The evolution of ATPase activity in SMC proteins

Proteins: Structure, Function and Genetics

Volumn 63, Issue 3, 2006, Pages 685-696

  Cobbe, Neville ^a   Heck, Margarete M S ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

ATPase; Coevolution; Cohesin; Condensin; Protein protein interaction; SMC

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; COHESIN; CONDENSIN; PROTEIN; STRUCTURAL MAINTENANCE OF CHROMOSOME PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; ENZYME ACTIVITY; EUKARYOTIC CELL; EVOLUTION; HEREDITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATASES; CHROMOSOMAL PROTEINS, NON-HISTONE; CONSERVED SEQUENCE; DATABASES, PROTEIN; EVOLUTION, MOLECULAR; PROTEIN STRUCTURE, SECONDARY;

EUKARYOTA;

EID: 33646018946     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.20795     Document Type: Article

References (73)

1. Cobbe N, Heck MM. SMCs in the world of chromosome biology-from prokaryotes to higher eukaryotes. J Struct Biol 2000;129:123-143.
2. Cobbe N, Heck MMS. The evolution of SMC proteins: Phylogenetic analysis and structural implications. Mol Biol Evol 2004;21:332-347.
3. Melby TE, Ciampaglio CN, Briscoe G, Erickson HP. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 1998;142:1595-1604.
4. Anderson DE, Losada A, Erickson HP, Hirano T. Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 2002;156:419-424.
5. Beasley M, Xu H, Warren W, McKay M. Conserved disruptions in the predicted coiled-coil domains of eukaryotic SMC complexes: implications for structure and function. Genome Res 2002;12:1201-1209.
6. Yoshimura SH, Hizume K, Murakami A, Sutani T, Takeyasu K, Yanagida M. Condensin architecture and interaction with DNA: Regulatory non-SMC subunits bind to the head of SMC heterodimer. Curr Biol 2002;12:508-513.
7. Haering CH, Löwe J, Hochwagen A, Nasmyth K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 2002;9:773-788.
8. Haering CH, Schoffnegger D, Nishino T, Helmhart W, Nasmyth K, Löwe J. Structure and stability of Cohesin's Smc1-Kleisin interaction. Mol Cell 2004;15:951-964.
9. Chuang PT, Albertson DG, Meyer BJ. DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 1994;79:459-474.
10. Verkade HM, Bugg SJ, Lindsay HD, Carr AM, O'Connell MJ. Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol Biol Cell 1999;10:2905-2918.
11. Fousteri MI, Lehmann AR. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J 2000;19:1691-1702.
12. Hirano M, Anderson DE, Erickson HP, Hirano T. Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J 2001;20:3238-3250.
13. Kimura K, Hirano T. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 1997;90:625-634.
14. Kimura K, Rybenkov W, Crisona NJ, Hirano T, Cozzarelli NR. 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 1999;98:239-248.
15. Bazett-Jones DP, Kimura K, Hirano T. Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol Cell 2002;9:1183-1190.
16. Strick TR, Kawaguchi T, Hirano T. Real-time detection of single-molecule DNA compaction by condensin I. Curr Biol 2004;14:874-880.
17. Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K. ATP hydrolysis is required for Cohesin's association with chromosomes. Curr Biol 2003;13:1941-1953.
18. Weitzer S, Lehane C, Uhlmann F. A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 2003;13:1930-1940.
19. Stray JE, Crisona NJ, Belotserkovskii BP, Lindsley JE, Cozzarelli NR. The Saccharomyces cerevisiae SMC2/4 condensin compacts DNA into (+) chiral structures without net supercoiling. J Biol Chem 2005;280:34723-34734.
20. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW. Evolutionary rate in the protein interaction network. Science 2002;296:750-752.
21. Cobbe N, Heck MM. Computer dating for proteins. Heredity 2004;93:523-524.
22. Shindyalov IN, Kolchanov NA, Sander C. Can three-dimensional contacts in protein structures be predicted by analysis of correlated mutations? Protein Eng 1994;7:349-358.
23. Taylor WR, Hatrick K. Compensating changes in protein multiple sequence alignments. Protein Eng 1994;7:341-348.
24. Pollock DD, Taylor WR. Effectiveness of correlation analysis in identifying protein residues undergoing correlated evolution. Protein Eng 1997;10:647-657.
25. Pollock DD, Taylor WR, Goldman N. Coevolving protein residues: maximum likelihood identification and relationship to structure. J Mol Biol 1999;287:187-198.
26. Tillier ER, Lui TW. Using multiple interdependency to separate functional from phylogenetic correlations in protein alignments. Bioinformatics 2003;19(6):750-755.
27. Gloor GB, Martin LC, Wahl LM, Dunn SD. Mutual information in protein multiple sequence alignments reveals two classes of coevolving positions. Biochemistry 2005;44:7156-7165.
28. Goh CS, Bogan AA, Joachimiak M, Walther D, Cohen FE. Co-evolution of proteins with their interaction partners. J Mol Biol 2000;299:283-293.
29. Pazos F, Valencia A. Similarity of phylogenetic trees as indicator of protein-protein interaction. Protein Eng 2001;14(9):609-614.
30. Goh CS, Cohen FE. Co-evolutionary analysis reveals insights into protein-protein interactions. J Mol Biol 2002;324:177-192.
31. Jothi R, Kann MG, Przytycka TM. Predicting protein-protein interaction by searching evolutionary tree automorphism space. Bioinformatics 2005;21(Suppl 1):i241-i250.
