Structural proteins of the SMC (Structural Maintenance of Chromosomes) family and their role in chromatin reorganization

Genetika

Volumn 39, Issue 10, 2003, Pages 1301-1316

  Pavlova, S V ^a   Zakian, S M ^a  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COHESIN; CONDENSIN; CELL CYCLE PROTEIN; DNA; SMC1L2 PROTEIN, MOUSE;

CAENORHABDITIS ELEGANS; CHROMATIN STRUCTURE; CHROMOSOME; ENERGY; EUKARYOTE; MEIOSIS; MITOSIS; NONHUMAN; PROTEIN STRUCTURE; REVIEW; X CHROMOSOME; CHEMISTRY; CHROMATIN; DIMERIZATION; HYDROLYSIS; METABOLISM; NUCLEIC ACID RENATURATION; PHYSIOLOGY; PROTEIN CONFORMATION; SISTER CHROMATID EXCHANGE;

CAENORHABDITIS ELEGANS; EUKARYOTA;

ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEINS; CHROMATIN; DIMERIZATION; DNA; HYDROLYSIS; MEIOSIS; MITOSIS; NUCLEIC ACID RENATURATION; PROTEIN CONFORMATION; SISTER CHROMATID EXCHANGE;

EID: 1542571977     PISSN: 00166758     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (124)

1. 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. 1993. V. 123. No 6. Pt 2. P. 1635-1648.
2. 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. 1994. V. 79. No 3. P. 459-474.
3. Fousteri M.I., Lehmann A.R. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein // EMBO J. 2000. V. 19. No 7. P. 1691-1702.
4. Hirano T., Mitchison T.J. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro // Cell. 1994. V. 79. No 3. P. 449-458.
5. Jessberger R., Chui G., Linn S., Kemper B. Analysis of the mammalian recombination protein complex RC-1 // Mutat. Res. 1996. V. 350. No 1. P. 217-227.
6. 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. 1998. V. 92. No 2. P. 265-277.
7. Revenkova E., Eijpe M., Heyting C. et al. Novel meiosis-specific isoform of mammalian SMC1 // Mol. Cell Biol. 2001. V. 21. No 20. P. 6984-6998.
8. Saitoh N., Goldberg I.G., Wood E.R., Earnshaw W.C. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure // J. Cell Biol. 1994. V. 127. No 2. P. 303-318.
9. Saka Y., Sutani T., Yamashita 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. 1994. V. 13. No 20. P. 4938-4952.
10. Schmiesing J.A., Ball A.R., Jr., Gregson H.C. et al. Identification of two distinct human SMC protein complexes involved in mitotic chromosome dynamics // Proc. Natl Acad. Sci. USA. 1998. V. 95. No 22. P. 12906-12911.
11. Steffensen S., Coelho P.A., Cobbe N. et al. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis // Curr. Biol. 2001. V. 11. No 5. P. 295-307.
12. 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. 1995. V. 9. No 5. P. 587-599.
13. Britton R.A., Lin D.C., Grossman A.D. Characterization of a prokaryotic SMC protein involved in chromosome partitioning // Genes Dev. 1998. V. 12. No 9. P. 1254-1259.
14. Sultana R., Adler D.A., Edelhoff S. et al. The mouse Sb1.8 gene located at the distal end of the X chromosome is subject to X inactivation // Hum. Mol. Genet. 1995. V. 4. No 2. P. 257-263.
15. Holt C.L., May G.S. An extragenic suppressor of the mitosis-defective bimD6 mutation of Aspergillus nidulans codes for a chromosome scaffold protein // Genetics. 1996. V. 142. No 3. P. 777-787.
16. 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. 2002. V. 16. No 6. P. 729-742.
17. Harvey S.H., Krien M.J., O'Cornell M.J. Structural maintenance of chromosomes (SMC) proteins, a family of conserved ATPases // Genome Biol. 2002. V. 3. No 2. P. 3003.1-3003.5.
18. Jessberger R. The many functions of smc proteins in chromosome dynamics // Nat. Rev. Mol. Cell Biol. 2002. V. 3. No 10. P. 767-778.
19. Hirano T. The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair // Genes Dev. 2002. V. 16. No 4. P. 399-414.
20. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis // Annu. Rev. Genet. 2001. V. 35. P. 673-745.
