Inhibition of Polo kinase by BI2536 affects centriole separation during Drosophila male meiosis

Cell Cycle

Volumn 13, Issue 13, 2014, Pages 2064-2263

  Riparbelli, Maria G ^a   Gottardo, Marco ^a   Glover, David M ^b   Callaini, Giuliano ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

BI2536; Centriole disengagement; Centrosome maturation; Drosophila; Gametogenesis; Polo kinase; Spindle assembly

Indexed keywords

4 (8 CYCLOPENTYL 7 ETHYL 5,6,7,8 TETRAHYDRO 5 METHYL 6 OXO 2 PTERIDINYLAMINO) 3 METHOXY N (1 METHYL 4 PIPERIDINYL)BENZAMIDE; GAMMA TUBULIN; POLO LIKE KINASE; DROSOPHILA PROTEIN; POLO PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; PTERIDINE DERIVATIVE; TUBULIN;

ANAPHASE; ANIMAL CELL; ARTICLE; AXONEME; CENTRIOLE; DROSOPHILA; DROSOPHILA STRAIN; GAMETOGENESIS; MALE; MEIOSIS; METAPHASE; MICROTUBULE; NONHUMAN; PROMETAPHASE; PROPHASE; PROTEIN DEGRADATION; SPERMATID; SPERMATOCYTE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHROMATID; CYTOLOGY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; PUPA; ULTRASTRUCTURE;

ANIMALS; AXONEME; CENTRIOLES; CHROMATIDS; DROSOPHILA; DROSOPHILA PROTEINS; MALE; MEIOSIS; PROTEIN-SERINE-THREONINE KINASES; PTERIDINES; PUPA; SPERMATOCYTES; TUBULIN;

EID: 84903759205     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.29083     Document Type: Article

References (66)

