SMC protein complexes and higher-order chromosome dynamics

Current Opinion in Cell Biology

Volumn 10, Issue 3, 1998, Pages 317-322

  Hirano, Tatsuya ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; PROTEIN SUBUNIT; STRUCTURAL MAINTENANCE OF CHROMOSOME PROTEIN; UNCLASSIFIED DRUG;

COMPLEX FORMATION; EUKARYOTE; GENETIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW; SISTER CHROMATID;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 0031804860     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80006-9     Document Type: Article

References (41)

1. 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 family. J Cell Biol. 123:1993;1635-1648.
2. Hirano T, Mitchison TJ, Swedlow JR. The SMC family: from chromosome condensation to dosage compensation. Curr Opin Cell Biol. 7:1995;329-336.
3. Saitoh N, Goldberg I, Earnshaw WC. The SMC proteins and the coming age of the chromosome scaffold hypothesis. BioEssays. 17:1995;759-766.
4. Koshland D, Strunnikov A. Mitotic chromosome condensation. of special interest Annu Rev Cell Dev Biol. 12:1996;305-333 A comprehensive review that summarizes recent progress in the field of chromosome condensation.
5. Heck MMS. Condensins, cohesins, and chromosome architecture: how to make and break a mitotic chromosome. of special interest Cell. 91:1997;5-8 An updated review on SMC proteins with an emphasis on their roles in chromosome condensation and sister chromatid cohesion.
6. Lehmann AR, Walicka M, Griffiths DJF, Murray JM, Watts FZ, McCready S, Carr AM. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol Cell Biol. 15:1995;7067-7080.
7. Hirano T, Mitchison TJ. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell. 79:1994;449-458.
8. Saitoh N, Goldberg I, Wood ER, Earnshaw WC. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPase with an unusual predicted tertiary structure. J Cell Biol. 127:1994;303-318.
9. 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. of outstanding interest Cell. 89:1997;511-521 This paper reports purification of chromosome condensation protein complexes from Xenopus egg extracts. The largest form, 13S condensin, is essential for chromosome condensation in vitro, and consists of two SMC subunits and three non-SMC 'regulatory' subunits. One of the non-SMC subunits, XCAP-H, is homologous to the Drosophila Barren protein (see Bhat 1996 [13]). Chromosomal targeting of condensins is mitosis-specific and appears to be regulated by phosphorylation.
10. Sutani T, Yanagida M. DNA renaturation activity of the SMC complex implicated in chromosome condensation. of outstanding interest Nature. 388:1997;798-801 Cut3p and Cut14p are overexpressed in fission yeast cells and purified individually or as a complex. The Cut3p - Cut14p complex, but not individual subunits, is shown to display a DNA renaturation activity in vitro, which does not require ATP. Chromatin isolated from a cut14 mutant is sensitive to S1-nuclease, implicating a contribution of the renaturation activity to chromosome structure. This activity might be a part of the 'full' activity supported by the chromosome condensation machinery.
11. 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 condenstaion and segregation in mitosis. EMBO J. 13:1994;4938-4952.
12. Strunnikov AV, Hogan E, Koshland D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Gene Dev. 9:1995;587-599.
13. Bhat MA, Philp AV, Glover DM, Bellen HJ. Chromatid segregation at anaphase requires the barren product, a novel chromosome associated protein that interacts with topoisomerase II. of outstanding interest Cell. 87:1996;1103-1114 The Drosophila barren mutant shows a defect in proper segregation of mitotic chromosomes in early embryos. Barren is a mitosis-specific chromosomal protein, and interacts with topoisomerase II both in vivo and in vitro. Barren has been found subsequently to be homologous to the XCAP-H subunit of 13S condensin (see Hirano 1997 [9]). This is the first evidence that one of the non-SMC subunits of 13S condensin is essential for chromosome segregation in vivo.
14. Kania A, Salzberg A, Bhat M, D'Evelyn D, He Y, Kiss I, Bellen HJ. P-element mutations affecting embryonic peripheral nervous system development in Drosophila melanogaster. Genetics. 139:1995;1663-1678.
15. Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. of outstanding interest Cell. 91:1997;35-45 A genetic screen for yeast mutants that exhibit premature sister chromatid separation identified four gene products: Smc1p, Smc3p, Scc1p and Scc2p. Scc1p, homologous to the S. pombe Rad21p implicated in DNA repair (see Birkenbihl and Subramani 1992 and 1995 [17,18]), associates with chromosomes during S phase and dissociates from them at the metaphase-anaphase transition. The chromosomal association of Scc1p depends on Smc1p, suggesting their functional interaction.
16. 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. of outstanding interest Cell. 91:1997;47-57 Mcd1p (identical to Scc1p; see Michaelis 1997 [15]) is identified through a screen for mutants that display enhanced lethality after a mitotic arrest. An independent screen isolates the same gene as a high copy suppressor of an smc1 mutant. Physical interaction between Mcd1p/Scc1p and Smc1p is shown by coimmunoprecipitation. Mcd1p is required for both sister chromatid cohesion and condensation, implying a link between the two processes.
17. Birkenbihl RP, Subramani S. Cloning and characterization of rad21, an essential gene of Schizosaccharomyces pombe involved in DNA double-strand-break repair. Nucleic Acids Res. 20:1992;6605-6611.
18. Birkenbihl RP, Subramani S. The rad21 gene product of Schizosaccharomyces pombe is a nuclear, cell cycle-regulated phosphoprotein. J Biol Chem. 270:1995;7703-7711.
19. McKay MJ, Troelstra C, van der Spek P, Kanaar R, Smit B, Hagemeijer A, Bootsma D, Hoeijmakers JHJ. Sequence conservation of the rad21 Schizosaccharomyces pombe DNA double-strand break repair gene in human and mouse. Genomics. 36:1996;305-315.
20. Sadoff BU, Heath-Pagliuso S, Castano IB, Zhu Y, Kieff FS, Christman MF. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I. Genetics. 141:1995;465-479.
21. Castano IB, Brzoska PM, Sadoff BU, Chen H, Christman MF. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae. of special interest Genes Dev. 10:1996;2564-2576 Neither Top1p (topoisomerase I) nor Trf4p is essential, but a top1-trf4 double mutant shows a growth defect (see Sadoff 1995 [20]). In this paper, the double mutant is shown to be defective in chromosome condensation in the rDNA. Trf4p interacts with Smc1p both genetically and physically. The authors also report coimmunoprecipitation of Trf4p with Smc2p, but not with Top1p.
22. Denison SH, Kafer E, May GS. Mutation in the bimD gene of Aspergillus nidulans confers a conditional mitotic block and sensitivity to DNA damaging agents. Genetics. 134:1992;1085-1096.
23. Holt CL, May GS. An extragenic suppressor of the mitosis-defective bimD6 mutation of Aspergillus nidulans codes for a chromosome scaffold protein. of special interest Genetics. 142:1996;777-787 BimD is one of the temperature-sensitive mutants that are 'blocked in mitosis' in Aspergillus nidulans (see Denison 1992 [22]). It is also sensitive to DNA-damaging agents. In this paper, four extragenic suppressors of bimD are isolated and one of them, SudA, is shown to encode an SMC3-type protein. SudA is defective in chromosome segregation and exhibits abnormal chromatin structures in both interphase and mitosis.
24. Jessberger R, Podust V, Hubscher U, Berg P. A mammalian protein complex that repairs double-strand breaks and deletions by recombination. J Biol Chem. 268:1993;15070-15079.
25. Jessberger R, Riwar B, Baechtold H, Akhmedov AT. SMC proteins constitute two subunits of the mammalian recombination complex RC-1. of outstanding interest EMBO J. 15:1996;4061-4068 Recombination complex-1 (RC-1) is a protein complex that catalyzes a recombinational repair reaction in vitro and contains DNA polymerase ε and DNA ligase III (see Jessberger 1993 [24]). In this paper, two remaining subunits of RC-1 are identified as SMC proteins. The bSMC1-bSMC3 heterodimer alone mediates DNA reannealing reactions in an ATP-independent manner. An ATPase activity is found in the whole complex, but not in the SMC heterodimer. This paper provides the first biochemical evidence that SMC proteins are involved in recombinational repair.
