The many functions of SMC proteins in chromosome dynamics

Nature Reviews Molecular Cell Biology

Volumn 3, Issue 10, 2002, Pages 767-778

  Jessberger, Rolf ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SMC; UNCLASSIFIED DRUG;

CHROMOSOME; CHROMOSOME CONDENSATION; CHROMOSOME STRUCTURE; DNA RECOMBINATION; DNA REPAIR; GENE DOSAGE; MEIOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; SISTER CHROMATID EXCHANGE; SOMATIC CELL;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DNA REPAIR; DNA-BINDING PROTEINS; DOSAGE COMPENSATION, GENETIC; FUNGAL PROTEINS; MACROMOLECULAR SUBSTANCES; MEIOSIS; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC;

EID: 0036792404     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm930     Document Type: Review

References (107)

1. Peterson, C. L. The SMC family: novel motor proteins for chromosome condensation? Cell 79, 389-392 (1994).
2. Gasser, S, M. Coiling up chromosomes. Curr. Biol. 5, 257-360 (1995).
3. Hirano, T., Mitchison, T. J. & Swedlow, J. R. The SMC family: from chromosome condensation to dosage compensation. Curr. Biol. 7, 329-336 (1995).
4. Strunnikov, A. V. & Jessberger, R. Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions. Eur J Biochem 263, 6-13 (1998).
5. Cobbe, N. & Heck, M. M. S. Review: SMCs in the world of chromosome biology - from prokaryotes to higher eukaryotes. J. Struct. Biol. 129, 123-143 (2000).
6. Nasmyth, K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745 (2001).
7. Hirano, T. The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev. 16, 399-414 (2002).
8. Soppa, J. Prokaryotic structural maintenance of chromosomes (SMC) proteins: distribution, phylogeny, and comparison with MukBs and additional prokaryotic and eukaryotic coiled-coil proteins. Gene 278, 253-264 (2001).
9. Strunnikov, A. V., Larionov, V. L. & 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. 123, 1635-1648 (1993).
10. Lehmann,A R. et al. The rad18 gene of Schizcsaccharcmyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol. Cell. Biol. 15, 7067-7080 (1995).
11. Jessberger, R. Frei, C. & Gasser, S. M. Chromosome dynamics: The SMC protein family. Curr. Opin. Genet. Dev. 8, 254-259 (1998).
12. Jones, S. & Sgouros, J. The cohesin complex: sequence homologies, interaction networks and shared motifs. Genome Biol. 2, 1-12 (2001).
13. Hagstrom, K A., Holmes, V F., Cozzarelli, N. R. & Meyer, B. J. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 16, 729-742 (2002).
14. Revenkova, E., Eijpe, M., Heyting, C., Gross, B. & Jessberger, R. Novel meiosis-specific isoform of mammalian SMC1. Mol. Cell. Biol. 21, 6984-6998 (2001).
15. Holland, I. B. & Blight, M A. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293, 381-399 (1999)
16. Hirano, M., Anderson, D E., Erickson, H. P. & Hirano, T. Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J. 20, 3238-3250 (2001).
17. Melby, T. E., Ciampaglio, C N, Briscoe, G. & Erickson, H. P. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J. Cell. Biol. 142, 1595-1604 (1998).
18. Akhmedov, A. T. et al. Structural maintenance of chromosomes protein C-terminal domains bind preferentially to DNA with secondary structure. J. Biol. Chem. 273, 24088-24094 (1998).
19. Akhmedov, A. T., 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. 274, 38216-38224(1999).
20. Blat, Y. & Kleckner, N Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arm versus the centric region Cell 98, 249-259 (1999).
21. Megee, P.C., Mistrot, C., Guacci, V. & Koshland, D. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences. Mol. Cell 4, 445-450 (1999).
22. Laloraya, S., Guacci, V & Koshland, D. Chromosomal addresses of the cohesin component Mcd1p. J. Cell Biol. 151, 1047-1056 (2000).
23. Sutani, T. & Yanagida, M. DNA renaturation activity of the SMC complex implicated in chromosome condensation. Nature 388, 798-801 (1997).