32. Fraser HB, Hirsh AE, Wall DP, Eisen MB. Coevolution of gene expression among interacting proteins. Proc Nat Acad Sci USA 2004;101:9033-9038.
33. Deng M, Mehta S, Sun F, Chen T. Inferring domain-domain interactions from protein-protein interactions. Genome Res 2002;12:1540-1548.
34. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
35. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000;302:205-217.
36. Wisconsin Package Version 10.3. San Diego, CA: Accelrys Inc.; 1982-2001.
37. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002;18:502-504.
38. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001;18:691-699.
39. Lupas A. Prediction and analysis of coiled-coil structures. Meth Enzymol 1996;266:513-525.
40. Drummond A, Strimmer K. PAL: An object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 2001;17:662-663.
41. Rokas A, Williams BL, King N, Carroll SB. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 2003;425:798-804.
42. Li WH, Wu CI, Luo CC. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 1985;2:150-174.
43. Li WH. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 1993;36:96-99.
44. Strunnikov AV, Larionov VL, Koshland D. SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol 1993;123:1635-1648.
45. Saka Y, Sutani T, Yamashita Y, Saitoh S, Takeuchi M, Nakaseko Y, Yanagida M. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J 1994;13:4938-4952.
46. Strunnikov AV, Hogan E, Koshland D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev 1995;9:587-599.
47. Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 1997;91:35-45.
48. Lieb JD, Albrecht MR, Chuang PT, Meyer BJ. MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell 1998;92:265-277.
49. Steffensen S, Coelho PA, Cobbe N, Vass S, Costa M, Hassan B, Prokopenko SN, et al. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr Biol 2001;11:295-307.
50. Hagstrom KA, Holmes VF, Cozzarelli NR, Meyer BJ. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev 2002;16:729-742.
51. Liu CC, McElver J, Tzafrir I, Joosen R, Wittich P, Patton D, Van Lammeren AA, et al. Condensin and cohesin knockouts in Arabidopsis exhibit a titan seed phenotype. Plant J 2002;29:405-415.
52. Siddiqui NU, Stronghill PE, Dengler RE, Hasenkampf CA, Riggs CD. Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis. Development 2003;130:3283-3295.
53. Gruber S, Haering CH, Nasmyth K. Chromosomal cohesin forms a ring. Cell 2003;112:765-777.
54. Akhmedov AT, Gross B, Jessberger R. Mammalian SMC3 C-terminal and coiled-coil protein domains specifically bind palindromic DNA, do not block DNA ends, and prevent DNA bending. J Biol Chem 1999;274:38216-38224.
55. Watanabe Y. The importance of being Smc5/6. Nat Cell Biol 2005;7:329-331.
56. Akhmedov AT, Frei C, Tsai-Pflugfelder M, Kemper B, Gasser SM, Jessberger R. Structural maintenance of chromosomes protein C-terminal domains bind preferentially to DNA with secondary structure. J Biol Chem 1998;273:24088- 24094.
57. Hopfner KP, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 2000;101:789-800.
58. Hirano T, Kobayashi R, Hirano M. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 1997;89:511-521.
59. Kimura K, Hirano M, Kobayashi R, Hirano T. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 1998;282:487-490.
60. Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, Yanagida M. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev 1999;13:2271-2283.
61. Kimura K, Hirano T. Dual roles of the 11S regulatory subcomplex in condensin functions. Proc Natl Acad Sci USA 2000;97:11972-11977.
62. Lavoie BD, Hogan E, Koshland D. In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J Cell Biol 2002;156:805-815.
63. Sakai A, Hizume K, Sutani T, Takeyasu K, Yanagida M. Condensin but not cohesin SMC heterodimer induces DNA reannealing through protein-protein assembly. EMBO J 2003;22:2764-2775.
64. Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, Hirano T. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 2003;115(1):109-121.
65. Ono T, Fang Y, Spector DL, Hirano T. Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 2004;15:3296-3308.
66. Ball AR Jr, Schmiesing JA, Zhou C, Gregson HC, Okada Y, Doi T, Yokomori K. Identification of a chromosome-targeting domain in the human condensin subunit CNAP1/hCAF-D2/Eg7. Mol Cell Biol 2002;22:5769-5781.
67. Losada A, Hirano T. Intermolecular DNA interactions stimulated by the cohesin complex in vitro. Implications for sister chromatid cohesion. Curr Biol 2001;11:268-272.
68. Kagansky A, Freeman L, Lukyanov D, Strunnikov A. Histone-tail independent chromatin-binding activity of recombinant cohesin holocomplex. J Biol Chem 2004;279:3382-3388.
69. Stray JE, Lindsley JE. Biochemical analysis of the yeast condensin Smc2/4 complex: an ATPase that promotes knotting of circular DNA. J Biol Chem 2003;278:26238-26248.
70. Uhlmann F, Nasmyth K. Cohesion between sister chromatids must be established during DNA replication Curr Biol 1998;8:1095-1101.
71. Bapteste E, Boucher Y, Leigh J, Doolittle WF. Phylogenetic reconstruction and lateral gene transfer. Trends Microbiol 2004;12:406-411.
72. Nei M, Xu P, Glazko G. Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms. Proc Natl Acad Sci USA 2001;98:2497-2502.
73. Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 1999;96:3801-3806.