SMC蛋白结构和功能的研究进展
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摘要
染色体不仅仅由DNA构成,还包含一些使染色体能具有特定形态特征以及在基因表达和基因组稳定性中起作用的蛋白。而使染色体能具有特定形态特征的首要物质就是染色体结构维持蛋白(structural maintenance of chromosomes,SMC)复合体。SMC复合体包含凝聚蛋白(condensin)、黏结蛋白(cohesin)和SMC5-SMC6复合体,是染色体的重要组分。SMC蛋白的表达依赖于ATP的水解以及DNA的拓扑作用。SMC复合体参与了多重染色体行为,其中尤为显著的是染色体集缩和姐妹染色单体的黏着。此外,SMC复合体在DNA修复中也有重要的作用。近年来,随着分子生物学研究技术的发展,对该类复合体的结构、功能及作用机制等方面已有较多研究并取得一些重要进展,本文对SMC蛋白结构和功能的研究进展做一综述。
引文
[1]Niki H,JafféA,Imamura R,et al.The new gene mukB codes for a177 kd protein with coiled‐coil domains involved in chromosome partitioning of E.coli[J].EMBO Journal,1991,10(1):183-193.
[2]Strunnikov A V,Larionov V L,Koshland D,et al.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].Journal of Cell Biology,1993,123(6 Pt 2):1635-1648.
[3]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[J].EMBO Journal,1994,13(20):4938-4952.
[4]Hirano T,Mitchison T J.A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro[J].Cell,1994,79(3):449-458.
[5]Saitoh N,Goldberg I G,Wood E R,et al.ScⅡ:an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure[J].Journal of Cell Biology,1994,127(2):303-318.
[6]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[J].Genes&Development,1995,9(5):587-599.
[7]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[J].Cell,1994,79(3):459-474.
[8]Lehmann A R,Walicka M,Griffiths D J,et al.The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMCsuperfamily involved in DNA repair[J].Molecular&Cellular Biology,1995,15(12):7067-7080.
[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[J].Cell,1997,89(4):511-521.
[10]Birkenbihl R P,Subramani S.Cloning and characterization of rad21an essential gene of Schizosaccharomyces pombe involved in DNAdouble-strand-break repair[J].Nucleic Acids Research,1992,20(24):6605-6611.
[11]Uhlmann F,Nasmyth K.Cohesion between sister chromatids must be established during DNA replication[J].Current Biology,1998,8(20):1095-1101.
[12]Uhlmann F,Lottspeich F,Nasmyth K.Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1[J].Nature,1999,400(6739):37-42.
[13]Uhlmann F,Wernic D,Poupart M A,et al.Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast[J].Cell,2000,103(3):375-386.
[14]Waizenegger I C,Hauf S,Meinke A,et al.Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase[J].Cell,2000,103(3):399-410.
[15]王洪振,程军,刘春明.SMC蛋白在有丝分裂染色体集缩中的作用研究进展[J].吉林师范大学学报(自然科学版),2007,28(1):71-73.
[16]张国莉,文建凡.SMC蛋白复合体的结构、功能和作用机制[J].生命的化学,2016,28(1):40-43.
[17]Revenkova E,Eijpe M,Heyting C,et al.Novel meiosis-specific isoform of mammalian SMC1[J].Molecular&Cellular Biology,2001,21(20):6984.
[18]Ono T,Losada A,Hirano M,et al.Differential contributions of condensinⅠand condensinⅡto mitotic chromosome architecture in vertebrate cells[J].Cell,2003,115(1):109-121.
[19]Str9m L,Karlsson C,Lindroos H B,et al.Postreplicative formation of cohesion is required for repair and induced by a single DNA break[J].Science,2007,317(5835):242-245.
[20]Haering C H,Schoffnegger D,Nishino T,et al.Structure and stability of cohesin’s Smc1-kleisin interaction[J].Molecular Cell,2004,15(6):951-964.
[21]Bürmann F,Shin H C,Basquin J,et al.An asymmetric SMC-kleisin bridge in prokaryotic condensin[J].Nature Structural&Molecular Biology,2013,20(3):371-379.
[22]Gligoris T G,Scheinost J C,Bürmann F,et al.Closing the cohesin ring:structure and function of its Smc3-kleisin interface[J].Science,2014,346(6212):963-967.
[23]Haering C H,Farcas A M,Arumugam P A,et al.The cohesin ring concatenates sister DNA molecules[J].Nature,2008,454(7202):297-301.
[24]Murayama Y,Uhlmann F.Biochemical reconstitution of topological DNA binding by the cohesin ring[J].Nature,2014,505(7483):367-371.
[25]Cuylen S,Metz J,Haering C H.Condensin structures chromosomal DNA through topological links[J].Nature Structural and Molecular Biology,2011,22(8):894-901.