1. Sunkel CE, Glover DM. polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J Cell Sci 1988; 89:25-38; PMID:3417791
2. Llamazares S, Moreira A, Tavares A, Girdham C, Spruce BA, Gonzalez C, Karess RE, Glover DM, Sunkel CE. polo encodes a protein kinase homolog required for mitosis in Drosophila. Genes Dev 1991; 5(12A):2153-65; PMID:1660828; http://dx.doi.org/10.1101/gad.5.12a.2153
3. Gonzalez C, Sunkel CE, Glover DM. Interactions between mgr, asp, and polo: asp function modulated by polo and needed to maintain the poles of monopolar and bipolar spindles. Chromosoma 1998; 107:452-60; PMID:9914377; http://dx.doi.org/10.1007/s004120050329
4. Donaldson MM, Tavares AA, Ohkura H, Deak P, Glover DM. Metaphase arrest with centromere separation in polo mutants of Drosophila. J Cell Biol 2001; 153:663-76; PMID:11352929; http://dx.doi.org/10.1083/jcb.153.4.663
5. Carmena M, Riparbelli MG, Minestrini G, Tavares AM, Adams R, Callaini G, Glover DM. Drosophila polo kinase is required for cytokinesis. J Cell Biol 1998; 143:659-71; PMID:9813088; http://dx.doi.org/10.1083/jcb.143.3.659
6. Herrmann S, Amorim I, Sunkel CE. The POLO kinase is required at multiple stages during spermatogenesis in Drosophila melanogaster. Chromosoma 1998; 107:440-51; PMID:9914376
7. Riparbelli MG, Callaini G, Glover DM. Failure of pronuclear migration and repeated divisions of polar body nuclei associated with MTOC defects in polo eggs of Drosophila. J Cell Sci 2000; 113:3341-50; PMID:10954431
8. Barr FA, Silljé HH, Nigg EA. Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 2004; 5:429-40; PMID:15173822; http://dx.doi.org/10.1038/nrm1401
9. Petronczki M, Lénárt P, Peters JM. Polo on the rise-from mitotic entry to cytokinesis with Plk1. Dev Cell 2008; 14:646-59; PMID:18477449; http://dx.doi.org/10.1016/j.devcel.2008.04.014
10. van de Weerdt BC, Medema RH. Polo-like kinases: a team in control of the division. Cell Cycle 2006; 5:853-64; PMID:16627997; http://dx.doi.org/10.4161/ cc.5.8.2692
11. Elez R, Piiper A, Kronenberger B, Kock M, Brendel M, Hermann E, Pliquett U, Neumann E, Zeuzem S. Tumor regression by combination antisense therapy against Plk1 and Bcl-2. Oncogene 2003; 22:69-80; PMID:12527909; http://dx.doi.org/10.1038/sj.onc.1206038
12. Liu X, Lei M, Erikson RL. Normal cells, but not cancer cells, survive severe Plk1 depletion. Mol Cell Biol 2006; 26:2093-108; PMID:16507989; http://dx.doi.org/10.1128/MCB.26.6.2093-2108.2006
13. Spänkuch-Schmitt B, Bereiter-Hahn J, Kaufmann M, Strebhardt K. Effect of RNA silencing of Polo-like kinase-1 (PLK1) on apoptosis and spindle formation in human cancer cells. J Natl Cancer Inst 2002; 94:1863-77; PMID:12488480; http://dx.doi.org/10.1093/jnci/94.24.1863
14. Lane HA, Nigg EA. Antibody microinjection reveals an essential role for human Polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J Cell Biol 1996; 135:1701-13; PMID:8991084; http://dx.doi.org/10. 1083/jcb.135.6.1701
15. Qian YW, Erikson E, Maller JL. Purification and cloning of a protein kinase that phosphorylates and activates the Polo-like kinase Plx1. Science 1998; 282:1701-4; PMID:9831560; http://dx.doi.org/10.1126/science.282.5394.1701
16. Lénárt P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of Polo-like kinase 1. Curr Biol 2007; 17:304-15; PMID:17291761; http://dx.doi.org/10.1016/j.cub.2006.12.046
17. Santamaria A, Neef R, Eberspächer U, Eis K, Husemann M, Mumberg D, Prechtl S, Schulze V, Siemeister G, Wortmann L, et al. Use of the novel Plk1 inhibitor ZK-thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis. Mol Biol Cell 2007; 18:4024-36; PMID:17671160; http://dx.doi.org/10.1091/mbc.E07-05-0517
