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Structural basis for the recognition of phosphorylated histone h3 by the survivin subunit of the chromosomal passenger complex.

Jeyaprakash AA, Basquin C, Jayachandran U, Conti E
Structure 19 1625-34 (2011)
Related entries: 4a0i, 4a0n

Cited: 63 times
EuropePMC logo PMID: 22032967

Abstract

Localization of the chromosomal passenger complex (CPC) at centromeres during early mitosis is essential for accurate chromosome segregation and is dependent on the phosphorylation of histone H3. We report the 2.7 Å resolution structure of the CPC subunit Survivin bound to the N-terminal tail of histone H3 carrying the Thr3 phosphorylation mark (Thr3ph). The BIR domain of Survivin recognizes the Ala1-Arg2-Thr3ph-Lys4 sequence, decoding the modification state and the free N terminus of histone H3 by a strategy similar to that used by PHD fingers. The structural analysis permitted the identification of putative Survivin-binding epitopes in other mitotic proteins, including human Shugoshin 1. Using biophysical and structural data, we show that a phospho-mimic N-terminal sequence such as that of hSgo1 (Ala1-Lys2-Glu3-Arg4) contains the specificity determinants to bind Survivin. Our findings suggest that the CPC engages in mutually exclusive interactions with other constituents of the mitotic machinery and a histone mark in chromatin.

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Articles - 4a0j mentioned but not cited (1)

  1. Determining Cysteines Available for Covalent Inhibition Across the Human Kinome. Zhao Z, Liu Q, Bliven S, Xie L, Bourne PE. J Med Chem 60 2879-2889 (2017)


Reviews citing this publication (24)

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  20. Aurora B Tension Sensing Mechanisms in the Kinetochore Ensure Accurate Chromosome Segregation. McVey SL, Cosby JK, Nannas NJ. Int J Mol Sci 22 8818 (2021)
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Articles citing this publication (37)

