Inhibitor-3 ensures bipolar mitotic spindle attachment by limiting association of SDS22 with kinetochore-bound protein phosphatase-1

EMBO Journal

Volumn 33, Issue 22, 2014, Pages 2704-2720

  Eiteneuer, Annika ^a   Seiler, Jonas ^a   Weith, Matthias ^a   Beullens, Monique ^b   Lesage, Bart ^b   Krenn, Veronica ^c   Musacchio, Andrea ^a,c   Bollen, Mathieu ^b   Meyer, Hemmo ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

Aurora B; chromosome segregation; kinetochore; mitosis; protein phosphatase 1

Indexed keywords

AURORA B KINASE; INHIBITOR 3; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN INHIBITOR; PROTEIN SDS22; REGULATOR PROTEIN; SURVIVIN; THREONINE; UNCLASSIFIED DRUG; AURKB PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; PPP1R11 PROTEIN, HUMAN; PPP1R7 PROTEIN, HUMAN; SIGNAL PEPTIDE;

ANAPHASE; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CENTROMERE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; IN VITRO STUDY; M PHASE CELL CYCLE CHECKPOINT; METAPHASE; MITOSIS SPINDLE; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; BIOLOGICAL MODEL; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPINDLE APPARATUS;

AURORA KINASE B; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETOCHORES; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; SPINDLE APPARATUS;

EID: 84911408872     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489054     Document Type: Article

References (37)

