Structural Basis and IP6 Requirement for Pds5-Dependent Cohesin Dynamics

Molecular Cell

Volumn 62, Issue 2, 2016, Pages 248-259

  Ouyang, Zhuqing ^a   Zheng, Ge ^a   Tomchick, Diana R ^b   Luo, Xuelian ^a,b   Yu, Hongtao ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; PDS5 PROTEIN; PHYTIC ACID; PROTEIN; SORORIN; UNCLASSIFIED DRUG; WAPL PROTEIN; CARRIER PROTEIN; CDCA5 PROTEIN, HUMAN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; ONCOPROTEIN; PDS5B PROTEIN, HUMAN; PHOSPHOPROTEIN; PROTEOCHONDROITIN SULFATE; RAD21 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMC3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; WAPAL PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INSECT CELL; INTERPHASE; ISOTHERMAL TITRATION CALORIMETRY; MITOSIS; MUTAGENESIS; NONHUMAN; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTON NUCLEAR MAGNETIC RESONANCE; TRANSIENT TRANSFECTION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CONSERVED SEQUENCE; GENETIC TRANSFECTION; GENETICS; HUMAN CHROMOSOME; KINETICS; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN DOMAIN; RNA INTERFERENCE; STRUCTURE ACTIVITY RELATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BINDING SITES; CARRIER PROTEINS; CELL CYCLE PROTEINS; CHONDROITIN SULFATE PROTEOGLYCANS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; KINETICS; MODELS, MOLECULAR; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHYTIC ACID; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84959864954     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.02.033     Document Type: Article

References (46)

1. Beckouët F., Srinivasan M., Roig M.B., Chan K.L., Scheinost J.C., Batty P., Hu B., Petela N., Gligoris T., Smith A.C., et al. Releasing activity disengages cohesin's Smc3/Scc1 interface in a process blocked by acetylation. Mol. Cell 2016, 61:563-574.
2. Bose T., Gerton J.L. Cohesinopathies, gene expression, and chromatin organization. J. Cell Biol. 2010, 189:201-210.
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. 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.
5. 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.
6. Evans P.R. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:282-292.
7. 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.
8. Gerlich D., Koch B., Dupeux F., Peters J.M., Ellenberg J. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr. Biol. 2006, 16:1571-1578.
9. 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.
10. 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.
11. Haering C.H., Farcas A.M., Arumugam P., Metson J., Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature 2008, 454:297-301.
12. 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.
13. Heidinger-Pauli J.M., Onn I., Koshland D. Genetic evidence that the acetylation of the Smc3p subunit of cohesin modulates its ATP-bound state to promote cohesion establishment in Saccharomyces cerevisiae. Genetics 2010, 185:1249-1256.
14. 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.
15. 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.
16. 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.
17. Macbeth M.R., Schubert H.L., Vandemark A.P., Lingam A.T., Hill C.P., Bass B.L. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 2005, 309:1534-1539.
18. Merkenschlager M., Odom D.T. CTCF and cohesin: linking gene regulatory elements with their targets. Cell 2013, 152:1285-1297.
19. 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.
20. Minor W., Cymborowski M., Otwinowski Z., Chruszcz M. HKL-3000: the integration of data reduction and structure solution--from diffraction images to an initial model in minutes. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:859-866.
21. Monserrate J.P., York J.D. Inositol phosphate synthesis and the nuclear processes they affect. Curr. Opin. Cell Biol. 2010, 22:365-373.
22. Montpetit B., Thomsen N.D., Helmke K.J., Seeliger M.A., Berger J.M., Weis K. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 2011, 472:238-242.
23. Murayama Y., Uhlmann F. DNA Entry into and Exit out of the Cohesin Ring by an Interlocking Gate Mechanism. Cell 2015, 163:1628-1640.
24. Nasmyth K., Haering C.H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 2009, 43:525-558.
25. 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.
26. Onn I., Heidinger-Pauli J.M., Guacci V., Unal E., Koshland D.E. Sister chromatid cohesion: a simple concept with a complex reality. Annu. Rev. Cell Dev. Biol. 2008, 24:105-129.
27. 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.
28. 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.
29. Peters J.M., Tedeschi A., Schmitz J. The cohesin complex and its roles in chromosome biology. Genes Dev. 2008, 22:3089-3114.
30. Rankin S. Sororin, the cell cycle and sister chromatid cohesion. Cell Cycle 2005, 4:1039-1042.
31. 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.
32. 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.
33. 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.
34. Sheard L.B., Tan X., Mao H., Withers J., Ben-Nissan G., Hinds T.R., Kobayashi Y., Hsu F.F., Sharon M., Browse J., et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 2010, 468:400-405.
35. Sherwood R., Takahashi T.S., Jallepalli P.V. Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev. 2010, 24:2723-2731.
36. 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.
37. Solomon D.A., Kim T., Diaz-Martinez L.A., Fair J., Elkahloun A.G., Harris B.T., Toretsky J.A., Rosenberg S.A., Shukla N., Ladanyi M., et al. Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science 2011, 333:1039-1043.
38. Ström L., Karlsson C., Lindroos H.B., Wedahl S., Katou Y., Shirahige K., Sjögren C. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 2007, 317:242-245.
39. 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.
40. Tan X., Calderon-Villalobos L.I., Sharon M., Zheng C., Robinson C.V., Estelle M., Zheng N. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 2007, 446:640-645.
41. 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.
42. Uhlmann F., Wernic D., Poupart M.A., Koonin E.V., Nasmyth K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 2000, 103:375-386.
43. 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.
44. Vaur S., Feytout A., Vazquez S., Javerzat J.P. Pds5 promotes cohesin acetylation and stable cohesin-chromosome interaction. EMBO Rep. 2012, 13:645-652.
45. Wu F.M., Nguyen J.V., Rankin S. A conserved motif at the C terminus of sororin is required for sister chromatid cohesion. J. Biol. Chem. 2011, 286:3579-3586.
46. Wu N., Kong X., Ji Z., Zeng W., Potts P.R., Yokomori K., Yu H. Scc1 sumoylation by Mms21 promotes sister chromatid recombination through counteracting Wapl. Genes Dev. 2012, 26:1473-1485.