24. Jessberger, R., Riwar, B., Baechtold, H. & Akhmedov, A. T., SMC proteins constitute two subunits of the mammalian recombination protein complex RC-1. EMBO J. 15, 4061-4068 (1996).
25. van den Ent, F., Lockhart, A., Kendrick-Jones, J. & Lowe, J. Crystal structure of the N-terminal domain of MukB: a protein involved in chromosome partitioning. Structure Fold. Des. 15, 1181-1187 (1999).
26. Löwe, J., Cordell, S. C. & van den Ent, F. Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted. J. Mol. Biol. 306, 25-35 (2001).
27. Hopfner, K. P. et al. Structural biology of Rad5O ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily Cell 101, 789-800 (2000).
28. Hearing, C. H., Löwe, J., Hochwagen, A. & Nasmyth, K. Molecular architecture of SMC proteins and the yeast cohesion complex Mol. Cell 9, 773-788 (2002).
29. Anderson, D. E., Losada, A., Erickson, H. P. & Hirano, T. Condensin and cohesin display different arm conformations with characteristic hinge angles. J. Cell Biol. 156, 419-424 (2002).
30. Beaseley, 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. 12, 1201-1209 (2002),
31. Yoshimura, S. H. et al. Condensin architecture and interaction with DNA. Regulatory non-SMC subunits bind to the head of SMC heterodimer. Curr. Biol. 12, 508-513 (2002).
32. Guacci, V., Koshland, D. & Strunnikov, A. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S cerevisiae. Cell 91, 47-58 (1997).
33. Michaelis, C., Ciosk, R. & Nasmyth, K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids Cell 91, 35-46 (1997). Cohesin, Scc1 and Smc1 are essential for sister-chromatid cohesion.
34. Losada, A, Hirano, M. & Hirano, T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev. 12, 1986-1997 (1998). The identification of vertebrate cohesin and demonstration of its essential function.
35. Hirano, T. & Mitchison, T. J. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79, 449-458 (1994).
36. 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 89, 511-521 (1997).
37. Fousteri, M. I. & Lehmann, A. R. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J. 19, 1691-1702 (2000).
38. Jeseberger, R., Podust, V., Hübscher, U. & Berg, R A mammalian protein complex that repairs double-strand breaks and deletions by recombination. J. Biol. Chem. 268, 15070-15079 (1993).
39. Lieb, J. D., Albrecht, M. R, Chuang, P T. & Meyer, B. J. MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell 92, 265-277 (1998).
40. Losada, A., Yokochi, T., Kobayashi, R. & Hirano, T. Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes. J. Cell Biol. 150, 405-416 (2000).
41. 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. 151, 749-762 (2000)
42. Toth, A. et al. Yeast cohesin complex requires a conserved protein Ecol p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev. 13, 320-333 (1999).
43. Tomonaga, T. et al. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev. 14, 2757-2770 (2000)
44. Carson, D. R. & Christman, M. F. Evidence that replication fork components catalyze establishment of cohesion between sister chromatids. Proc. Natl Acad. Sci. USA 98, 8270-8275 (2001).
45. Tanaka, T., Cosma, M. R, Wirth, K. & Nasmyth, K. Identification of cohesin association sites at centromeres and along chromosome arms. Cell 98, 847-858 (1999).
46. Donze, D., Adams, C. R., Rine, J. & Kamakaka, R. T. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev. 13, 698-708 (1999).
47. Uhlmann, F. & Nasmyth, K. Cohesion between sister chromatids must be established during DNA replication. Curr Biol. 8, 1095-1101 (1998).
48. Ciosk, R. et al. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol. Cell 5, 243-254 (2000).
49. Uhlmann, F. Secured cutting: controlling separase at the metaphase to anaphase transition. EMBO Rep. 2, 487-492 (2001).
50. Waizenegger I. C., Hauf, S., Meinke, A. & Peters, J. M. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103, 399-410 (2000).
51. 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 103, 375-386 (2000).
