Comparative analysis of chromosome segregation in human, yeasts and trypanosome
Received date: 02 Jul 2014
Accepted date: 19 Sep 2014
Published date: 13 Jan 2015
Copyright
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.
Xianxian HAN , Ziyin LI . Comparative analysis of chromosome segregation in human, yeasts and trypanosome[J]. Frontiers in Biology, 2014 , 9(6) : 472 -480 . DOI: 10.1007/s11515-014-1334-y
1 |
Akiyoshi B, Gull K (2013). Evolutionary cell biology of chromosome segregation: insights from trypanosomes. Open Biol, 3(5): 130023
|
2 |
Beckouët 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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
12 |
de Gramont A, Cohen-Fix O (2005). The many phases of anaphase. Trends Biochem Sci, 30(10): 559-568
|
13 |
Ersfeld K, Gull K (1997). Partitioning of large and minichromosomes in Trypanosoma brucei. Science, 276(5312): 611-614
|
14 |
Ersfeld K, Melville S E, Gull K (1999). Nuclear and genome organization of Trypanosoma brucei. Parasitol Today, 15(2): 58-63
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
22 |
Holt L J, Krutchinsky A N, Morgan D O (2008). Positive feedback sharpens the anaphase switch. Nature, 454(7202): 353-357
|
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
|
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
|
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
|
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
|
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
|
28 |
Jäger 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
|
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
|
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
|
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
|
32 |
Kateneva A V, Higgins J M (2009). Shugoshin and PP2A: collaborating to keep chromosomes connected. Dev Cell, 17(3): 303-305
|
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
|
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
|
35 |
Kumar P, Wang C C (2006). Dissociation of cytokinesis initiation from mitotic control in a eukaryote. Eukaryot Cell, 5(1): 92-102
|
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
|
37 |
Li R, Murray A W (1991). Feedback control of mitosis in budding yeast. Cell, 66(3): 519-531
|
38 |
Li Z (2012). Regulation of the cell division cycle in Trypanosoma brucei. Eukaryot Cell, 11(10): 1180-1190
|
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
|
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
|
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
|
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
|
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
|
44 |
Michaelis C, Ciosk R, Nasmyth K (1997). Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell, 91(1): 35-45
|
45 |
Pati D (2008). Oncogenic activity of separase. Cell Cycle, 7(22): 3481-3482
|
46 |
Pei L, Melmed S (1997). Isolation and characterization of a pituitary tumor-transforming gene (PTTG). Mol Endocrinol, 11(4): 433-441
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
54 |
Uhlmann F (2011). Cohesin subunit Rad21L, the new kid on the block has new ideas. EMBO Rep, 12(3): 183-184
|
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
|
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
|
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
|
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
|
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
|
60 |
Vlotides G, Eigler T, Melmed S (2007). Pituitary tumor-transforming gene: physiology and implications for tumorigenesis. Endocr Rev, 28(2): 165-186
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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