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Molecular basis for phosphospecific recognition of histone H3 tails by Survivin paralogues at inner centromeres.

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Niedzialkowska E, Wang F, Porebski PJ, Minor W, Higgins JM, Stukenberg PT
OpenAccess logo Mol Biol Cell 23 1457-66 (2012)
Related entries: 3uec, 3ued, 3uee, 3uef, 3ueh, 3uei

Cited: 43 times
EuropePMC logo PMID: 22357620

Abstract

Survivin, a subunit of the chromosome passenger complex (CPC), binds the N-terminal tail of histone H3, which is phosphorylated on T3 by Haspin kinase, and localizes the complex to the inner centromeres. We used x-ray crystallography to determine the residues of Survivin that are important in binding phosphomodified histone H3. Mutation of amino acids that interact with the histone N-terminus lowered in vitro tail binding affinity and reduced CPC recruitment to the inner centromere in cells, validating our solved structures. Phylogenetic analysis shows that nonmammalian vertebrates have two Survivin paralogues, which we name class A and B. A distinguishing feature of these paralogues is an H-to-R change in an amino acid that interacts with the histone T3 phosphate. The binding to histone tails of the human class A paralogue, which has a histidine at this position, is sensitive to changes around physiological pH, whereas Xenopus Survivin class B is less so. Our data demonstrate that Survivin paralogues have different characteristics of phosphospecific binding to threonine-3 of histone H3, providing new insight into the biology of the inner centromere.

Articles - 3ueg mentioned but not cited (3)

  1. Molecular basis for phosphospecific recognition of histone H3 tails by Survivin paralogues at inner centromeres. Niedzialkowska E, Wang F, Porebski PJ, Minor W, Higgins JM, Stukenberg PT. Mol Biol Cell 23 1457-1466 (2012)
  2. Specific inhibition of the Survivin-CRM1 interaction by peptide-modified molecular tweezers. Meiners A, Bäcker S, Hadrović I, Heid C, Beuck C, Ruiz-Blanco YB, Mieres-Perez J, Pörschke M, Grad JN, Vallet C, Hoffmann D, Bayer P, Sánchez-García E, Schrader T, Knauer SK. Nat Commun 12 1505 (2021)
  3. Exploring the nucleotide molecular mechanism of compound kushen injection for lung adenocarcinoma based on network pharmacology and molecular docking. Ye Z, Yao X, Chen Z, Jin Q, You Q. Front Oncol 12 1013052 (2022)


Reviews citing this publication (11)

  1. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Carmena M, Wheelock M, Funabiki H, Earnshaw WC. Nat Rev Mol Cell Biol 13 789-803 (2012)
  2. Perceiving the epigenetic landscape through histone readers. Musselman CA, Lalonde ME, Côté J, Kutateladze TG. Nat Struct Mol Biol 19 1218-1227 (2012)
  3. The Aurora B Kinase in Chromosome Bi-Orientation and Spindle Checkpoint Signaling. Krenn V, Musacchio A. Front Oncol 5 225 (2015)
  4. Histone modifications and mitosis: countermarks, landmarks, and bookmarks. Wang F, Higgins JM. Trends Cell Biol 23 175-184 (2013)
  5. Kinase and Phosphatase Cross-Talk at the Kinetochore. Saurin AT. Front Cell Dev Biol 6 62 (2018)
  6. The Ins and Outs of Aurora B Inner Centromere Localization. Hindriksen S, Lens SMA, Hadders MA. Front Cell Dev Biol 5 112 (2017)
  7. A Centromere-Signaling Network Underlies the Coordination among Mitotic Events. Trivedi P, Stukenberg PT. Trends Biochem Sci 41 160-174 (2016)
  8. Survivin in autoimmune diseases. Gravina G, Wasén C, Garcia-Bonete MJ, Turkkila M, Erlandsson MC, Töyrä Silfverswärd S, Brisslert M, Pullerits R, Andersson KM, Katona G, Bokarewa MI. Autoimmun Rev 16 845-855 (2017)
  9. IAPs: Modular regulators of cell signalling. Budhidarmo R, Day CL. Semin Cell Dev Biol 39 80-90 (2015)
  10. A Condensed View of the Chromosome Passenger Complex. Trivedi P, Stukenberg PT. Trends Cell Biol 30 676-687 (2020)
  11. Establishing correct kinetochore-microtubule attachments in mitosis and meiosis. Cairo G, Lacefield S. Essays Biochem 64 277-287 (2020)

