24):5731-42
16317047
Nat Rev Cancer. 2007 Mar;7(3):182-91
17318211
Curr Biol. 2005 Apr 26;15(8):724-31
15854904
J Cell Biol. 1997 Jun 16;137(6):1309-19
9182664
Curr Biol. 1999 Jul 29-Aug 12;9(15):849-52
10469572
EMBO Rep. 2009 Feb;10(2):186-91
19098712
Mol Biol Cell. 1993 May;4(5):531-9
8334307
Genes Dev. 1997 Nov 15;11(22):2939-51
9367977
Science. 2002 Jan 25;295(5555):669-71
11809970
Traffic. 2008 Dec;9(12):2089-99
18939956
Nature. 1985 Mar 14-20;314(6007):194-6
2983234
Genes Dev. 1998 Jan 1;12(1):84-94
9420333
J Cell Biol. 2003 Jun 9;161(5):875-87
12796476
J Cell Biol. 2009 Sep 7;186(5):739-53
19736319
Science. 2005 Oct 14;310(5746):310-4
16224022
J Cell Biol. 2003 May 12;161(3):535-45
12732615
PLoS Biol. 2008 Sep 2;6(9):e209
18767903
J Cell Sci. 2001 Dec;114(Pt 24):4521-32
11792817
Genetics. 1998 Jul;149(3):1265-75
9649519
Curr Biol. 2010 Mar 23;20(6):561-6
20226666
Cell Motil Cytoskeleton. 2003 Dec;56(4):207-18
14584023
Curr Biol. 2001 Oct 16;11(20):1559-68
11676915
Curr Biol. 2008 Oct 28;18(20):1594-9
18951025
Cell Cycle. 2009 Nov 15;8(22):3643-7
19844171
Genes Dev. 2009 Jul 15;23(14):1613-8
19605682
Yeast. 2001 Mar 30;18(5):433-44
11255251
Mol Biol Cell. 2005 Sep;16(9):4124-38
15975911
Mol Biol Cell. 2002 Aug;13(8):2963-76
12181359
Trends Microbiol. 2010 Jan;18(1):38-45
19959363
J Cell Sci. 2006 Jul 1;119(Pt 13):2768-79
16772338
Mol Biol Cell. 2006 Apr;17(4):1933-45
16467379
Curr Biol. 1998 May 21;8(11):611-21
9635188
Nature. 2004 Aug 19;430(7002):908-13
15282614
Curr Biol. 2009 Jun 9;19(11):961-6
19427212
J Cell Biol. 2008 Nov 3;183(3):457-70
18955555
Mol Biol Cell. 2008 May;19(5):2328-38
18287523
J Biol Chem. 2003 Aug 29;278(35):33450-5
12807904
Trends Cell Biol. 2005 Aug;15(8):404-13
16009554
Mol Biol Cell. 2001 Dec;12(12):4044-53
11739799
Science. 2001 May 25;292(5521):1502-6
11379633
Curr Biol. 2005 Apr 26;15(8):732-6
15854905
EMBO J. 1996 Oct 1;15(19):5268-79
8895572
Mol Biol Cell. 1998 Nov;9(11):3211-25
9802907
J Cell Sci. 2003 Nov 1;116(Pt 21):4263-75
14514882
J Cell Biol. 1999 Aug 23;146(4):777-90
10459013
Mol Biol Cell. 2005 Jan;16(1):193-201
15496454
Biol Bull. 2000 Oct;199(2):205-6
11081738
J Cell Biol. 2006 Jul 31;174(3):391-402
16864655
J Cell Sci. 2001 Jul;114(Pt 14):2649-64
11683392
Genes Dev. 1996 Nov 1;10(21):2707-19
8946912
J Cell Sci. 1999 Jul;112 ( Pt 14):2313-21
10381387
FEBS Lett. 2001 Nov 9;508(1):136-42
11707284
J Cell Sci. 2000 May;113 ( Pt 10):1695-704
10769201
J Cell Biol. 2000 Aug 7;150(3):539-52
10931866
J Cell Sci. 1989 Dec;94 ( Pt 4):647-56
2630561
Genes Dev. 2004 May 1;18(9):1007-21
15132994
J Cell Biol. 2004 Oct 25;167(2):315-25
15504913
Mol Biol Cell. 2008 Jan;19(1):318-26
17959823
Proc Natl Acad Sci U S A. 2000 May 9;97(10):5249-54
10805785
Genes Cells. 2002 Apr;7(4):365-73
11952833