18. Strebhardt K, Ullrich A. Targeting Polo-like kinase 1 for cancer therapy. Nat Rev Cancer 2006; 6:321-30; PMID:16557283; http://dx.doi.org/10.1038/nrc1841
19. Giménez-Abián JF, Sumara I, Hirota T, Hauf S, Gerlich D, de la Torre C, Ellenberg J, Peters JM. Regulation of sister chromatid cohesion between chromosome arms. Curr Biol 2004; 14:1187-93; PMID:15242616; http://dx.doi.org/10.1016/j.cub.2004.06.052
20. Lu B, Mahmud H, Maass AH, Yu B, van Gilst WH, de Boer RA, Silljé HH. The Plk1 inhibitor BI 2536 temporarily arrests primary cardiac fibroblasts in mitosis and generates aneuploidy in vitro. PLoS One 2010; 5:e12963; PMID:20886032; http://dx.doi.org/10.1371/journal.pone.0012963
21. Steegmaier M, Hoffmann M, Baum A, Lénárt P, Petronczki M, Krssák M, Gürtler U, Garin-Chesa P, Lieb S, Quant J, et al. BI 2536, a potent and selective inhibitor of Polo-like kinase 1, inhibits tumor growth in vivo. Curr Biol 2007; 17:316-22; PMID:17291758; http://dx.doi.org/10.1016/j. cub.2006.12.037
22. Rebollo E, González C. Visualizing the spindle checkpoint in Drosophila spermatocytes. EMBO Rep 2000; 1:65-70; PMID:11256627; http://dx.doi.org/10.1093/embo-reports/kvd011
23. Callaini G, Riparbelli MG. Centriole and centrosome cycle in the early Drosophila embryo. J Cell Sci 1990; 97:539-43; PMID:2127418
24. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW. Flies without centrioles. Cell 2006; 125:1375-86; PMID:16814722; http://dx.doi.org/10.1016/j.cell.2006.05.025
25. Savoian MS, Glover DM. Drosophila Klp67A binds prophase kinetochores to subsequently regulate congression and spindle length. J Cell Sci 2010; 123:767-76; PMID:20144994; http://dx.doi.org/10.1242/jcs.055905
26. Zhang J, Megraw TL. Proper recruitment of gamma-tubulin and D-TACC/Msps to embryonic Drosophila centrosomes requires Centrosomin Motif 1. Mol Biol Cell 2007; 18:4037-49; PMID:17671162; http://dx.doi.org/10.1091/mbc.E07-05-0474
27. Fu J, Glover DM. Structured illumination of the interface between centriole and peri-centriolar material. Open Biol 2012; 2:120104; PMID:22977736; http://dx.doi.org/10.1098/rsob.120104
28. do Carmo Avides M, Tavares A, Glover DM. Polo kinase and Asp are needed to promote the mitotic organizing activity of centrosomes. Nat Cell Biol 2001; 3:421-4; PMID:11283617; http://dx.doi.org/10.1038/35070110
29. Blachon S, Cai X, Roberts KA, Yang K, Polyanovsky A, Church A, Avidor-Reiss T. A proximal centriole-like structure is present in Drosophila spermatids and can serve as a model to study centriole duplication. Genetics 2009; 182:133-44; PMID:19293139; http://dx.doi.org/10.1534/genetics.109.101709
30. Dzhindzhev NS, Yu QD, Weiskopf K, Tzolovsky G, Cunha-Ferreira I, Riparbelli M, Rodrigues-Martins A, Bettencourt-Dias M, Callaini G, Glover DM. Asterless is a scaffold for the onset of centriole assembly. Nature 2010; 467:714-8; PMID:20852615; http://dx.doi.org/10.1038/nature09445
31. Gottardo M, Callaini G, Riparbelli MG. The cilium-like region of the Drosophila spermatocyte: an emerging flagellum? J Cell Sci 2013; 126:5441-52; PMID:24105264; http://dx.doi.org/10.1242/jcs.136523
32. Bettencourt-Dias M, Giet R, Sinka R, Mazumdar A, Lock WG, Balloux F, Zafiropoulos PJ, Yamaguchi S, Winter S, Carthew RW, et al. Genome-wide survey of protein kinases required for cell cycle progression. Nature 2004; 432:980-7; PMID:15616552; http://dx.doi.org/10.1038/nature03160
33. Maiato H, DeLuca J, Salmon ED, Earnshaw WC. The dynamic kinetochore-microtubule interface. J Cell Sci 2004; 117:5461-77; PMID:15509863; http://dx.doi.org/10.1242/jcs.01536