[26]Kanno T,Berta D G,Sj9gren C.The Smc5/6 complex is an ATP-Dependent intermolecular DNA linker[J].Cell Reports,2015,12(9):1471-1482.
[27]Wilhelm L,Bürmann F,Minnen A,et al.SMC condensin entraps chromosomal DNA by an ATP hydrolysis dependent loading mechanism in Bacillus subtilis[J].e LIFE,2015,4:e06659.
[28]Kagansky A,Freeman L,Lukyanov D,et al.Histone tailindependent chromatin binding activity of recombinant cohesin holocomplex[J].Journal of Biological Chemistry,2004,279(5):3382-3388.
[29]张一帆,张兴义,姜睿,等.SMC1A在肿瘤领域的研究[J].中国实验诊断学,2012,16(12):2350-2354.
[30]Losada A,Hirano T.Dynamic molecular linkers of the genome:the first decade of SMC proteins[J].Genes Dev,2005,19(11):1269-1287.
[31]Mehta G D,Rizvi S M A,Ghosh S K.Cohesin:a guardian of genome integrity[J].Biochimica et Biophysica Acta-Molecular Cell Research,2012,1823(8):1324-1342.
[32]Skibbens R V,Maradeo M,Eastman L.Fork it over:the cohesion establishment factor Ctf7p and DNA replication[J].Journal of Cell Science,2007,120(15):2471-2477.
[33]Surcel A,Koshland D,Ma H,et al.Cohesin interaction with centromeric minichromosomes shows a Multi-Complex RodShaped structure[J].PLo S One,2008,3(6):e2453.
[34]Bauerschmidt C,Arrichiello C,Burdak-Rothkamm S,et al.Cohesin promotes the repair of ionizing radiation-induced DNAdouble-strand breaks in replicated chromatin[J].Nucleic Acids Research,2010,38(2):477-487.
[35]Lou Z K,Minter-Dykhouse K,Franco S,et al.MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals[J].Molecular Cell,2006,21(2):187-200.
[36]Watrin E,Peters J M.The cohesin complex is required for the DNAdamage-induced G2/M checkpoint in mammalian cells[J].EMBOJournal,2009,28(17):2625-2635.
[37]王洪振,杨斯涵,李桂英.真核生物集缩素SMC2/SMC4异二聚体的结构解析研究进展[J].中国细胞生物学学报,2018,40(3):439-447.
[38]Liu C C,Mcelver J,Tzafrir I,et al.Condensin and cohesin knockouts in Arabidopsis exhibit a titan seed phenotype[J].The Plant Journal,2002,29(4):405-415.
[39]Freeman L,Aragon-Alcaide L,Strunnikov A.The condensin complex governs chromosome condensation and mitotic transmission of r DNA[J].The Journal of Cell Biology,2000,149(4):811-824.
[40]Menolfi D,Delamarre A,Lengronne A,et al.Essential roles of the Smc5/6 complex in replication through natural pausing sites and endogenous DNA damage tolerance[J].Molecular Cell,2015,60(6):835-846.
[41]靳全文.裂殖酵母核仁蛋白Dnt1通过调控集缩素蛋白(Condensin)实现抑制姊妹染色体的错误分离[C]//中国细胞生物学学会全体会员代表大会暨第十二次学术大会论文集.北京,2011:146.
[42]Murray J M,Carr A M.Smc5/6:a link between DNA repair and unidirectional replication?[J].Nature Reviews Molecular Cell Biology,2008,9(2):177-182.
[43]Jeppsson K,Carlborg K K,Nakato R,et al.The chromosomal association of the Smc5/6 complex depends on cohesion and predicts the level of sister chromatid entanglement[J].PLo S Genetics,2014,10(10):e1004680.
[44]Palecek J J,Gruber S.Kite proteins:a superfamily of SMC/kleisin partners conserved across Bacteria,Archaea,and Eukaryotes[J].Structure,2015,23(12):2183-2190.
[45]Andrews E A,Palecek J,Sergeant J,et al.Nse2,a component of the Smc5-6 complex,is a SUMO ligase required for the response to DNA damage[J].Molecular and Cellular Biology,2005,25(1):185-196.
[46]de Piccoli G,Cortes-Ledesma F,Ira G,et al.Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination[J].Nature Cell Biology,2006,8(9):1032-1034.
[47]Zabrady K,Adamus M,Vondrova L,et al.Chromatin association of the SMC5/6 complex is dependent on binding of its NSE3 subunit to DNA[J].Nucleic Acids Research,2016,44(3):1064-1079.
[48]Harvey S H,Sheedy D M,Cuddihy A R,et al.Coordination of DNAdamage responses via the Smc5/Smc6 complex[J].Molecular and Cellular Biology,2004,24(2):662-674.