21. Graumann P.L., Losick R., Strunnikov A.V. Subcellular localization of Bacillus subtilis SMC, a protein involved in chromosome condensation and segregation // J. Bacteriol. 1998. V. 180. No 21. P. 5749-5755.
22. Ghiselli G., Siracusa L.D., Iozzo R.V. Complete cDNA cloning, genomic organization, chromosomal assignment, functional characterization of the promoter, and expression of the murine Bamacan gene // J. Biol. Chem. 1999. V. 274. No 24. P. 17384-17393.
23. Jones S., Sgouros J. The cohesin complex: sequence homologies, interaction networks and shared motifs // Genome Biol. 2001. V. 2. No 3. P. 0009.1-0009.12.
24. Anderson D.E., Losada A., Erickson H.P., Hirano T. Condensin and cohesin display different arm conformations with characteristic hinge angles // J. Cell Biol. 2002. V. 28. P. 28.
25. 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. 1998. V. 142. No 6. P. 1595-1604.
26. Haering C.H., Lowe J., Hochwagen A., Nasmyth K. Molecular architecture of SMC proteins and the yeast cohesin complex // Mol. Cell. 2002. V. 9. No 4. P. 773-788.
27. Lowe 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. 2001. V. 306. No 1. P. 25-35.
28. Hirano M., Anderson D.E., Erickson H.P., Hirano T. Bimodal activation of SMC ATPase by intra- and intermolecular interactions // EMBO J. 2001. V. 20. No 12. P. 3238-3250.
29. Saitoh N., Goldberg I., Earnshaw W.C. The SMC proteins and the coming of age of the chromosome scaffold hypothesis // Bioessays. 1995. V. 17. No 9. P. 759-766.
30. Peterson C.L. The SMC family: novel motor proteins for chromosome condensation? // Cell. 1994. V. 79. No 3. P. 389-392.
31. Hirano T., Mitchison T.J., Swedlow J.R. The SMC family: from chromosome condensation to dosage compensation // Curr. Opin. Cell Biol. 1995. V. 7. No 3. P. 329-336.
32. Akhmedov A.T., Frei C., Tsai-Pflugfelder M. et al. Structural maintenance of chromosomes protein C-terminal domains bind preferentially to DNA with secondary structure // J. Biol. Chem. 1998. V. 273. No 37. P. 24088-24094.
33. 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. 1999. V. 274. No 53. P. 38216-38224.
34. Kimura K., Hirano T. ATP-dependent positive super-coiling of DNA by 13S condensin: a biochemical implication for chromosome condensation // Cell. 1997. V. 90. No 4. P. 625-634.
35. Kimura K., Hirano T. Dual roles of the 11S regulatory subcomplex in condensin functions // Proc. Natl Acad. Sci. USA. 2000. V. 97. No 22. P. 11972-11977.
36. Losada A., Hirano T. Intermolecular DNA interactions stimulated by the cohesin complex in vitro: implications for sister chromatid cohesion // Curr. Biol. 2001. V. 11. No 4. P. 268-272.
37. Hirano M., Hirano T. ATP-dependent aggregation of single-stranded DNA by a bacterial SMC homodimer // EMBO J. 1998. V. 17. No 23. P. 7139-7148.
38. 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. 1997. V. 91. No 1. P. 47-57.
39. Michaelis C., Ciosk R., Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids // Cell. 1997. V. 91. No 1. P. 35-45.
40. Losada A., Hirano M., Hirano T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion // Genes Dev. 1998. V. 12. No 13. P. 1986-1997.
41. 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. V. 89. No 4. P. 511-521.
42. Schmiesing J.A., Gregson H.C., Zliou 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. 2000. V. 20. No 18. P. 6996-7006.
43. Gregson H.C., VanHooser A.A., Ball A.R., Jr. et al. Localization of human SMC1 protein at kinetochores // Chromosome Res. 2002. V. 10. No 4. P. 267-277.
44. Ball Jr A.R., Yokomori K. The structural maintenance of chromosomes (SMC) family of proteins in mammals // Chromosome Res. 2001. V. 9. No 2. P. 85-96.
45. Cobbe N., Heck M.M. Review: SMCs in the world of chromosome biology-from prokaryotes to higher eukaryotes // J. Struct. Biol. 2000. V. 129. No 2-3. P. 123-143.
46. Hirano T. SMC protein complexes and higher-order chromosome dynamics // Curr. Opin. Cell Biol. 1998. V. 10. No 3. P. 317-322.
