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Comparative analysis of chromosome segregation in human, yeasts and trypanosome |
Xianxian HAN,Ziyin LI() |
Department of Microbiology and Molecular Genetics, University of Texas Medical School, Houston, TX 77030, USA |
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Abstract Chromosome segregation is a tightly regulated process through which duplicated genetic materials are equally partitioned into daughter cells. During the past decades, tremendous efforts have been made to understand the molecular mechanism of chromosome segregation using animals and yeasts as model systems. Recently, new insights into chromosome segregation have gradually emerged using trypanosome, an early branching parasitic protozoan, as a model organism. To uncover the unique aspects of chromosome segregation in trypanosome, which potentially could serve as new drug targets for anti-trypanosome chemotherapy, it is necessary to perform a comparative analysis of the chromosome segregation machinery between trypanosome and its human host. Here, we briefly review the current knowledge about chromosome segregation in human and Trypanosoma brucei, with a focus on the regulation of cohesin and securin degradation triggered by the activation of the anaphase promoting complex/cyclosome (APC/C). We also include yeasts in our comparative analysis since some of the original discoveries were made using budding and fission yeasts as the model organisms and, therefore, these could provide hints about the evolution of the machinery. We highlight both common and unique features in these model systems and also provide perspectives for future research in trypanosome.
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Keywords
cohesin
separase
securin
anaphase promoting complex
spindle assembly checkpoint
Trypanosoma brucei
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Corresponding Author(s):
Ziyin LI
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Just Accepted Date: 09 October 2014
Online First Date: 17 November 2014
Issue Date: 13 January 2015
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1 |
Akiyoshi B, Gull K (2013). Evolutionary cell biology of chromosome segregation: insights from trypanosomes. Open Biol, 3(5): 130023
https://doi.org/10.1098/rsob.130023
pmid: 23635522
|
2 |
Beckou?t F, Hu B, Roig M B, Sutani T, Komata M, Uluocak P, Katis V L, Shirahige K, Nasmyth K (2010). An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol Cell, 39(5): 689-699
https://doi.org/10.1016/j.molcel.2010.08.008
pmid: 20832721
|
3 |
Bessat M, Ersfeld K (2009). Functional characterization of cohesin SMC3 and separase and their roles in the segregation of large and minichromosomes in Trypanosoma brucei. Mol Microbiol, 71(6): 1371-1385
https://doi.org/10.1111/j.1365-2958.2009.06611.x
pmid: 19183276
|
4 |
Bessat M, Knudsen G, Burlingame A L, Wang C C (2013). A minimal anaphase promoting complex/cyclosome (APC/C) in Trypanosoma brucei. PLoS ONE, 8(3): e59258
https://doi.org/10.1371/journal.pone.0059258
pmid: 23533609
|
5 |
Brues A M, Cohen A(1936). Effects of colchicine and related substances on cell division. Biochem J, 30: 1363-1368
|
6 |
Buschhorn B A, Peters J M (2006). How APC/C orders destruction. Nat Cell Biol, 8(3): 209-211
https://doi.org/10.1038/ncb0306-209
pmid: 16508672
|
7 |