[49]Str9m L,Lindroos H B,Shirahige K,et al.Postreplicative recruitment of cohesin to double-strand breaks is required for DNArepair[J].Molecular Cell,2004,16(6):1003-1015.
[50]nal E,Arbel-Eden A,Sattler U,et al.DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain[J].Molecular Cell,2004,16(6):991-1002.
[51]Lindroos H B,Str9m L,Itoh T,et al.Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways[J].Molecular Cell,2006,22(6):755-767.
[52]Copsey A,Tang S M,Jordan P W,et al.Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions[J].PLo S Genetics,2013,9(12):e1004071.
[2]Strunnikov A V,Larionov V L,Koshland D,et al.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].Journal of Cell Biology,1993,123(6 Pt 2):1635-1648.
[3]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[J].EMBO Journal,1994,13(20):4938-4952.
[4]Hirano T,Mitchison T J.A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro[J].Cell,1994,79(3):449-458.
[5]Saitoh N,Goldberg I G,Wood E R,et al.ScⅡ:an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure[J].Journal of Cell Biology,1994,127(2):303-318.
[6]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[J].Genes&Development,1995,9(5):587-599.
[7]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[J].Cell,1994,79(3):459-474.
[8]Lehmann A R,Walicka M,Griffiths D J,et al.The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMCsuperfamily involved in DNA repair[J].Molecular&Cellular Biology,1995,15(12):7067-7080.
[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[J].Cell,1997,89(4):511-521.
[10]Birkenbihl R P,Subramani S.Cloning and characterization of rad21an essential gene of Schizosaccharomyces pombe involved in DNAdouble-strand-break repair[J].Nucleic Acids Research,1992,20(24):6605-6611.
[11]Uhlmann F,Nasmyth K.Cohesion between sister chromatids must be established during DNA replication[J].Current Biology,1998,8(20):1095-1101.
[12]Uhlmann F,Lottspeich F,Nasmyth K.Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1[J].Nature,1999,400(6739):37-42.
[13]Uhlmann F,Wernic D,Poupart M A,et al.Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast[J].Cell,2000,103(3):375-386.
[14]Waizenegger I C,Hauf S,Meinke A,et al.Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase[J].Cell,2000,103(3):399-410.
[15]王洪振,程军,刘春明.SMC蛋白在有丝分裂染色体集缩中的作用研究进展[J].吉林师范大学学报(自然科学版),2007,28(1):71-73.
[16]张国莉,文建凡.SMC蛋白复合体的结构、功能和作用机制[J].生命的化学,2016,28(1):40-43.
[17]Revenkova E,Eijpe M,Heyting C,et al.Novel meiosis-specific isoform of mammalian SMC1[J].Molecular&Cellular Biology,2001,21(20):6984.
[18]Ono T,Losada A,Hirano M,et al.Differential contributions of condensinⅠand condensinⅡto mitotic chromosome architecture in vertebrate cells[J].Cell,2003,115(1):109-121.
[19]Str9m L,Karlsson C,Lindroos H B,et al.Postreplicative formation of cohesion is required for repair and induced by a single DNA break[J].Science,2007,317(5835):242-245.
[20]Haering C H,Schoffnegger D,Nishino T,et al.Structure and stability of cohesin’s Smc1-kleisin interaction[J].Molecular Cell,2004,15(6):951-964.
[21]Bürmann F,Shin H C,Basquin J,et al.An asymmetric SMC-kleisin bridge in prokaryotic condensin[J].Nature Structural&Molecular Biology,2013,20(3):371-379.
[22]Gligoris T G,Scheinost J C,Bürmann F,et al.Closing the cohesin ring:structure and function of its Smc3-kleisin interface[J].Science,2014,346(6212):963-967.
[23]Haering C H,Farcas A M,Arumugam P A,et al.The cohesin ring concatenates sister DNA molecules[J].Nature,2008,454(7202):297-301.
[24]Murayama Y,Uhlmann F.Biochemical reconstitution of topological DNA binding by the cohesin ring[J].Nature,2014,505(7483):367-371.
[25]Cuylen S,Metz J,Haering C H.Condensin structures chromosomal DNA through topological links[J].Nature Structural and Molecular Biology,2011,22(8):894-901.
[26]Kanno T,Berta D G,Sj9gren C.The Smc5/6 complex is an ATP-Dependent intermolecular DNA linker[J].Cell Reports,2015,12(9):1471-1482.
[27]Wilhelm L,Bürmann F,Minnen A,et al.SMC condensin entraps chromosomal DNA by an ATP hydrolysis dependent loading mechanism in Bacillus subtilis[J].e LIFE,2015,4:e06659.
[28]Kagansky A,Freeman L,Lukyanov D,et al.Histone tailindependent chromatin binding activity of recombinant cohesin holocomplex[J].Journal of Biological Chemistry,2004,279(5):3382-3388.