47. Hirano T. SMC-mediated chromosome mechanics: a conserved scheme from bacteria to vertebrates? // Genes Dev. 1999. V. 13. No 1. P. 11-19.
48. Hirano T. Chromosome cohesion, condensation, and separation // Annu. Rev. Biochem. 2000. V. 69. P. 115-144.
49. Jessberger R., Frei C., Gasser S.M. Chromosome dynamics: the SMC protein family // Curr. Opin. Genet. Dev. 1998. V. 8. No 2. P. 254-259.
50. Nasmyth K., Peters J.M., Uhlmann F. Splitting the chromosome: cutting the ties that bind sister chromatids // Science. 2000. V. 288. No 5470. P. 1379-1385.
51. Nasmyth K. Segregating sister genomes: the molecular biology of chromosome separation // Science. 2002. V. 297. No 5581. P. 559-565.
52. Strunnikov A.V. SMC proteins and chromosome structure // Trends Cell Biol. 1998. V. 8. No 11. P. 454-459.
53. Strunnikov A.V., Jessberger R. Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions // Eur. J. Biochem. 1999. V. 263. No 1. P. 6-13.
54. Taylor E.M., Moghraby J.S., Lees J.H. et al. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex // Mol. Biol. Cell. 2001. V. 12. No 6. P. 1583-1594.
55. Uhlmann F. Chromosome condensation: packaging the genome // Curr. Biol. 2001. V. 11. No 10. P. R384-387.
56. Lee J.Y., Orr-Weaver T.L. The molecular basis of sister-chromatid cohesion // Annu. Rev. Cell Dev. Biol. 2001. V. 17. P. 753-777.
57. Donze D., Adams C.R., Rine J., Kamakaka R.T. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae II Genes Dev. 1999. V. 13. No 6. P. 698-708.
58. Losada A., Hirano T. Shaping the metaphase chromosome: coordination of cohesion and condensation // Bioessays. 2001. V. 23. No 10. P. 924-935.
59. 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. 2000. V. 150. No 3. P. 405-416.
60. Toth A., Ciosk R., Uhlmann F. et al. Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication // Genes Dev. 1999. V. 13. No 3. P. 320-333.
61. Tomonaga T., Nagao K., Kawasaki Y. et al. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase // Genes Dev. 2000. V. 14. No 21. P. 2757-2770.
62. Sumara I., Vorlaufer E., Gieffers C. et al. Characterization of vertebrate cohesin complexes and their regulation in prophase // J. Cell Biol. 2000. V. 151. No 4. P. 749-762.
63. Darwiche N., Freeman L.A., Strunnikov A. Characterization of the components of the putative mammalian sister chromatid cohesion complex // Gene. 1999. V. 233. No 1-2. P. 39-47.
64. Skibbens R.V., Corson L.B., Koshland D., Hieter P. Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery // Genes Dev. 1999. V. 13. No 3. P. 307-319.
65. Ivanov D., Schleiffer A., Eisenhaber F. et al. Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion // Curr. Biol. 2002. V. 12. No 4. P. 323-328.
66. Tanaka K., Yonekawa T., Kawasaki Y. et al. Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase // Mol. Cell Biol. 2000. V. 20. No 10. P. 3459-3469.
67. Wang Z., Castano I.B., De Las Penas A. et al. Pol kappa: A DNA polymerase required for sister chromatid cohesion // Science. 2000. V. 289. No 5480. P. 774-779.
68. Mayer M.L., Gygi S.P., Aebersold R., Hieter P. Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae // Mol. Cell. 2001. V. 7. No 5. P. 959-970.
69. Ciosk R., Shirayama M., Shevchenko A. et al. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins // Mol. Cell. 2000. V. 5. No 2. P. 243-254.
70. Furuya K., Takahashi K., Yanagida M. Faithful anaphase is ensured by Mis4, a sister chromatid cohesion molecule required in S phase and not destroyed in G1 phase // Genes Dev. 1998. V. 12. No 21. P. 3408-3418.
71. 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. V. 151. No 3. P. 613-626.
72. Panizza S., Tanaka T., Hochwagen A. et al. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion // Curr. Biol. 2000. V. 10. No 24. P. 1557-1564.
73. 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. V. 20. No 20. P. 5779-5790.