26. Chuang P-T, Albertson DG, Meyer BJ. DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell. 79:1994;459-474.
27. Chuang P-T, Lieb JD, Meyer BJ. Sex-specific assembly of a dosage compensation complex on the nematode X chromosome. of outstanding interest Science. 274:1996;1736-1739 This paper reports identification of a dosage compensation complex containing DPY-27, DPY-26, and at least two yet-to-be identified subunits (one of them is likely to be MIX-1 [28]). Specific localization of the complex to the hermaphrodite X chromosomes requires three gene products, SDC-2, SDC-3, and DPY-30.
28. Lieb JD, Albrecht MR, Chuang P-T, Meyer BJ. MIX-1: an essential component of the C. elegans mitotic machinery executes X-chromosome dosage compensation. of outstanding interest Cell. 92:1998;265-277 MIX-1 (SMC2-type) is required for both dosage compensation and mitosis. It appears that MIX-1 functions as a component of the dosage compensation protein complex in interphase, and associates with other proteins in mitosis, contributing to chromosome condensation. The results suggest a mechanism by which combinatorial association of different SMC proteins gives rise to their structural and functional diversity.
29. Lieb JD, Capowski EE, Meneely P, Meyer BJ. DPY-26, a link between dosage compensation and meiotic chromosome segregation in the nematode. of special interest Science. 274:1996;1732-1736 In somatic cells, DPY-26 associates specifically with hermaphrodite X chromosomes as a component of the dosage compensation protein complex and reduces their transcriptional level. In germ cells, on the other hand, it localizes to all meiotic chromosomes to ensure proper segregation, providing another functional link between dosage compensation and higher-order chromosome structure.
30. Kimura K, Hirano T. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. of outstanding interest Cell. 90:1997;625-634 13S condensin is purified from Xenopus egg extracts, and shown to have a DNA-stimulated ATPase activity. 13S condensin is able to introduce positive supercoils into a relaxed circular DNA in the presence of topoisomerase I. The supercoiling reaction is ATP-dependent and is stoichiometric rather than catalytic. 13S condensin might wrap DNA in a right-handed direction, or overwind the DNA helix, by utilizing the energy of ATP hydrolysis. Based on these findings, a superhelical tension model for chromosome condensation is proposed.
31. Strick R, Laemmli UK. SARs are cis DNA elements of chromosome dynamics: synthesis of a SAR repressor protein. Cell. 83:1995;1137-1148.
32. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD, et al. Complete genome sequence of the methanogenic archeon, Methanococcus jannaschii. Science. 273:1996;1058-1073.
33. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, et al. The minimal gene complement of Mycoplasma genitalium. Science. 270:1995;397-403.
34. Himmelreich R, Hilbert H, Plagens H, Pirkl E, Li B-C, Hermann R. Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res. 24:1996;4420-4449.
35. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature. 390:1997;249-256.
36. Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, et al. The complete genome sequence of the hyperthermophilic, sulphate- reducing archaeon Archaeoglobus fulgidus. Nature. 390:1997;364-370.
37. Elie C, Baucher MF, Fondrat C, Forterre P. A protein related to eucaryal and bacterial DNA-motor proteins in the hyperthermophilic archaeon Sulfolobus acidocaldarius. J Mol Evol. 45:1997;107-114.
38. Blattner FR, Plunkett Gr, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, et al. The complete genome sequence of Escherichia coli K-12. Science. 277:1997;1453-1474.
39. Hong C-S, Ganetzky B. Molecular characterization of neurally expressing genes in the para sodium channel gene cluster of Drosophila. Genetics. 142:1996;879-892.
40. Rocques PJ, Clark J, Ball S, Crew J, Gill S, Christodoulou Z, Borts RH, Louis EJ, Davies K, Cooper CS. The human SB1.8 gene (DXS423) encodes a putative chromosome segregation protein conserved in lower eukaryotes and prokaryotes. Mol Human Genet. 4:1995;243-249.
41. Losada A, Hirano M, Hirano T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev. 1998;. in press.