34. Wadsworth P, Khodjakov A. E pluribus unum: towards a universal mechanism for spindle assembly. Trends Cell Biol 2004; 14:413-9; PMID:15308207; http://dx.doi.org/10.1016/j.tcb.2004.07.004
35. Tsou MF, Stearns T. Mechanism limiting centrosome duplication to once per cell cycle. Nature 2006; 442:947-51; PMID:16862117; http://dx.doi.org/10.1038/ nature04985
36. Uhlmann F, Lottspeich F, Nasmyth K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 1999; 400:37-42; PMID:10403247; http://dx.doi.org/10.1038/21831
37. Nasmyth K, Peters JM, Uhlmann F. Splitting the chromosome: cutting the ties that bind sister chromatids. Science 2000; 288:1379-85; PMID:10827941; http://dx.doi.org/10.1126/science.288.5470.1379
38. Guan J, Ekwurtzel E, Kvist U, Yuan L. Cohesin protein SMC1 is a centrosomal protein. Biochem Biophys Res Commun 2008; 372:761-4; PMID:18515072; http://dx.doi.org/10.1016/j.bbrc.2008.05.120
39. Wong RW, Blobel G. Cohesin subunit SMC1 associates with mitotic microtubules at the spindle pole. Proc Natl Acad Sci U S A 2008; 105:15441-5; PMID:18832153; http://dx.doi.org/10.1073/pnas.0807660105
40. Kong X, Ball AR Jr., Sonoda E, Feng J, Takeda S, Fukagawa T, Yen TJ, Yokomori K. Cohesin associates with spindle poles in a mitosis-specific manner and functions in spindle assembly in vertebrate cells. Mol Biol Cell 2009; 20:1289-301; PMID:19116315; http://dx.doi.org/10.1091/mbc.E08-04-0419
41. Nakamura A, Arai H, Fujita N. Centrosomal Aki1 and cohesin function in separase-regulated centriole disengagement. J Cell Biol 2009; 187:607-14; PMID:19948489; http://dx.doi.org/10.1083/jcb.200906019
42. Schvarzstein M, Pattabiraman D, Bembenek JN, Villeneuve AM. Meiotic HORMA domain proteins prevent untimely centriole disengagement during Caenorhabditis elegans spermatocyte meiosis. Proc Natl Acad Sci U S A 2013; 110:E898-907; PMID:23401519; http://dx.doi.org/10.1073/pnas.1213888110
43. Schöckel L, Möckel M, Mayer B, Boos D, Stemmann O. Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat Cell Biol 2011; 13:966-72; PMID:21743463; http://dx.doi.org/10.1038/ncb2280
44. McGuinness BE, Hirota T, Kudo NR, Peters JM, Nasmyth K. Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells. PLoS Biol 2005; 3:e86; PMID:15737064; http://dx.doi.org/10.1371/journal. pbio.0030086
45. Salic A, Waters JC, Mitchison TJ. Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 2004; 118:567-78; PMID:15339662; http://dx.doi.org/10.1016/j.cell.2004.08.016
46. Gregson HC, Schmiesing JA, Kim JS, Kobayashi T, Zhou S, Yokomori K. A potential role for human cohesin in mitotic spindle aster assembly. J Biol Chem 2001; 276:47575-82; PMID:11590136; http://dx.doi.org/10.1074/jbc.M103364200
47. Wang X, Yang Y, Duan Q, Jiang N, Huang Y, Darzynkiewicz Z, Dai W. sSgo1, a major splice variant of Sgo1, functions in centriole cohesion where it is regulated by Plk1. Dev Cell 2008; 14:331-41; PMID:18331714; http://dx.doi.org/ 10.1016/j.devcel.2007.12.007
48. Yamada HY, Yao Y, Wang X, Zhang Y, Huang Y, Dai W, Rao CV. Haploinsufficiency of SGO1 results in deregulated centrosome dynamics, enhanced chromosomal instability and colon tumorigenesis. Cell Cycle 2012; 11:479-88; PMID:22262168; http://dx.doi.org/10.4161/cc.11.3.18994
49. Ricke RM, Jeganathan KB, Malureanu L, Harrison AM, van Deursen JM. Bub1 kinase activity drives error correction and mitotic checkpoint control but not tumor suppression. J Cell Biol 2012; 199:931-49; PMID:23209306; http://dx.doi.org/10.1083/jcb.201205115