Science. 2003 Mar 14;299(5613):1743-7
12637748
Curr Opin Cell Biol. 2010 Feb;22(1):50-6
20031383
Fly (Austin). 2009 Jan-Mar;3(1):68-73
19164949
Mol Biol Cell. 1996 Aug;7(8):1259-82
8856669
Trends Cell Biol. 2005 Jan;15(1):10-8
15653073
J Cell Biol. 1980 Aug;86(2):568-75
6995468
Mol Biol Cell. 2008 May;19(5):2208-19
18305104
Cell Cycle. 2006 Jul;5(13):1456-63
16855399
Dev Cell. 2006 Sep;11(3):423-30
16950131
Dev Biol. 2008 Oct 1;322(1):21-32
18662680
J Cell Sci. 2009 Apr 15;122(Pt 8):1071-9
19339546
EMBO J. 2005 Jul 6;24(13):2436-46
15933715
J Cell Biol. 1997 Apr 7;137(1):169-82
9105045
Cell Struct Funct. 2001 Dec;26(6):545-54
11942608
J Biol Chem. 1999 Apr 16;274(16):11339-43
10196225
J Cell Sci. 1997 Jan;110 ( Pt 2):123-37
9044043
Cell Mol Life Sci. 2007 Dec;64(23):3044-58
17882379
Nature. 2005 May 26;435(7041):507-12
15917811
J Cell Sci. 2008 Mar 1;121(Pt 5):601-8
18252797
Biochem Soc Trans. 2008 Jun;36(Pt 3):371-7
18481961
J Cell Biol. 2004 Jun 7;165(5):685-95
15184401
J Ultrastruct Mol Struct Res. 1986 Jan;94(1):92-103
3772181
Int J Mol Sci. 2008 Sep;9(9):1863-1875
19325835
Mol Gen Genet. 1999 Aug;262(1):163-72
10503548
Dev Growth Differ. 1975;17(1):27-38
37282081
Curr Biol. 2009 Dec 15;19(23):R1063-8
20064401
J Cell Sci. 2006 Nov 15;119(Pt 22):4710-8
17077120
Nature. 2002 Sep 5;419(6902):82-6
12214236
J Cell Biol. 2009 Sep 7;186(5):727-38
19720876
Curr Biol. 2001 Jun 26;11(12):931-40
11448769
Science. 2008 Dec 5;322(5907):1543-6
19056985
Cell Biol Int Rep. 1991 Jul;15(7):607-10
1934083
J Cell Sci. 2008 May 15;121(Pt 10):1569-76
18469013
Genes Genet Syst. 1998 Aug;73(4):181-91
9880916
Mol Biol Cell. 1999 Aug;10(8):2771-85
10436027
Mol Biol Cell. 2005 Apr;16(4):2003-17
15689498
J Cell Biol. 1996 Jun;133(6):1307-19
8682866
Mol Biol Cell. 2000 Aug;11(8):2757-73
10930468
J Biol Chem. 2008 Feb 1;283(5):2586-94
18042546
Cell. 2005 Oct 7;123(1):75-87
16213214
Mol Cell. 2010 Jul 9;39(1):86-99
20603077
Proc Natl Acad Sci U S A. 2008 Dec 2;105(48):18942-6
18987308
Eukaryot Cell. 2003 Jun;2(3):510-20
12796296
Nature. 2009 Jun 11;459(7248):852-6
19474792
J Cell Sci. 2008 Mar 15;121(Pt 6):843-53
18303049
Exp Cell Res. 1980 Aug;128(2):407-17
6773789
Curr Biol. 1998 Aug 27;8(17):947-54
9742395
Mol Biol Cell. 2000 Jan;11(1):79-91
10637292
J Cell Biol. 2003 Mar 31;160(7):1083-92
12654901
Mol Biol Cell. 2001 Nov;12(11):3515-26
11694585
Curr Biol. 2008 Mar 11;18(5):322-30
18328707
Genes Dev. 1998 May 1;12(9):1356-70
9573052
Curr Biol. 2002 Dec 23;12(24):2066-75
12498681
PLoS Genet. 2008 Jan;4(1):e17
18225957
J Cell Biol. 1995 Nov;131(4):989-1002
7490299
Nature. 1982 Dec 23;300(5894):706-9
6757758
Cell Motil Cytoskeleton. 2006 Mar;63(3):149-61
16421926
J Cell Sci. 1999 Sep;112 Pt 18:3103-14
10462526
Curr Biol. 2010 Jun 8;20(11):1029-34