1. Andrews PD, Ovechkina Y, Morrice N, Wagenbach M, Duncan K, Wordeman L, Swedlow JR, (2004) Aurora B regulates MCAK at the mitotic centromere. Dev Cell 6: 253-268
2. Bharucha JP, Larson JR, Gao L, Daves LK, Tatchell K, (2008) Ypi1, a positive regulator of nuclear protein phosphatase type 1 activity in Saccharomyces cerevisiae. Mol Biol Cell 19: 1032-1045
3. Ceulemans H, Vulsteke V, De Maeyer M, Tatchell K, Stalmans W, Bollen M, (2002) Binding of the concave surface of the Sds22 superhelix to the alpha 4/alpha 5/alpha 6-triangle of protein phosphatase-1. J Biol Chem 277: 47331-47337
4. Cheeseman IM, Anderson S, Jwa M, Green EM, Kang J, Yates JR 3rd, Chan CS, Drubin DG, Barnes G, (2002) Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111: 163-172
5. Ciferri C, Pasqualato S, Screpanti E, Varetti G, Santaguida S, Dos Reis G, Maiolica A, Polka J, De Luca JG, De Wulf P, Salek M, Rappsilber J, Moores CA, Salmon ED, Musacchio A, (2008) Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133: 427-439
6. DeGuzman A, Lee EY, (1988) Preparation of low-molecular-weight forms of rabbit muscle protein phosphatase. Methods Enzymol 159: 356-368
7. Emanuele MJ, Lan W, Jwa M, Miller SA, Chan CS, Stukenberg PT, (2008) Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J Cell Biol 181: 241-254
8. Garcia-Gimeno MA, Munoz I, Arino J, Sanz P, (2003) Molecular characterization of Ypi1, a novel Saccharomyces cerevisiae type 1 protein phosphatase inhibitor. J Biol Chem 278: 47744-47752
9. Heroes E, Lesage B, Gornemann J, Beullens M, Van Meervelt L, Bollen M, (2013) The PP1 binding code: a molecular-lego strategy that governs specificity. FEBS J 280: 584-595
10. Huang HS, Pozarowski P, Gao Y, Darzynkiewicz Z, Lee EY, (2005) Protein phosphatase-1 inhibitor-3 is co-localized to the nucleoli and centrosomes with PP1gamma1 and PP1alpha, respectively. Arch Biochem Biophys 443: 33-44
11. Jagiello I, Van Eynde A, Vulsteke V, Beullens M, Boudrez A, Keppens S, Stalmans W, Bollen M, (2000) Nuclear and subnuclear targeting sequences of the protein phosphatase-1 regulator NIPP1. J Cell Sci 113 (Pt 21): 3761-3768
12. Jiang L, Stanevich V, Satyshur KA, Kong M, Watkins GR, Wadzinski BE, Sengupta R, Xing Y, (2013) Structural basis of protein phosphatase 2A stable latency. Nat Commun 4: 1699
13. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H, (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235-239
14. Kim Y, Holland AJ, Lan W, Cleveland DW, (2010) Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E. Cell 142: 444-455
15. Krenn V, Overlack K, Primorac I, van Gerwen S, Musacchio A, (2013) KI motifs of human Knl1 enhance assembly of comprehensive spindle checkpoint complexes around MELT repeats. Curr Biol 24: 29-39
16. Lampson MA, Renduchitala K, Khodjakov A, Kapoor TM, (2004) Correcting improper chromosome-spindle attachments during cell division. Nat Cell Biol 6: 232-237
17. Lan W, Zhang X, Kline-Smith SL, Rosasco SE, Barrett-Wilt GA, Shabanowitz J, Hunt DF, Walczak CE, Stukenberg PT, (2004) Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr Biol 14: 273-286
18. Lesage B, Beullens M, Pedelini L, Garcia-Gimeno MA, Waelkens E, Sanz P, Bollen M, (2007) A complex of catalytically inactive protein phosphatase-1 sandwiched between Sds22 and inhibitor-3. Biochemistry 46: 8909-8919
19. Liu D, Vleugel M, Backer CB, Hori T, Fukagawa T, Cheeseman IM, Lampson MA, (2010) Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J Cell Biol 188: 809-820
20. Meadows JC, Shepperd LA, Vanoosthuyse V, Lancaster TC, Sochaj AM, Buttrick GJ, Hardwick KG, Millar JB, (2011) Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin-8 motors. Dev Cell 20: 739-750
21. Meyer HH, Shorter JG, Seemann J, Pappin D, Warren G, (2000) A complex of mammalian Ufd1 and Npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. EMBO J 19: 2181-2192
22. Nuytten M, Beke L, Van Eynde A, Ceulemans H, Beullens M, Van Hummelen P, Fuks F, Bollen M, (2008) The transcriptional repressor NIPP1 is an essential player in EZH2-mediated gene silencing. Oncogene 27: 1449-1460
23. Pedelini L, Marquina M, Arino J, Casamayor A, Sanz L, Bollen M, Sanz P, Garcia-Gimeno MA, (2007) YPI1 and SDS22 proteins regulate the nuclear localization and function of yeast type 1 phosphatase Glc7. J Biol Chem 282: 3282-3292
24. Peggie MW, MacKelvie SH, Bloecher A, Knatko EV, Tatchell K, Stark MJ, (2002) Essential functions of Sds22p in chromosome stability and nuclear localization of PP1. J Cell Sci 115: 195-206
25. Pinsky BA, Kotwaliwale CV, Tatsutani SY, Breed CA, Biggins S, (2006) Glc7/protein phosphatase 1 regulatory subunits can oppose the Ipl1/aurora protein kinase by redistributing Glc7. Mol Cell Biol 26: 2648-2660
26. Posch M, Khoudoli GA, Swift S, King EM, Deluca JG, Swedlow JR, (2010) Sds22 regulates aurora B activity and microtubule-kinetochore interactions at mitosis. J Cell Biol 191: 61-74
27. Poser I, Sarov M, Hutchins JR, Heriche JK, Toyoda Y, Pozniakovsky A, Weigl D, Nitzsche A, Hegemann B, Bird AW, Pelletier L, Kittler R, Hua S, Naumann R, Augsburg M, Sykora MM, Hofemeister H, Zhang Y, Nasmyth K, White KP, et al, (2008) BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat Methods 5: 409-415
28. Qian J, Beullens M, Lesage B, Bollen M, (2013) Aurora B defines its own chromosomal targeting by opposing the recruitment of the phosphatase scaffold Repo-Man. Curr Biol 23: 1136-1143
29. Qian J, Lesage B, Beullens M, Van Eynde A, Bollen M, (2011) PP1/Repo-man dephosphorylates mitotic histone H3 at T3 and regulates chromosomal aurora B targeting. Curr Biol 21: 766-773
30. Rosenberg JS, Cross FR, Funabiki H, (2011) KNL1/Spc105 recruits PP1 to silence the spindle assembly checkpoint. Curr Biol 21: 942-947
31. Ruchaud S, Carmena M, Earnshaw WC, (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812
32. Santaguida S, Tighe A, D'Alise AM, Taylor SS, Musacchio A, (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J Cell Biol 190: 73-87
33. Trinkle-Mulcahy L, Andrews PD, Wickramasinghe S, Sleeman J, Prescott A, Lam YW, Lyon C, Swedlow JR, Lamond AI, (2003) Time-lapse imaging reveals dynamic relocalization of PP1gamma throughout the mammalian cell cycle. Mol Biol Cell 14: 107-117
34. Trinkle-Mulcahy L, Lamond AI, (2006) Mitotic phosphatases: no longer silent partners. Curr Opin Cell Biol 18: 623-631
35. Welburn JP, Vleugel M, Liu D, Yates JR 3rd, Lampson MA, Fukagawa T, Cheeseman IM, (2010) Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol Cell 38: 383-392
36. Wurzenberger C, Held M, Lampson MA, Poser I, Hyman AA, Gerlich DW, (2012) Sds22 and Repo-Man stabilize chromosome segregation by counteracting Aurora B on anaphase kinetochores. J Cell Biol 198: 173-183
37. Yamagishi Y, Honda T, Tanno Y, Watanabe Y, (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330: 239-243