52. Alexandru, G., Uhlmann, F., Mechtler, K., Poupart, M. A. & Nasmyth, K. Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105, 459-472 (2001).
53. Sumara, I. et al. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol. Cell 9, 515-525 (2002).
54. Losada, A. & Hirano, T. Shaping the metaphase chromosome: coordination of cohesion and condensation. Bioessays 23, 924-935 (2001).
55. Wang, Z., Castano, I. B., De Las Penas, A., Adams, C. & Christman, M. F. Pol kappa: a DNA polymerase required for sister chromatid cohesion. Science 289, 774-779 (2000).
56. Schmiesing, J. A., Gregson, H. C., Zhou, S. & Yokomori, K. A human condensin complex containing hCAP-C-hCAP-E and CNAP1, a homolog of Xenopus XCAP-D2, colocalizes with phosphorylated histone H3 during the early stage of mitotic chromosome condensation. Mol. Cell. Biol. 20, 6996-6700 (2000).
57. Saitoh, N., Goldberg, I. G., Wood, E. R. & Earnshaw, W. C. Scll: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J Cell Biol. 127, 303-318 (1994).
58. Freeman, L., Aragon-Alcaide, L. & Strunnikov, A. The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol. 149, 811-824 (2000).
59. Kimura, K., Cuvier, O. & Hirano, T. Chromosome condensation by a human condensin complex in Xenopus egg extracts. J. Biol. Chem. 276, 5417-5420 (2001).
60. Saka, Y. et al. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J. 13, 4938-4952 (1994).
61. Strunnikov, A. V., Hogan, E. & Koshland, D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation defines a subgroup within the SMC family. Genes Dev. 9, 587-599 (1995).
62. Bhat, M. A., Philp, A. V., Glover, D. M. Bellen, H. J. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II. Cell 87, 1103-1114 (1996).
63. Britton, R. A., Lin, D. C. & Grossman, A. D. Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev. 12, 1254-1259 (1998).
64. Sutani, T. et al. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev. 13, 2271-2283 (1999).
65. Lavoie, B. D., Hogan, E. & Koshland, D. In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J. Cell Biol. 156, 805-815 (2002).
66. Biggins, S., Bhalla, N., Chang, A., Smith, D. L. & Murray, A. W. Genes involved in sister chromatid separation and segregation in the budding yeast Saccharomyces cerevisiae. Genetics 159, 453-470 (2001).
67. Steffensen, S. et al. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr Biol. 11, 295-307 (2001).
68. Kimura, K. & Hirano, T. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 90, 625-634 (1997).
69. Kimura, K. & Hirano, T. Dual roles of the 11S regulatory subcomplex in condensin functions. Proc. Natl Acad. Sci. USA 97, 11972-11977 (2000).
70. Kimura, K., Rybenkov, V. V., Crisona, N. J., Hirano, T. & Cozzarelli, N. R. 13S condesin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98, 239-248 (1999).
71. Bazett-Jones, D. P., Kimura, K. & Hirano, T. Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol. Cell 9, 1183-1190 (2002).
72. Kimura, K., Hirano, M., Kobayashi, R. & Hirano, T. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 282, 487-490 (1998).
73. Sutani, et al. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev. 13, 2271-2283 (1999).
74. Giet, R. & Glover, D. M. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669-682 (2001).
75. Hirano, T. Chromosome cohesion, condensation, and separation. Annu. Rev. Bioehem. 69, 115-144 (2000).
76. Castano, I. B., Brzoska, P. M., Sadoff, B. U., Chen, H. & Christman, M. F. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae. Genes Dev. 10, 2564-2576 (1996).
77. 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. 151, 613, 626 (2000).
78. Sonoda, E. et al. Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev. Cell. 1,759-770 (2001).
79. Chuang, P. T., Albertson, D. G. & Meyer, B, J. DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 79, 459-474 (1994). An SMC4-like protein in C. elegans acts in gene-dosage compensation, a new function for SMC proteins.