20434336
Mol Biol Cell. 2002 Mar;13(3):989-1000
11907277
J Cell Biol. 1993 Nov;123(4):837-48
8227144
Biochem Soc Trans. 2008 Jun;36(Pt 3):411-5
18481970
Mol Biol Cell. 2002 Feb;13(2):515-29
11854409
J Cell Biol. 1998 Sep 7;142(5):1301-12
9732290
Curr Biol. 2001 May 1;11(9):702-7
11369234
J Cell Biol. 2007 Aug 27;178(5):765-71
17724118
EMBO J. 1999 Feb 15;18(4):854-62
10022828
Genetics. 2002 Sep;162(1):45-58
12242222
Curr Biol. 2002 Apr 30;12(9):724-9
12007415
Mol Biol Cell. 1997 Aug;8(8):1461-79
9285819
Nat Cell Biol. 2006 Aug;8(8):891-3
16845379
J Cell Biol. 2008 Dec 15;183(6):979-88
19075108
Curr Opin Genet Dev. 2007 Apr;17(2):157-62
17324569
Nat Rev Mol Cell Biol. 2010 Feb;11(2):149-55
20094054
PLoS Biol. 2009 May 5;7(5):e1000110
19468300
Genes Dev. 2008 Nov 15;22(22):3082-8
19056889
J Cell Sci. 1971 Sep;9(2):475-507
4108061
Annu Rev Genet. 2004;38:203-32
15568976
Nat Cell Biol. 2007 Nov;9(11):1263-72
17952063
J Cell Biol. 1972 May;53(2):419-34
5063470
Mol Biol Cell. 2002 Apr;13(4):1203-14
11950932
J Cell Sci. 2005 May 1;118(Pt 9):1843-50
15827087
Proc Natl Acad Sci U S A. 2008 Jun 10;105(23):8014-9
18523008
EMBO J. 1994 Jul 1;13(13):3011-9
8039497
J Cell Biol. 1998 Oct 19;143(2):415-27
9786952
Biochem Soc Trans. 2008 Jun;36(Pt 3):425-30
18481973
Curr Biol. 2004 Apr 6;14(7):579-84
15062098
Dev Cell. 2002 Dec;3(6):779-90
12479804
Nature. 1987 May 7-13;327(6117):31-5
3553962
Mol Cell Biol. 2001 Oct;21(19):6681-94
11533255
EMBO J. 2010 Feb 3;29(3):546-58
19959995
J Cell Biol. 1996 Mar;132(5):871-85
8603919
Genes Dev. 2009 Mar 15;23(6):660-74
19299557
J Cell Sci Suppl. 1986;5:229-41
3477553
J Cell Sci. 2002 Mar 1;115(Pt 5):887-98
11870208
Phys Biol. 2006 Dec 04;3(4):264-73
17200602
J Cell Biol. 2010 Sep 6;190(5):793-805
20805322
Dev Cell. 2007 Oct;13(4):554-65
17925230
J Bacteriol. 1979 Jan;137(1):440-6
762020
Mol Biol Cell. 2009 Dec;20(24):5195-210
19864459
Curr Biol. 2000 May 18;10(10):619-22
10837231
Genes Dev. 1995 May 1;9(9):1059-73
7744248
Mol Biol Cell. 2006 Jul;17(7):3254-66
16687577
J Biol Chem. 2006 Apr 14;281(15):9935-41
16469735
Biofactors. 2009 Jul-Aug;35(4):338-45
19484742
J Cell Sci. 2000 May;113 ( Pt 10):1813-25
10769212
Mol Biol Cell. 2010 Mar 15;21(6):989-1000
20110347
Genes Dev. 1997 Jun 15;11(12):1519-34
9203579
J Cell Sci. 1984 Jul;69:47-65
6490749
J Cell Sci. 1992 Apr;101 ( Pt 4):801-8
1527180
Genetics. 2001 Aug;158(4):1413-29
11514436
Curr Biol. 2006 Dec 19;16(24):2480-7
17140794
EMBO J. 2005 Sep 7;24(17):3012-25
16096637
J Cell Sci. 1998 Jun;111 ( Pt 12):1635-47
9601094
J Cell Sci. 2004 Aug 1;117(Pt 17):3897-910
15265986
Curr Opin Cell Biol. 1992 Feb;4(1):43-52
1313686
Cell Cycle. 2009 Mar 1;8(5):757-64
19221476
Science. 1967 Jun 2;156(3779):1241-3
6067406
Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7965-70