Articles citing this publication (29)

  1. Haspin inhibitors reveal centromeric functions of Aurora B in chromosome segregation. Wang F, Ulyanova NP, Daum JR, Patnaik D, Kateneva AV, Gorbsky GJ, Higgins JM. J Cell Biol 199 251-268 (2012)
  2. A small-molecule inhibitor of Haspin alters the kinetochore functions of Aurora B. De Antoni A, Maffini S, Knapp S, Musacchio A, Santaguida S. J Cell Biol 199 269-284 (2012)
  3. HELLS and CDCA7 comprise a bipartite nucleosome remodeling complex defective in ICF syndrome. Jenness C, Giunta S, Müller MM, Kimura H, Muir TW, Funabiki H. Proc Natl Acad Sci U S A 115 E876-E885 (2018)
  4. Polo-like kinase-1 triggers histone phosphorylation by Haspin in mitosis. Zhou L, Tian X, Zhu C, Wang F, Higgins JM. EMBO Rep 15 273-281 (2014)
  5. Characterizing metal-binding sites in proteins with X-ray crystallography. Handing KB, Niedzialkowska E, Shabalin IG, Kuhn ML, Zheng H, Minor W. Nat Protoc 13 1062-1090 (2018)
  6. The inner centromere is a biomolecular condensate scaffolded by the chromosomal passenger complex. Trivedi P, Palomba F, Niedzialkowska E, Digman MA, Gratton E, Stukenberg PT. Nat Cell Biol 21 1127-1137 (2019)
  7. Untangling the contribution of Haspin and Bub1 to Aurora B function during mitosis. Hadders MA, Hindriksen S, Truong MA, Mhaskar AN, Wopken JP, Vromans MJM, Lens SMA. J Cell Biol 219 e201907087 (2020)
  8. EB1 enables spindle microtubules to regulate centromeric recruitment of Aurora B. Banerjee B, Kestner CA, Stukenberg PT. J Cell Biol 204 947-963 (2014)
  9. The N-Terminal Non-Kinase-Domain-Mediated Binding of Haspin to Pds5B Protects Centromeric Cohesion in Mitosis. Zhou L, Liang C, Chen Q, Zhang Z, Zhang B, Yan H, Qi F, Zhang M, Yi Q, Guan Y, Xiang X, Zhang X, Ye S, Wang F. Curr Biol 27 992-1004 (2017)
  10. Phosphorylation of threonine 3 on histone H3 by haspin kinase is required for meiosis I in mouse oocytes. Nguyen AL, Gentilello AS, Balboula AZ, Shrivastava V, Ohring J, Schindler K. J Cell Sci 127 5066-5078 (2014)
  11. RecQL4 helicase amplification is involved in human breast tumorigenesis. Fang H, Nie L, Chi Z, Liu J, Guo D, Lu X, Hei TK, Balajee AS, Zhao Y. PLoS One 8 e69600 (2013)
  12. Centromere-localized Aurora B kinase is required for the fidelity of chromosome segregation. Liang C, Zhang Z, Chen Q, Yan H, Zhang M, Zhou L, Xu J, Lu W, Wang F. J Cell Biol 219 e201907092 (2020)
  13. A kinase-dependent role for Haspin in antagonizing Wapl and protecting mitotic centromere cohesion. Liang C, Chen Q, Yi Q, Zhang M, Yan H, Zhang B, Zhou L, Zhang Z, Qi F, Ye S, Wang F. EMBO Rep 19 43-56 (2018)
  14. Borealin-nucleosome interaction secures chromosome association of the chromosomal passenger complex. Abad MA, Ruppert JG, Buzuk L, Wear M, Zou J, Webb KM, Kelly DA, Voigt P, Rappsilber J, Earnshaw WC, Jeyaprakash AA. J Cell Biol 218 3912-3925 (2019)
  15. Chromatin condensation and recruitment of PHD finger proteins to histone H3K4me3 are mutually exclusive. Gatchalian J, Gallardo CM, Shinsky SA, Ospina RR, Liendo AM, Krajewski K, Klein BJ, Andrews FH, Strahl BD, M van Wely KH, Kutateladze TG. Nucleic Acids Res 44 6102-6112 (2016)