Chestukhin A, Pfeffer C, Milligan S, DeCaprio J A, Pellman D (2003). Processing, localization, and requirement of human separase for normal anaphase progression. Proc Natl Acad Sci USA, 100(8): 4574-4579
https://doi.org/10.1073/pnas.0730733100
pmid: 12672959
|
8 |
Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K (2000). Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell, 5(2): 243-254
https://doi.org/10.1016/S1097-2765(00)80420-7
pmid: 10882066
|
9 |
Ciosk R, Zachariae W, Michaelis C, Shevchenko A, Mann M, Nasmyth K (1998). An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell, 93(6): 1067-1076
https://doi.org/10.1016/S0092-8674(00)81211-8
pmid: 9635435
|
10 |
Cohen-Fix O, Peters J M, Kirschner M W, Koshland D (1996). Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev, 10(24): 3081-3093
https://doi.org/10.1101/gad.10.24.3081
pmid: 8985178
|
11 |
da Fonseca P C, Kong E H, Zhang Z, Schreiber A, Williams M A, Morris E P, Barford D (2011). Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature, 470(7333): 274-278
https://doi.org/10.1038/nature09625
pmid: 21107322
|
12 |
de Gramont A, Cohen-Fix O (2005). The many phases of anaphase. Trends Biochem Sci, 30(10): 559-568
https://doi.org/10.1016/j.tibs.2005.08.008
pmid: 16126387
|
13 |
Ersfeld K, Gull K (1997). Partitioning of large and minichromosomes in Trypanosoma brucei. Science, 276(5312): 611-614
https://doi.org/10.1126/science.276.5312.611
pmid: 9110983
|
14 |
Ersfeld K, Melville S E, Gull K (1999). Nuclear and genome organization of Trypanosoma brucei. Parasitol Today, 15(2): 58-63
https://doi.org/10.1016/S0169-4758(98)01378-7
pmid: 10234187
|
15 |
Fernius J, Nerusheva O O, Galander S, Alves F L, Rappsilber J, Marston A L (2013). Cohesin-dependent association of scc2/4 with the centromere initiates pericentromeric cohesion establishment. Curr Biol, 23(7): 599-606
https://doi.org/10.1016/j.cub.2013.02.022
pmid: 23499533
|
16 |
Funabiki H, Yamano H, Kumada K, Nagao K, Hunt T, Yanagida M (1996). Cut2 proteolysis required for sister-chromatid seperation in fission yeast. Nature, 381(6581): 438-441
https://doi.org/10.1038/381438a0
pmid: 8632802
|
17 |
Gluenz E, Sharma R, Carrington M, Gull K (2008). Functional characterization of cohesin subunit SCC1 in Trypanosoma brucei and dissection of mutant phenotypes in two life cycle stages. Mol Microbiol, 69(3): 666-680
https://doi.org/10.1111/j.1365-2958.2008.06320.x
pmid: 18554326
|
18 |
Gorr I H, Boos D, Stemmann O (2005). Mutual inhibition of separase and Cdk1 by two-step complex formation. Mol Cell, 19(1): 135-141
https://doi.org/10.1016/j.molcel.2005.05.022
pmid: 15989971
|
19 |
Gutiérrez-Caballero C, Herrán Y, Sánchez-Martín M, Suja J A, Barbero J L, Llano E, Pendás A M (2011). Identification and molecular characterization of the mammalian α-kleisin RAD21L. Cell Cycle, 10(9): 1477-1487
https://doi.org/10.4161/cc.10.9.15515
pmid: 21527826
|
20 |
Hauf S, Roitinger E, Koch B, Dittrich C M, Mechtler K, Peters J M (2005). Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol, 3(3): e69
https://doi.org/10.1371/journal.pbio.0030069
pmid: 15737063
|
21 |
Heinrich S, Windecker H, Hustedt N, Hauf S (2012). Mph1 kinetochore localization is crucial and upstream in the hierarchy of spindle assembly checkpoint protein recruitment to kinetochores. J Cell Sci, 125(Pt 20): 4720-4727
https://doi.org/10.1242/jcs.110387
pmid: 22825872
|
22 |