9223296
Mol Cell. 2006 Oct 6;24(1):13-23
17018289
J Cell Sci. 2000 Apr;113 ( Pt 7):1223-30
10704373
Mol Biol Cell. 2002 Jul;13(7):2448-60
12134082
J Cell Sci. 2005 Sep 15;118(Pt 18):4231-42
16141239
EMBO J. 2000 Apr 17;19(8):1803-15
10775265
FEMS Yeast Res. 2007 Sep;7(6):761-70
17596184
Science. 2003 Jun 6;300(5625):1569-74
12791993
Trends Cell Biol. 2005 May;15(5):277-83
15866032
J Cell Biol. 2003 Mar 31;160(7):1093-103
12668659
Cell Cycle. 2008 Apr 1;7(7):879-84
18414046
Proc Natl Acad Sci U S A. 2005 Jun 7;102(23):8228-32
15928091
Trends Cell Biol. 2005 Nov;15(11):581-8
16209923
J Mol Biol. 1966 Sep;20(2):391-401
5970667
J Cell Biol. 2008 Jul 28;182(2):301-13
18644888
J Cell Sci. 1988 Mar;89 ( Pt 3):343-57
3198697
Dev Cell. 2003 Nov;5(5):723-34
14602073
FEBS Lett. 2005 Nov 21;579(28):6311-6
16256112
Genetics. 2006 Apr;172(4):2101-12
16415366
J Cell Sci. 2003 May 15;116(Pt 10):2073-85
12679387
J Cell Sci. 2002 Dec 1;115(Pt 23):4629-39
12415007
Mol Biol Cell. 2006 Sep;17(9):3793-805
16775007
J Cell Biol. 2006 May 8;173(3):383-94
16651381
J Cell Sci. 1985 Apr;75:357-76
4044680
Science. 2008 Jan 4;319(5859):97-100
18079366
Eur J Cell Biol. 2005 Dec;84(12):915-26
16325501
Dev Cell. 2007 Jun;12(6):987-96
17543869
Nat Biotechnol. 2006 Jul;24(7):841-7
16823372
J Cell Sci. 2004 Oct 15;117(Pt 22):5313-21
15454571
J Cell Biol. 2008 Apr 7;181(1):79-88
18378776
Mol Biol Cell. 2009 Sep;20(17):3941-52
19570908
Curr Biol. 2008 Mar 25;18(6):R247-50
18364227
J Cell Sci. 2000 Jul;113 ( Pt 13):2421-32
10852821
J Cell Biol. 2003 Sep 1;162(5):851-62
12939254
Dev Cell. 2002 Jan;2(1):41-54
11782313
J Cell Sci. 1990 May;96 ( Pt 1):71-7
2197287
J Cell Biol. 1995 Dec;131(5):1243-59
8522587
Mol Biol Cell. 2005 Jul;16(7):3162-75
15857958
J Cell Sci. 1996 Jan;109 ( Pt 1):131-42
8834798
Dev Cell. 2008 May;14(5):646-59
18477449
Annu Rev Biochem. 2006;75:543-66
16756502
Mol Biol Cell. 2007 Aug;18(8):2924-34
17538026
J Cell Biol. 1998 Dec 14;143(6):1603-16
9852154
J Biol Chem. 2001 Jul 27;276(30):28185-9
11384993
Mol Biol Cell. 2005 Oct;16(10):4867-81
16079182
Cell. 1995 Aug 11;82(3):435-44
7634333
Nat Rev Mol Cell Biol. 2001 Nov;2(11):815-26
11715048
J Cell Sci. 1998 Jun;111 ( Pt 12):1603-12
9601091
Nature. 2009 Jun 11;459(7248):857-60
19474789
Eur J Cell Biol. 1998 Aug;76(4):288-95
9765059
Genes Dev. 2008 Nov 15;22(22):3205-16
19056897
EMBO J. 1996 Dec 2;15(23):6438-46
8978671
Mol Biol Cell. 2001 May;12(5):1367-80
11359928
Mol Biol Cell. 2005 Nov;16(11):5346-55
16148042
Mol Biol Cell. 2005 Aug;16(8):3865-72
15944220
J Biol Chem. 2000 May 12;275(19):14381-7
10799520
EMBO J. 1993 Jul;12(7):2697-704
8334988
Curr Biol. 2009 Dec 1;19(22):R1040-2
19948143
J Cell Biol. 1990 Nov;111(5 Pt 1):1905-11
2229180
Bioessays. 2007 Apr;29(4):371-81
17373659