  16. Aurora A-dependent CENP-A phosphorylation at inner centromeres protects bioriented chromosomes against cohesion fatigue. Eot-Houllier G, Magnaghi-Jaulin L, Fulcrand G, Moyroud FX, Monier S, Jaulin C. Nat Commun 9 1888 (2018)
  17. Functional Disruption of the Cancer-Relevant Interaction between Survivin and Histone H3 with a Guanidiniocarbonyl Pyrrole Ligand. Vallet C, Aschmann D, Beuck C, Killa M, Meiners A, Mertel M, Ehlers M, Bayer P, Schmuck C, Giese M, Knauer SK. Angew Chem Int Ed Engl 59 5567-5571 (2020)
  18. Molecular basis of MKLP2-dependent Aurora B transport from chromatin to the anaphase central spindle. Serena M, Bastos RN, Elliott PR, Barr FA. J Cell Biol 219 e201910059 (2020)
  19. Differential requirement for Bub1 and Bub3 in regulation of meiotic versus mitotic chromosome segregation. Cairo G, MacKenzie AM, Lacefield S. J Cell Biol 219 e201909136 (2020)
  20. Genome-wide CRISPR screen uncovers a synergistic effect of combining Haspin and Aurora kinase B inhibition. Huang M, Feng X, Su D, Wang G, Wang C, Tang M, Paulucci-Holthauzen A, Hart T, Chen J. Oncogene 39 4312-4322 (2020)
  21. Molecular structures guide the engineering of chromatin. Tekel SJ, Haynes KA. Nucleic Acids Res 45 7555-7570 (2017)
  22. The Borealin dimerization domain interacts with Sgo1 to drive Aurora B-mediated spindle assembly. Bonner MK, Haase J, Saunders H, Gupta H, Li BI, Kelly AE. Mol Biol Cell 31 2207-2218 (2020)
  23. Switching of INCENP paralogs controls transitions in mitotic chromosomal passenger complex functions. Feng H, Raasholm M, Moosmann A, Campsteijn C, Thompson EM. Cell Cycle 18 2006-2025 (2019)
  24. Mechanistic basis for Sgo1-mediated centromere localization and function of the CPC. Abad MA, Gupta T, Hadders MA, Meppelink A, Wopken JP, Blackburn E, Zou J, Gireesh A, Buzuk L, Kelly DA, McHugh T, Rappsilber J, Lens SMA, Jeyaprakash AA. J Cell Biol 221 e202108156 (2022)
  25. Nucleosome-Dependent Pathways That Control Mitotic Progression. Funabiki H, Jenness C, Zierhut C. Cold Spring Harb Symp Quant Biol 82 173-185 (2017)
  26. Structure of the pre-mRNA leakage 39-kDa protein reveals a single domain of integrated zf-C3HC and Rsm1 modules. Hashimoto H, Ramirez DH, Lautier O, Pawlak N, Blobel G, Palancade B, Debler EW. Sci Rep 12 17691 (2022)
  27. Histone Readers and Their Roles in Cancer. Wen H, Shi X. Cancer Treat Res 190 245-272 (2023)
  28. Survivin prevents the polycomb repressor complex 2 from methylating histone 3 lysine 27. Jensen M, Chandrasekaran V, García-Bonete MJ, Li S, Anindya AL, Andersson K, Erlandsson MC, Oparina NY, Burmann BM, Brath U, Panchenko AR, Bokarewa I M, Katona G. iScience 26 106976 (2023)
  29. Tip60 acetylation of histone H3K4 temporally controls chromosome passenger complex localization. Niedzialkowska E, Liu L, Kuscu C, Mayo Z, Minor W, Strahl BD, Adli M, Stukenberg PT. Mol Biol Cell 33 br15 (2022)


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