74. Neuwald A.F., Hirano T. HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions // Genome Res. 2000. V. 10. No 10. P. 1445-1452.
75. Blat Y., Kleckner N. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region // Cell. 1999. V. 98. No 2. P. 249-259.
76. Laloraya S., Guacci V., Koshland D. Chromosomal addresses of the cohesin component Mcd1p // J. Cell Biol. 2000. V. 151. No 5. P. 1047-1056.
77. Megee P.C., Mistrot C., Guacci V., Koshland D. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences // Mol. Cell. 1999. V. 4. No 3. P. 445-450.
78. Sumara I., Vorlaufer E., Stukenberg P.T. et al. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase // Mol. Cell. 2002. V. 9. No 3. P. 515-525.
79. Gregson H.C., Schmiesing J.A., Kim J.S. et al. A potential role for human cohesin in mitotic spindle aster assembly // J. Biol. Chem. 2001. V. 276. No 50. P. 47575-47582.
80. Hoque M.T., Ishikawa F. Human chromatid cohesin component hRad21 is phosphorylated in M phase and associated with metaphase centromeres // J. Biol. Chem. 2001. V. 276. No 7. P. 5059-5067.
81. Warren W.D., Steffensen S., Lin E. et al. The Drosophila RAD21 cohesin persists at the centromere region in mitosis // Curr. Biol. 2000. V. 10. No 22. P. 1463-1466.
82. Sutani T., Yuasa T., Tomonaga T. et al. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4 // Genes Dev. 1999. V. 13. No 17. P. 2271-2283.
83. Freeman L., Aragon-Alcaide L., Strunnikov A. The condensin complex governs chromosome condensation and mitotic transmission of rDNA // J. Cell Biol. 2000. V. 149. No 4. P. 811-824.
84. 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. 1996. V. 87. No 6. P. 1103-1114.
85. Cabello O.A., Eliseeva E., He W.G. et al. Cell cycle-dependent expression and nucleolar localization of hCAP-H // Mol. Biol. Cell. 2001. V. 12. No 11. P. 3527-3537.
86. Yoshimura S.H., Hizume K., Murakami A. et al. Condensin architecture and interaction with DNA: regulatory non-SMC subunits bind to the head of SMC heterodimer // Curr. Biol. 2002. V. 12. No 6. P. 508-513.
87. Kimura K., Hirano M., Kobayashi R., Hirano T. Phosphorylation and activation of 13S condensin by Cdc2 in vitro // Science. 1998. V. 282. No 5388. P. 487-490.
88. Kimura K., Cuvier O., Hirano T. Chromosome condensation by a human condensin complex in Xenopus egg extracts // J. Biol. Chem. 2001. V. 276. No 8. P. 5417-5420.
89. 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. 2002. V. 156. No 5. P. 805-815.
90. Chu D.S., Dawes H.E., Lieb J.D. et al. A molecular link between gene-specific and chromosome-wide transcriptional repression // Genes Dev. 2002. V. 16. No 7. P. 796-805.
91. Ball A.R., Jr., Schmiesing J.A., Zhou C. et al. Identification of a chromosome-targeting domain in the human condensin subunit CNAP1/hCAP-D2/Eg7 // Mol. Cell Biol. 2002. V. 22. No 16. P. 5769-5781.
92. Hendzel M.J., Wei Y., Mancini M.A. et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation // Chromosoma. 1997. V. 106. No 6. P. 348-360.
93. MacCallum D.E., Losada A., Kobayashi R., Hirano T. ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B // Mol. Biol. Cell. 2002. V. 13. No 1. P. 25-39.
94. Eide T., Carlson C., Tasken K.A. et al. Distinct but overlapping domains of AKAP95 are implicated in chromosome condensation and condensin targeting // EMBO Rep. 2002. V. 18. No P. 18.
95. Steen R.L., Cubizolles F., Le Guellec K., Collas P. A kinase-anchoring protein (AKAP)95 recruits human chromosome-associated protein (hCAP)-D2/Eg7 for chromosome condensation in mitotic extract // J. Cell Biol. 2000. V. 149. No 3. P. 531-536.
96. Lupo R., Breiling A., Blanchi M.E., Orlando V. Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing // Mol. Cell. 2001. V. 7. No 1. P. 127-136.
97. Sutani T., Yanagida M. DNA renaturation activity of the SMC complex implicated in chromosome condensation // Nature. 1997. V. 388. No 6644. P. 798-801.