  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)
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  3. 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)
  4. 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)
  5. Structural basis for recognition of H3T3ph and Smac/DIABLO N-terminal peptides by human Survivin. Du J, Kelly AE, Funabiki H, Patel DJ. Structure 20 185-195 (2012)
  6. The Inner Centromere Protein (INCENP) Coil Is a Single α-Helix (SAH) Domain That Binds Directly to Microtubules and Is Important for Chromosome Passenger Complex (CPC) Localization and Function in Mitosis. Samejima K, Platani M, Wolny M, Ogawa H, Vargiu G, Knight PJ, Peckham M, Earnshaw WC. J Biol Chem 290 21460-21472 (2015)
  7. EB1 enables spindle microtubules to regulate centromeric recruitment of Aurora B. Banerjee B, Kestner CA, Stukenberg PT. J Cell Biol 204 947-963 (2014)
  8. SUMOylation of DNA topoisomerase IIα regulates histone H3 kinase Haspin and H3 phosphorylation in mitosis. Yoshida MM, Ting L, Gygi SP, Azuma Y. J Cell Biol 213 665-678 (2016)
  9. A noncatalytic function of the topoisomerase II CTD in Aurora B recruitment to inner centromeres during mitosis. Edgerton H, Johansson M, Keifenheim D, Mukherjee S, Chacón JM, Bachant J, Gardner MK, Clarke DJ. J Cell Biol 213 651-664 (2016)
  10. 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)
  11. 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)
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  13. Structural basis for histone mimicry and hijacking of host proteins by influenza virus protein NS1. Qin S, Liu Y, Tempel W, Eram MS, Bian C, Liu K, Senisterra G, Crombet L, Vedadi M, Min J. Nat Commun 5 3952 (2014)
  14. Survivin co-ordinates formation of follicular T-cells acting in synergy with Bcl-6. Andersson KM, Brisslert M, Cavallini NF, Svensson MN, Welin A, Erlandsson MC, Ciesielski MJ, Katona G, Bokarewa MI. Oncotarget 6 20043-20057 (2015)
  15. 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)
  16. Topoisomerase II SUMOylation activates a metaphase checkpoint via Haspin and Aurora B kinases. Pandey N, Keifenheim D, Yoshida MM, Hassebroek VA, Soroka C, Azuma Y, Clarke DJ. J Cell Biol 219 e201807189 (2020)
  17. 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)
  18. Piperine derivatives as potential inhibitors of Survivin: An in silico molecular docking. Sattarinezhad E, Bordbar AK, Fani N. Comput Biol Med 63 219-227 (2015)
  19. Molecular structures guide the engineering of chromatin. Tekel SJ, Haynes KA. Nucleic Acids Res 45 7555-7570 (2017)
  20. 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)
  21. Molecular Signature of CAID Syndrome: Noncanonical Roles of SGO1 in Regulation of TGF-β Signaling and Epigenomics. Piché J, Gosset N, Legault LM, Pacis A, Oneglia A, Caron M, Chetaille P, Barreiro L, Liu D, Qi X, Nattel S, Leclerc S, Breton-Larrivée M, CoHEART Consortium, McGraw S, Andelfinger G. Cell Mol Gastroenterol Hepatol 7 411-431 (2019)
  22. Structure-Guided Exploration of SDS22 Interactions with Protein Phosphatase PP1 and the Splicing Factor BCLAF1. Heroes E, Van der Hoeven G, Choy MS, Garcia JDP, Ferreira M, Nys M, Derua R, Beullens M, Ulens C, Peti W, Van Meervelt L, Page R, Bollen M. Structure 27 507-518.e5 (2019)
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  24. Distinct roles of haspin in stem cell division and male gametogenesis. Soupsana K, Karanika E, Kiosse F, Christogianni A, Sfikas Y, Topalis P, Batistatou A, Kanaki Z, Klinakis A, Politou AS, Georgatos S. Sci Rep 11 19901 (2021)
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  26. 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)
  27. Histone mimics: digging down under. Lin Y, Zhou BP. Front Biol (Beijing) 8 228-233 (2013)
  28. A two-step resin based approach to reveal survivin-selective fluorescent probes. Ambrose AJ, Pham NT, Sivinski J, Guimarães L, Mollasalehi N, Jimenez P, Abad MA, Jeyaprakash AA, Shave S, Costa-Lotufo LV, La Clair JJ, Auer M, Chapman E. RSC Chem Biol 2 181-186 (2021)
  29. Elucidating respective functions of two domains BIR and C-helix of human IAP survivin for precise targeted regulating mitotic cycle, apoptosis and autophagy of cancer cells. Hu F, Pan D, Zheng W, Yan T, He X, Ren F, Lu Y, Ma X. Oncotarget 8 113687-113700 (2017)
  30. Nucleosome-Dependent Pathways That Control Mitotic Progression. Funabiki H, Jenness C, Zierhut C. Cold Spring Harb Symp Quant Biol 82 173-185 (2017)
  31. An Insight into Survivin in Relevance to Hematological, Biochemical and Genetic Characteristics in Tobacco Chewers with Oral Squamous Cell Carcinoma. Yesupatham ST, Dayanand CD, Azeem Mohiyuddin SM, Harendra Kumar ML. Cells 12 1444 (2023)
  32. Distinct Aurora B pools at the inner centromere and kinetochore have different contributions to meiotic and mitotic chromosome segregation. Cairo G, Greiwe C, Jung GI, Blengini C, Schindler K, Lacefield S. Mol Biol Cell 34 ar43 (2023)
  33. Histone Readers and Their Roles in Cancer. Wen H, Shi X. Cancer Treat Res 190 245-272 (2023)
  34. Low tension recruits the yeast Aurora B protein Ipl1 to centromeres in metaphase. Edgerton HD, Mukherjee S, Johansson M, Bachant J, Gardner MK, Clarke DJ. J Cell Sci 136 jcs261416 (2023)
  35. Neferine Targets the Oncogenic Characteristics of Androgen-Dependent Prostate Cancer Cells via Inducing Reactive Oxygen Species. Dasari S, Pathak N, Thomas A, Bitla S, Kumar R, Munirathinam G. Int J Mol Sci 24 14242 (2023)
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