Holt L J, Krutchinsky A N, Morgan D O (2008). Positive feedback sharpens the anaphase switch. Nature, 454(7202): 353-357
https://doi.org/10.1038/nature07050
pmid: 18552837
|
23 |
Hornig N C, Knowles P P, McDonald N Q, Uhlmann F (2002). The dual mechanism of separase regulation by securin. Curr Biol, 12(12): 973-982
https://doi.org/10.1016/S0960-9822(02)00847-3
pmid: 12123570
|
24 |
Hoyt M A, Totis L, Roberts B T (1991). S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell, 66(3): 507-517
https://doi.org/10.1016/0092-8674(81)90014-3
pmid: 1651171
|
25 |
Irniger S, Piatti S, Michaelis C, Nasmyth K (1995). Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell, 81(2): 269-278
https://doi.org/10.1016/0092-8674(95)90337-2
pmid: 7736579
|
26 |
Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011). A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep, 12(3): 267-275
https://doi.org/10.1038/embor.2011.2
pmid: 21274006
|
27 |
Ivanov D, Schleiffer A, Eisenhaber F, Mechtler K, Haering C H, Nasmyth K (2002). Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr Biol, 12(4): 323-328
https://doi.org/10.1016/S0960-9822(02)00681-4
pmid: 11864574
|
28 |
J?ger H, Herzig A, Lehner C F, Heidmann S (2001). Drosophila separase is required for sister chromatid separation and binds to PIM and THR. Genes Dev, 15(19): 2572-2584
https://doi.org/10.1101/gad.207301
pmid: 11581162
|
29 |
Jallepalli P V, Waizenegger I C, Bunz F, Langer S, Speicher M R, Peters J M, Kinzler K W, Vogelstein B, Lengauer C (2001). Securin is required for chromosomal stability in human cells. Cell, 105(4): 445-457
https://doi.org/10.1016/S0092-8674(01)00340-3
pmid: 11371342
|
30 |
Jensen S, Segal M, Clarke D J, Reed S I (2001). A novel role of the budding yeast separin Esp1 in anaphase spindle elongation: evidence that proper spindle association of Esp1 is regulated by Pds1. J Cell Biol, 152(1): 27-40
https://doi.org/10.1083/jcb.152.1.27
pmid: 11149918
|
31 |
Kakar S S, Jennes L (1999). Molecular cloning and characterization of the tumor transforming gene (TUTR1): a novel gene in human tumorigenesis. Cytogenet Cell Genet, 84(3-4): 211-216
https://doi.org/10.1159/000015261
pmid: 10393434
|
32 |
Kateneva A V, Higgins J M (2009). Shugoshin and PP2A: collaborating to keep chromosomes connected. Dev Cell, 17(3): 303-305
https://doi.org/10.1016/j.devcel.2009.08.016
pmid: 19758553
|
33 |
King R W, Peters J M, Tugendreich S, Rolfe M, Hieter P, Kirschner M W (1995). A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell, 81(2): 279-288
https://doi.org/10.1016/0092-8674(95)90338-0
pmid: 7736580
|
34 |
Kumada K, Nakamura T, Nagao K, Funabiki H, Nakagawa T, Yanagida M (1998). Cut1 is loaded onto the spindle by binding to Cut2 and promotes anaphase spindle movement upon Cut2 proteolysis. Curr Biol, 8(11): 633-641
https://doi.org/10.1016/S0960-9822(98)70250-7
pmid: 9635190
|
35 |
Kumar P, Wang C C (2006). Dissociation of cytokinesis initiation from mitotic control in a eukaryote. Eukaryot Cell, 5(1): 92-102
https://doi.org/10.1128/EC.5.1.92-102.2006
pmid: 16400171
|
36 |
Lee J, Hirano T (2011). RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol, 192(2): 263-276
https://doi.org/10.1083/jcb.201008005
pmid: 21242291
|
37 |
Li R, Murray A W (1991). Feedback control of mitosis in budding yeast. Cell, 66(3): 519-531
https://doi.org/10.1016/0092-8674(81)90015-5
pmid: 1651172
|
38 |