98. 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. 2002. V. 9. No 6. P. 1183-1190.
99. Kimura K., Rybenkov V.V., Crisona N.J. et al. 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation // Cell. 1999. V. 98. No 2. P. 239-248.
100. Uhlmann F., Nasmyth K. Cohesion between sister chromatids must be established during DNA replication // Curr. Biol. 1998. V. 8. No 20. P. 1095-1101.
101. Hauf S., Waizenegger I.C., Peters J.M. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells // Science. 2001. V. 293. No 5533. P. 1320-1323.
102. Jager H., Herzig A., Lehner C.F., Heidmann S. Drosophila separase is required for sister chromatid separation and binds to PIM and THR // Genes Dev. 2001. V. 15. No 19. P. 2572-2584.
103. Jallepalli P.V., Waizenegger I.C., Bunz F. et al. Securin is required for chromosomal stability in human cells // Cell. 2001. V. 105. No 4. P. 445-457.
104. Ciosk R., Zachariae W., Michaelis C. et al. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast // Cell. 1998. V. 93. No 6. P. 1067-1076.
105. 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. 2000. V. 103. No 3. P. 399-410.
106. Amon A. Together until separin do us part // Nat. Cell. Biol. 2001. V. 3. No 1. P. E12-14.
107. Alexandra G., Uhlmann F., Mechtler K. et al. Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast // Cell. 2001. V. 105. No 4. P. 459-472.
108. Chuang P.T., Lieb J.D., Meyer B.J. Sex-specific assembly of a dosage compensation complex on the nematode X chromosome // Science. 1996. V. 274. No 5293. P. 1736-1739.
109. 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. 1996. V. 274. No 5293. P. 1732-1736.
110. Carmi I., Meyer B.J. The primary sex determination signal of Caenorhabditis elegans // Genetics. 1999. V. 152. No 3. P. 999-1015.
111. Wood W.B., Streit A., Li W. Dosage compensation: X-repress yourself // Curr. Biol. 1997. V. 7. No 4. P. R227-R230.
112. Dawes H.E., Berlin D.S., Lapidus D.M. et al. Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate // Science. 1999. V. 284. No 5421. P. 1800-1804.
113. Kuroda M.I., Villeneuve A.M. Promiscuous chromosomal proteins: complexes about sex // Science. 1996. V. 274. No 5293. P. 1633-1634.
114. Klein F., Mahr P., Galova M. et al. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis // Cell. 1999. V. 98. No 1. P. 91-103.
115. Watanabe Y., Nurse P. Cohesin Rec8 is required for reductional chromosome segregation at meiosis // Nature. 1999. V. 400. No 6743. P. 461-464.
116. Prieto I., Suja J.A., Pezzi N. et al. Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I // Nat. Cell Biol. 2001. V. 3. No 8. P. 761-766.
117. Eijpe M., Heyting C., Gross B., Jessberger R. Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes // J. Cell Sci. 2000. V. 113. P. 673-682.
118. Jessberger R., Podust V., Hubscher U., Berg P. A mammalian protein complex that repairs double-strand breaks and deletions by recombination // J. Biol. Chem. 1993. V. 268. No 20. P. 15070-15079.
119. Stursberg S., Riwar B., Jessberger R. Cloning and characterization of mammalian SMC1 and SMC3 genes and proteins, components of the DNA recombination complexes RC-1 // Gene. 1999. V. 228. No 1-2. P. 1-12.
120. Mengiste T., Revenkova E., Bechtold N., Paszkowski J. An SMC-like protein is required for efficient homologous recombination in Arabidopsis // EMBO J. 1999. V. 18. No 16. P. 4505-4512.
121. Lehmann A.R., Walicka M., Griffiths D.J. et al. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair // Mol. Cell Biol. 1995. V. 15. No 12. P. 7067-7080.
122. Yonemasu R., McCready S.J., Murray J.M. et al. Characterization of the alternative excision repair pathway of UV-damaged DNA in Schizosaccharomyces pombe // Nucl. Acids Res. 1997. V. 25. No 8. P. 1553-1558.
123. Verkade H.M., Bugg S.J., Lindsay H.D. et al. Rad18 is required for DNA repair and checkpoint responses in fission yeast // Mol. Biol. Cell. 1999. V. 10. No 9. P. 2905-2918.