50. Warren WD, Steffensen S, Lin E, Coelho P, Loupart M, Cobbe N, Lee JY, McKay MJ, Orr-Weaver T, Heck MM, et al. The Drosophila RAD21 cohesin persists at the centromere region in mitosis. Philos Trans R Soc Lond B Biol Sci 2005; 360:543-52; PMID:15915585
51. Lee JY, Hayashi-Hagihara A, Orr-Weaver TL. Roles and regulation of the Drosophila centromere cohesion protein MEI-S332 family. J Cell Sci •••; 200:733-42
52. Clarke AS, Tang TT, Ooi DL, Orr-Weaver TL. POLO kinase regulates the Drosophila centromere cohesion protein MEI-S332. Dev Cell 2005; 8:53-64; PMID:15621529; http://dx.doi.org/10.1016/j.devcel.2004.12.003
53. Oliveira RA, Nasmyth K. Cohesin cleavage is insufficient for centriole disengagement in Drosophila. Curr Biol 2013; 23:R601-3; PMID:23885871; http://dx.doi.org/10.1016/j.cub.2013.04.003
54. Pandey R, Heidmann S, Lehner CF. Epithelial reorganization and dynamics of progression through mitosis in Drosophila separase complex mutants. J Cell Sci 2005; 118:733-42; PMID:15671062; http://dx.doi.org/10.1242/jcs.01663
55. Matsuo K, Ohsumi K, Iwabuchi M, Kawamata T, Ono Y, Takahashi M. Kendrin is a novel substrate for separase involved in the licensing of centriole duplication. Curr Biol 2012; 22:915-21; PMID:22542101; http://dx.doi.org/10. 1016/j.cub.2012.03.048
56. Lee K, Rhee K. Separase-dependent cleavage of pericentrin B is necessary and sufficient for centriole disengagement during mitosis. Cell Cycle 2012; 11:2476-85; PMID:22722493; http://dx.doi.org/10.4161/cc.20878
57. Martinez-Campos M, Basto R, Baker J, Kernan M, Raff JW. The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J Cell Biol 2004; 165:673-83; PMID:15184400; http://dx.doi.org/10.1083/jcb.200402130
58. Tsou MF, Wang WJ, George KA, Uryu K, Stearns T, Jallepalli PV. Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev Cell 2009; 17:344-54; PMID:19758559; http://dx.doi.org/10.1016/ j.devcel.2009.07.015
59. Cabral G, Sans SS, Cowan CR, Dammermann A. Multiple mechanisms contribute to centriole separation in C. elegans. Curr Biol 2013; 23:1380-7; PMID:23885867; http://dx.doi.org/10.1016/j.cub.2013.06.043
60. Sumara I, Vorlaufer E, Stukenberg PT, Kelm O, Redemann N, Nigg EA, Peters JM. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 2002; 9:515-25; PMID:11931760; http://dx.doi.org/10. 1016/S1097-2765(02)00473-2
61. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 2005; 3:e69; PMID:15737063; http://dx.doi.org/10.1371/journal.pbio.0030069
62. Nakajima M, Kumada K, Hatakeyama K, Noda T, Peters JM, Hirota T. The complete removal of cohesin from chromosome arms depends on separase. J Cell Sci 2007; 120:4188-96; PMID:18003702; http://dx.doi.org/10.1242/jcs.011528
63. Stevens NR, Roque H, Raff JW. DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev Cell 2010; 19:913-9; PMID:21145506; http://dx.doi.org/10.1016/j.devcel.2010.11.010
64. Baker JD, Adhikarakunnathu S, Kernan MJ. Mechanosensory-defective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila. Development 2004; 131:3411-22; PMID:15226257; http://dx.doi.org/10.1242/dev.01229
65. Vaizel-Ohayon D, Schejter ED. Mutations in centrosomin reveal requirements for centrosomal function during early Drosophila embryogenesis. Curr Biol 1999; 9:889-98; PMID:10469591; http://dx.doi.org/10.1016/S0960- 9822(99)80393-5
66. Saunders RD, Avides MC, Howard T, Gonzalez C, Glover DM. The Drosophila gene abnormal spindle encodes a novel microtubule-associated protein that associates with the polar regions of the mitotic spindle. J Cell Biol 1997; 137:881-90; PMID:9151690; http://dx.doi.org/10.1083/jcb.137.4.881