Li Z (2012). Regulation of the cell division cycle in Trypanosoma brucei. Eukaryot Cell, 11(10): 1180-1190
https://doi.org/10.1128/EC.00145-12
pmid: 22865501
|
39 |
Li Z, Wang C C (2002). Functional characterization of the 11 non-ATPase subunit proteins in the trypanosome 19 S proteasomal regulatory complex. J Biol Chem, 277(45): 42686-42693
https://doi.org/10.1074/jbc.M207183200
pmid: 12213827
|
40 |
Lyons N A, Morgan D O (2011). Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol Cell, 42(3): 378-389
https://doi.org/10.1016/j.molcel.2011.03.023
pmid: 21549314
|
41 |
Matsuo K, Ohsumi K, Iwabuchi M, Kawamata T, Ono Y, Takahashi M (2012). Kendrin is a novel substrate for separase involved in the licensing of centriole duplication. Curr Biol, 22(10): 915-921
https://doi.org/10.1016/j.cub.2012.03.048
pmid: 22542101
|
42 |
Maure J F, Kitamura E, Tanaka T U (2007). Mps1 kinase promotes sister-kinetochore bi-orientation by a tension-dependent mechanism. Curr Biol, 17(24): 2175-2182
https://doi.org/10.1016/j.cub.2007.11.032
pmid: 18060784
|
43 |
McGrew J T, Goetsch L, Byers B, Baum P (1992). Requirement for ESP1 in the nuclear division of Saccharomyces cerevisiae. Mol Biol Cell, 3(12): 1443-1454
https://doi.org/10.1091/mbc.3.12.1443
pmid: 1493337
|
44 |
Michaelis C, Ciosk R, Nasmyth K (1997). Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell, 91(1): 35-45
https://doi.org/10.1016/S0092-8674(01)80007-6
pmid: 9335333
|
45 |
Pati D (2008). Oncogenic activity of separase. Cell Cycle, 7(22): 3481-3482
https://doi.org/10.4161/cc.7.22.7048
pmid: 19001849
|
46 |
Pei L, Melmed S (1997). Isolation and characterization of a pituitary tumor-transforming gene (PTTG). Mol Endocrinol, 11(4): 433-441
https://doi.org/10.1210/mend.11.4.9911
pmid: 9092795
|
47 |
Ploubidou A, Robinson D R, Docherty R C, Ogbadoyi E O, Gull K (1999). Evidence for novel cell cycle checkpoints in trypanosomes: kinetoplast segregation and cytokinesis in the absence of mitosis. J Cell Sci, 112(Pt 24): 4641-4650
pmid: 10574712
|
48 |
Shou W, Seol J H, Shevchenko A, Baskerville C, Moazed D, Chen Z W, Jang J, Shevchenko A, Charbonneau H, Deshaies R J (1999). Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell, 97(2): 233-244
https://doi.org/10.1016/S0092-8674(00)80733-3
pmid: 10219244
|
49 |
Stemmann O, Zou H, Gerber S A, Gygi S P, Kirschner M W (2001). Dual inhibition of sister chromatid separation at metaphase. Cell, 107(6): 715-726
https://doi.org/10.1016/S0092-8674(01)00603-1
pmid: 11747808
|
50 |
Sudakin V, Chan G K, Yen T J (2001). Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol, 154(5): 925-936
https://doi.org/10.1083/jcb.200102093
pmid: 11535616
|
51 |
Sudakin V, Ganoth D, Dahan A, Heller H, Hershko J, Luca F C, Ruderman J V, Hershko A (1995). The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol Biol Cell, 6(2): 185-197
https://doi.org/10.1091/mbc.6.2.185
pmid: 7787245
|
52 |
Sullivan M, Lehane C, Uhlmann F (2001). Orchestrating anaphase and mitotic exit: separase cleavage and localization of Slk19. Nat Cell Biol, 3(9): 771-777
https://doi.org/10.1038/ncb0901-771
pmid: 11533655
|
53 |
Tsou M F, Wang W J, George K A, Uryu K, Stearns T, Jallepalli P V (2009). Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev Cell, 17(3): 344-354
https://doi.org/10.1016/j.devcel.2009.07.015
pmid: 19758559
|
54 |
