Structure of the Pds5-Scc1 Complex and Implications for Cohesin Function

Cell Reports

Volumn 14, Issue 9, 2016, Pages 2116-2126

  Muir, Kyle W ^a   Kschonsak, Marc ^b   Li, Yan ^a   Metz, Jutta ^b   Haering, Christian H ^b   Panne, Daniel ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; NUCLEAR PROTEIN; PDS5 PROTEIN; PROTEIN SCC1; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; MCD1 PROTEIN, S CEREVISIAE; NONHISTONE PROTEIN; PDS5 PROTEIN, S CEREVISIAE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SISTER CHROMATID; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; ALPHA HELIX; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; CHROMOSOME; CHROMOSOME SEGREGATION; MICROBIAL VIABILITY; MOLECULAR MODEL; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SMALL ANGLE SCATTERING; STRUCTURAL HOMOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; CHROMOSOMES, FUNGAL; CRYSTALLOGRAPHY, X-RAY; MICROBIAL VIABILITY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCATTERING, SMALL ANGLE; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84960365049     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.078     Document Type: Article

References (55)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Brunger A.T., Adams P.D., Fromme P., Fromme R., Levitt M., Schröder G.F. Improving the accuracy of macromolecular structure refinement at 7 Å resolution. Structure 2012, 20:957-966.
3. Buheitel J., Stemmann O. Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J. 2013, 32:666-676.
4. Carretero M., Ruiz-Torres M., Rodríguez-Corsino M., Barthelemy I., Losada A. Pds5B is required for cohesion establishment and Aurora B accumulation at centromeres. EMBO J. 2013, 32:2938-2949.
5. Chan K.L., Roig M.B., Hu B., Beckouët F., Metson J., Nasmyth K. Cohesin's DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell 2012, 150:961-974.
6. Chan K.L., Gligoris T., Upcher W., Kato Y., Shirahige K., Nasmyth K., Beckouët F. Pds5 promotes and protects cohesin acetylation. Proc. Natl. Acad. Sci. USA 2013, 110:13020-13025.
7. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:12-21.
8. Eichinger C.S., Kurze A., Oliveira R.A., Nasmyth K. Disengaging the Smc3/kleisin interface releases cohesin from Drosophila chromosomes during interphase and mitosis. EMBO J. 2013, 32:656-665.
9. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
10. Gandhi R., Gillespie P.J., Hirano T. Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr. Biol. 2006, 16:2406-2417.
11. Gligoris T.G., Scheinost J.C., Bürmann F., Petela N., Chan K.L., Uluocak P., Beckouët F., Gruber S., Nasmyth K., Löwe J. Closing the cohesin ring: structure and function of its Smc3-kleisin interface. Science 2014, 346:963-967.
12. Gruber S., Haering C.H., Nasmyth K. Chromosomal cohesin forms a ring. Cell 2003, 112:765-777.
13. Guacci V., Koshland D. Cohesin-independent segregation of sister chromatids in budding yeast. Mol. Biol. Cell 2012, 23:729-739.
14. Haarhuis J.H., Elbatsh A.M., van den Broek B., Camps D., Erkan H., Jalink K., Medema R.H., Rowland B.D. WAPL-mediated removal of cohesin protects against segregation errors and aneuploidy. Curr. Biol. 2013, 23:2071-2077.
15. Haarhuis J.H., Elbatsh A.M., Rowland B.D. Cohesin and its regulation: on the logic of X-shaped chromosomes. Dev. Cell 2014, 31:7-18.
16. Haering C.H., Farcas A.M., Arumugam P., Metson J., Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature 2008, 454:297-301.
17. Hara K., Zheng G., Qu Q., Liu H., Ouyang Z., Chen Z., Tomchick D.R., Yu H. Structure of cohesin subcomplex pinpoints direct shugoshin-Wapl antagonism in centromeric cohesion. Nat. Struct. Mol. Biol. 2014, 21:864-870.
18. Hartman T., Stead K., Koshland D., Guacci V. Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J. Cell Biol. 2000, 151:613-626.
19. Hou F., Zou H. Two human orthologues of Eco1/Ctf7 acetyltransferases are both required for proper sister-chromatid cohesion. Mol. Biol. Cell 2005, 16:3908-3918.
20. Huis in 't Veld P.J., Herzog F., Ladurner R., Davidson I.F., Piric S., Kreidl E., Bhaskara V., Aebersold R., Peters J.M. Characterization of a DNA exit gate in the human cohesin ring. Science 2014, 346:968-972.
21. Kabsch W. Xds. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:125-132.
22. Kueng S., Hegemann B., Peters B.H., Lipp J.J., Schleiffer A., Mechtler K., Peters J.M. Wapl controls the dynamic association of cohesin with chromatin. Cell 2006, 127:955-967.
23. Lee B.-G., Roig M.B., Jansma M., Petela N., Metson J., Nasmyth K., Löwe J. Crystal structure of the cohesin gatekeeper Pds5 and in complex with kleisin Scc. Cell Rep. 2016, 14:2108-2115. this issue.
24. Lopez-Serra L., Lengronne A., Borges V., Kelly G., Uhlmann F. Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr. Biol. 2013, 23:64-69.
25. Losada A., Yokochi T., Hirano T. Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts. J. Cell Sci. 2005, 118:2133-2141.
26. Michaelis C., Ciosk R., Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 1997, 91:35-45.