80. Chuang, P. T., Lieb, J. D. & Meyer, B. J. Sex-specific assembly of a dosage compensation complex on the nematode X chromosome, Science 274, 1736-1738 (1996).
81. Lieb, J. D., Capowski, E. E., Meneely, P. & Meyer, B. J. DPY-26, a link between dosage compensation and meiotic chromosome segregation in the nematode. Science 274, 1732-1736 (1996).
82. Davis, T. L. & Meyer, B. J. SDC-3 coordinates the assembly of a dosage compensation complex on the nematode X chromosome. Development 124, 1019-1031 (1997).
83. Jessberger, R., Chui, G., Linn, S. & Kemper B. Analysis of the mammalian recombination protein complex RC-1. Mutat. Res. 350, 217-222 (1996).
84. Hübscher, U., Nasheuer, H.-P. & Syväoja, J. Eukaryotic DNA polymerases, a growing family. Trends Biochem. Sci. 25, 143-147 (2000).
85. Morishita, T., Tsutsui, Y. Iwasaki, H. & Shinagawa, H. The Schizosaccharomyces pombe rad60 gene is essential for repairing double-strand DNA breaks spontaneously occurring during replication and induced by DNA-damaging agents. Mol. Cell. Biol. 22, 3537-3548 (2002).
86. Fujioka, Y., Kimata, Y., Nomaguchi, K., Watanabe, K. & Kohno, K. Identification of a novel non-SMC component of the SMC5/SMC6 complex involved in DNA repair. J. Biol. Chem 377, 21585-21591 (2002).
87. Taylor, E. M .et al. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol. Biol. Cell 12, 1583-1594 (2001).
88. Mengiste, T., Revenkova, E., Bechtold, N. & Paszkowski, J. An SMC-like protein is required for efficient homologous recombination in Arabidopsis. EMBO J. 18, 4505-4512 (1999).
89. Hanin, M., Mengiste, T., Bogucki, A. & Paszkowski, J. Elevated levels of intrachromosomal homologous recombination in Arabidopsis overexpressing the MIM gene Plant J. 24, 183-189 (2000).
90. Sjøgren, C. & Nasmyth, K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevesiae. Curr Biol. 11, 991-995 (2001).
91. Birkenbihi, R. P. & Subramani, S. Cloning and characterization of rad21 an essential gene of Schizosaccharomyces pombe involved in DNA double-strand-break repair Nucl. Acids Res. 20, 6605-6611 (1992).
92. Johnson, R. D. & Jasin, M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19, 3398-3407 (2000).
93. Kim, S. T., Xu, B. & Kastan, M. B. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 16, 560-570 (2002).
94. Yazdi, P. T. et al. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev. 16, 571-582 (2002).
95. Shiloh, Y. ATM and ATR: networking cellular responses to DNA damage. Curr Opin. Genet. Dev. 11, 71-77 (2001).
96. Klein, F. et al. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis Cell 98, 91-103 (1999).
97. Eijpe, M., Heyting, C., Gross, B. & Jessberger, R. Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes. J. Cell Sci. 113, 673-682 (2000).
98. Pelttari, J. et al. A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammaJian meiotic cells. Mol Cell Biol. 21, 5667-5677 (2001).
99. Prieto, I. et al. Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nature Cell Biol. 3, 761-766 (2001).
100. Watanabe, Y. & Nurse, P. Cohesin Rec8 is required for reductional chromosome segregation at meiosis Nature 400, 461-464 (1999).
101. Watanbe, Y., Yokobayashi, S., Yamamoto, M. & Nurse, P. Pre-meiotic S phase is linked to reductional chromosome segregation and recombination. Nature 409, 359-363 (2001).
102. Pasierbek, P. et al. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15,1349-1360 (2001).
103. Ghiselli, G. & Iozzo, R. V. Overexpression of bamacan/SMC3 causes transformation. J Biol. Chem. 275, 20235-20238 (2000)
104. Hopfner, K. P. at al. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105, 473-485 (2001).
105. Hopfner, K. P., Putnam, C. D. & Tainer, J. DNA double- strand break repair from head to tail Curr. Opin. Struct. Biol. 12, 115-122 (2002).
106. Hopfner, K. P. et al. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418, 562-566 (2002).
107. de Jager, M. et al. Human Rad50/Mre11 is a flexible complex that can tether DNA ends Mol. Cell 8, 1129-1135 (2001).