Uhlmann F (2011). Cohesin subunit Rad21L, the new kid on the block has new ideas. EMBO Rep, 12(3): 183-184
https://doi.org/10.1038/embor.2011.24
pmid: 21311562
|
55 |
Uhlmann F, Lottspeich F, Nasmyth K (1999). Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature, 400(6739): 37-42
https://doi.org/10.1038/21831
pmid: 10403247
|
56 |
Uhlmann F, Wernic D, Poupart M A, Koonin E V, Nasmyth K (2000). Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell, 103(3): 375-386
https://doi.org/10.1016/S0092-8674(00)00130-6
pmid: 11081625
|
57 |
Uzawa S, Samejima I, Hirano T, Tanaka K, Yanagida M (1990). The fission yeast cut1+ gene regulates spindle pole body duplication and has homology to the budding yeast ESP1 gene. Cell, 62(5): 913-925
https://doi.org/10.1016/0092-8674(90)90266-H
pmid: 2203537
|
58 |
Viadiu H, Stemmann O, Kirschner M W, Walz T (2005). Domain structure of separase and its binding to securin as determined by EM. Nat Struct Mol Biol, 12(6): 552-553
https://doi.org/10.1038/nsmb935
pmid: 15880121
|
59 |
Vigneron S, Prieto S, Bernis C, Labbé J C, Castro A, Lorca T (2004). Kinetochore localization of spindle checkpoint proteins: who controls whom? Mol Biol Cell, 15(10): 4584-4596
https://doi.org/10.1091/mbc.E04-01-0051
pmid: 15269280
|
60 |
Vlotides G, Eigler T, Melmed S (2007). Pituitary tumor-transforming gene: physiology and implications for tumorigenesis. Endocr Rev, 28(2): 165-186
https://doi.org/10.1210/er.2006-0042
pmid: 17325339
|
61 |
Waizenegger I, Giménez-Abián J F, Wernic D, Peters J M (2002). Regulation of human separase by securin binding and autocleavage. Curr Biol, 12(16): 1368-1378
https://doi.org/10.1016/S0960-9822(02)01073-4
pmid: 12194817
|
62 |
Weiss E, Winey M (1996). The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol, 132(1-2): 111-123
https://doi.org/10.1083/jcb.132.1.111
pmid: 8567717
|
63 |
Wirth K G, Wutz G, Kudo N R, Desdouets C, Zetterberg A, Taghybeeglu S, Seznec J, Ducos G M, Ricci R, Firnberg N, Peters J M, Nasmyth K (2006). Separase: a universal trigger for sister chromatid disjunction but not chromosome cycle progression. J Cell Biol, 172(6): 847-860
https://doi.org/10.1083/jcb.200506119
pmid: 16533945
|
64 |
Xiong B, Lu S, Gerton J L (2010). Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr Biol, 20(18): 1660-1665
https://doi.org/10.1016/j.cub.2010.08.019
pmid: 20797861
|
65 |
Zhang N, Ge G, Meyer R, Sethi S, Basu D, Pradhan S, Zhao Y J, Li X N, Cai W W, El-Naggar A K, Baladandayuthapani V, Kittrell F S, Rao P H, Medina D, Pati D (2008). Overexpression of Separase induces aneuploidy and mammary tumorigenesis. Proc Natl Acad Sci USA, 105(35): 13033-13038
https://doi.org/10.1073/pnas.0801610105
pmid: 18728194
|
66 |
Zhang X, Horwitz G A, Prezant T R, Valentini A, Nakashima M, Bronstein M D, Melmed S (1999). Structure, expression, and function of human pituitary tumor-transforming gene (PTTG). Mol Endocrinol, 13(1): 156-166
https://doi.org/10.1210/mend.13.1.0225
pmid: 9892021
|
67 |
Zou H, McGarry T J, Bernal T, Kirschner M W (1999). Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science, 285(5426): 418-422
https://doi.org/10.1126/science.285.5426.418
pmid: 10411507
|
68 |
Zou H, Stemman O, Anderson J S, Mann M, Kirschner M W (2002). Anaphase specific auto-cleavage of separase. FEBS Lett, 528(1-3): 246-250
https://doi.org/10.1016/S0014-5793(02)03238-6
pmid: 12297314
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