[29]张一帆,张兴义,姜睿,等.SMC1A在肿瘤领域的研究[J].中国实验诊断学,2012,16(12):2350-2354.
[30]Losada A,Hirano T.Dynamic molecular linkers of the genome:the first decade of SMC proteins[J].Genes Dev,2005,19(11):1269-1287.
[31]Mehta G D,Rizvi S M A,Ghosh S K.Cohesin:a guardian of genome integrity[J].Biochimica et Biophysica Acta-Molecular Cell Research,2012,1823(8):1324-1342.
[32]Skibbens R V,Maradeo M,Eastman L.Fork it over:the cohesion establishment factor Ctf7p and DNA replication[J].Journal of Cell Science,2007,120(15):2471-2477.
[33]Surcel A,Koshland D,Ma H,et al.Cohesin interaction with centromeric minichromosomes shows a Multi-Complex RodShaped structure[J].PLo S One,2008,3(6):e2453.
[34]Bauerschmidt C,Arrichiello C,Burdak-Rothkamm S,et al.Cohesin promotes the repair of ionizing radiation-induced DNAdouble-strand breaks in replicated chromatin[J].Nucleic Acids Research,2010,38(2):477-487.
[35]Lou Z K,Minter-Dykhouse K,Franco S,et al.MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals[J].Molecular Cell,2006,21(2):187-200.
[36]Watrin E,Peters J M.The cohesin complex is required for the DNAdamage-induced G2/M checkpoint in mammalian cells[J].EMBOJournal,2009,28(17):2625-2635.
[37]王洪振,杨斯涵,李桂英.真核生物集缩素SMC2/SMC4异二聚体的结构解析研究进展[J].中国细胞生物学学报,2018,40(3):439-447.
[38]Liu C C,Mcelver J,Tzafrir I,et al.Condensin and cohesin knockouts in Arabidopsis exhibit a titan seed phenotype[J].The Plant Journal,2002,29(4):405-415.
[39]Freeman L,Aragon-Alcaide L,Strunnikov A.The condensin complex governs chromosome condensation and mitotic transmission of r DNA[J].The Journal of Cell Biology,2000,149(4):811-824.
[40]Menolfi D,Delamarre A,Lengronne A,et al.Essential roles of the Smc5/6 complex in replication through natural pausing sites and endogenous DNA damage tolerance[J].Molecular Cell,2015,60(6):835-846.
[41]靳全文.裂殖酵母核仁蛋白Dnt1通过调控集缩素蛋白(Condensin)实现抑制姊妹染色体的错误分离[C]//中国细胞生物学学会全体会员代表大会暨第十二次学术大会论文集.北京,2011:146.
[42]Murray J M,Carr A M.Smc5/6:a link between DNA repair and unidirectional replication?[J].Nature Reviews Molecular Cell Biology,2008,9(2):177-182.
[43]Jeppsson K,Carlborg K K,Nakato R,et al.The chromosomal association of the Smc5/6 complex depends on cohesion and predicts the level of sister chromatid entanglement[J].PLo S Genetics,2014,10(10):e1004680.
[44]Palecek J J,Gruber S.Kite proteins:a superfamily of SMC/kleisin partners conserved across Bacteria,Archaea,and Eukaryotes[J].Structure,2015,23(12):2183-2190.
[45]Andrews E A,Palecek J,Sergeant J,et al.Nse2,a component of the Smc5-6 complex,is a SUMO ligase required for the response to DNA damage[J].Molecular and Cellular Biology,2005,25(1):185-196.
[46]de Piccoli G,Cortes-Ledesma F,Ira G,et al.Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination[J].Nature Cell Biology,2006,8(9):1032-1034.
[47]Zabrady K,Adamus M,Vondrova L,et al.Chromatin association of the SMC5/6 complex is dependent on binding of its NSE3 subunit to DNA[J].Nucleic Acids Research,2016,44(3):1064-1079.
[48]Harvey S H,Sheedy D M,Cuddihy A R,et al.Coordination of DNAdamage responses via the Smc5/Smc6 complex[J].Molecular and Cellular Biology,2004,24(2):662-674.
[49]Str9m L,Lindroos H B,Shirahige K,et al.Postreplicative recruitment of cohesin to double-strand breaks is required for DNArepair[J].Molecular Cell,2004,16(6):1003-1015.
[50]nal E,Arbel-Eden A,Sattler U,et al.DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain[J].Molecular Cell,2004,16(6):991-1002.
[51]Lindroos H B,Str9m L,Itoh T,et al.Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways[J].Molecular Cell,2006,22(6):755-767.
[52]Copsey A,Tang S M,Jordan P W,et al.Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions[J].PLo S Genetics,2013,9(12):e1004071.