27. Minamino M., Ishibashi M., Nakato R., Akiyama K., Tanaka H., Kato Y., Negishi L., Hirota T., Sutani T., Bando M., Shirahige K. Esco1 Acetylates Cohesin via a Mechanism Different from That of Esco2. Curr. Biol. 2015, 25:1694-1706.
28. Murayama Y., Uhlmann F. DNA Entry into and Exit out of the Cohesin Ring by an Interlocking Gate Mechanism. Cell 2015, 163:1628-1640.
29. Nishiyama T., Ladurner R., Schmitz J., Kreidl E., Schleiffer A., Bhaskara V., Bando M., Shirahige K., Hyman A.A., Mechtler K., Peters J.M. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 2010, 143:737-749.
30. Nishiyama T., Sykora M.M., Huis in 't Veld P.J., Mechtler K., Peters J.M. Aurora B and Cdk1 mediate Wapl activation and release of acetylated cohesin from chromosomes by phosphorylating Sororin. Proc. Natl. Acad. Sci. USA 2013, 110:13404-13409.
31. O'Donovan D.J., Stokes-Rees I., Nam Y., Blacklow S.C., Schröder G.F., Brunger A.T., Sliz P. A grid-enabled web service for low-resolution crystal structure refinement. Acta Crystallogr. D Biol. Crystallogr. 2012, 68:261-267.
32. Ouyang Z., Zheng G., Song J., Borek D.M., Otwinowski Z., Brautigam C.A., Tomchick D.R., Rankin S., Yu H. Structure of the human cohesin inhibitor Wapl. Proc. Natl. Acad. Sci. USA 2013, 110:11355-11360.
33. Panizza S., Tanaka T., Hochwagen A., Eisenhaber F., Nasmyth K. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr. Biol. 2000, 10:1557-1564.
34. Parelho V., Hadjur S., Spivakov M., Leleu M., Sauer S., Gregson H.C., Jarmuz A., Canzonetta C., Webster Z., Nesterova T., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
35. Pernot P., Round A., Barrett R., De Maria Antolinos A., Gobbo A., Gordon E., Huet J., Kieffer J., Lentini M., Mattenet M., et al. Upgraded ESRF BM29 beamline for SAXS on macromolecules in solution. J. Synchrotron Radiat. 2013, 20:660-664.
36. Peters J.-M., Nishiyama T. Sister chromatid cohesion. Cold Spring Harb. Perspect. Biol. 2012, 4:a011130.
37. Petoukhov M.V., Franke D., Shkumatov A.V., Tria G., Kikhney A.G., Gajda M., Gorba C., Mertens H.D., Konarev P.V., Svergun D.I. New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Cryst. 2012, 45:342-350.
38. Roig M.B., Löwe J., Chan K.L., Beckouët F., Metson J., Nasmyth K. Structure and function of cohesin's Scc3/SA regulatory subunit. FEBS Lett. 2014, 588:3692-3702.
39. Rolef Ben-Shahar T., Heeger S., Lehane C., East P., Flynn H., Skehel M., Uhlmann F. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 2008, 321:563-566.
40. Rowland B.D., Roig M.B., Nishino T., Kurze A., Uluocak P., Mishra A., Beckouët F., Underwood P., Metson J., Imre R., et al. Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. Mol. Cell 2009, 33:763-774.
41. Schröder G.F., Levitt M., Brunger A.T. Super-resolution biomolecular crystallography with low-resolution data. Nature 2010, 464:1218-1222.
42. Schrodinger, LLC (2010). The PyMOL Molecular Graphics System, Version 1.3r1.
43. Shintomi K., Hirano T. Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev. 2009, 23:2224-2236.
44. Sjögren C., Nasmyth K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 2001, 11:991-995.
45. Stead K., Aguilar C., Hartman T., Drexel M., Meluh P., Guacci V. Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J. Cell Biol. 2003, 163:729-741.
46. Sumara I., Vorlaufer E., Gieffers C., Peters B.H., Peters J.M. Characterization of vertebrate cohesin complexes and their regulation in prophase. J. Cell Biol. 2000, 151:749-762.
47. Sutani T., Kawaguchi T., Kanno R., Itoh T., Shirahige K. Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr. Biol. 2009, 19:492-497.
48. Svensson O., Malbet-Monaco S., Popov A., Nurizzo D., Bowler M.W. Fully automatic characterization and data collection from crystals of biological macromolecules. Acta Crystallogr. D Biol. Crystallogr. 2015, 71:1757-1767.
49. Tanaka K., Hao Z., Kai M., Okayama H. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J. 2001, 20:5779-5790.
50. Tedeschi A., Wutz G., Huet S., Jaritz M., Wuensche A., Schirghuber E., Davidson I.F., Tang W., Cisneros D.A., Bhaskara V., et al. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 2013, 501:564-568.
51. Unal E., Heidinger-Pauli J.M., Kim W., Guacci V., Onn I., Gygi S.P., Koshland D.E. A molecular determinant for the establishment of sister chromatid cohesion. Science 2008, 321:566-569.
52. Vaur S., Feytout A., Vazquez S., Javerzat J.P. Pds5 promotes cohesin acetylation and stable cohesin-chromosome interaction. EMBO Rep. 2012, 13:645-652.
53. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., Evans P.R., Keegan R.M., Krissinel E.B., Leslie A.G., McCoy A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:235-242.
54. Yan J., Enge M., Whitington T., Dave K., Liu J., Sur I., Schmierer B., Jolma A., Kivioja T., Taipale M., Taipale J. Transcription factor binding in human cells occurs in dense clusters formed around cohesin anchor sites. Cell 2013, 154:801-813.
55. Zhang J., Shi X., Li Y., Kim B.J., Jia J., Huang Z., Yang T., Fu X., Jung S.Y., Wang Y., et al. Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol. Cell 2008, 31:143-151.