Jeppsson, K., Kanno, T., Shirahige, K. & Sjögren, C. The maintenance of chromosome structure: positioning and functioning of SMC complexes. Nat. Rev. Mol. Cell Biol. 15, 601–614 (2014).

CAS  PubMed  Article  Google Scholar 

Gligoris, T. & Löwe, J. Structural insights into ring formation of cohesin and related Smc complexes. Trends Cell Biol. 26, 680–693 (2016).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Alt, A. et al. Specialized interfaces of Smc5/6 control hinge stability and DNA association. Nat. Commun. 8, 14011 (2017).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Adamus, M. et al. Molecular Insights into the architecture of the human SMC5/6 complex. J. Mol. Biol. 432, 3820–3837 (2020).

CAS  PubMed  Article  Google Scholar 

Palecek, J., Vidot, S., Feng, M., Doherty, A. J. & Lehmann, A. R. The Smc5-Smc6 DNA repair complex: bridging of the Smc5-Smc6 heads by the kleisin, nse4, and non-kleisin subunits. J. Biol. Chem. 281, 36952–36959 (2006).

CAS  PubMed  Article  Google Scholar 

Kanno, T., Berta, D. G. & Sjögren, C. The Smc5/6 complex is an ATP-dependent intermolecular DNA linker. Cell Rep. 12, 1471–1482 (2015).

CAS  PubMed  Article  Google Scholar 

Aragón, L. The Smc5/6 complex: new and old functions of the enigmatic long-distance relative. Annu. Rev. Genet. 52, 89–107 (2018).

PubMed  Article  CAS  Google Scholar 

Palecek, J. J. SMC5/6: multifunctional player in replication. Genes 10, 7 (2019).

Article  CAS  Google Scholar 

Palecek, J. J. & Gruber, S. Kite proteins: a superfamily of SMC/kleisin partners conserved across bacteria, archaea, and eukaryotes. Structure 23, 2183–2190 (2015).

CAS  PubMed  Article  Google Scholar 

De Piccoli, G. et al. Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol. 8, 1032–1034 (2006).

PubMed  PubMed Central  Article  CAS  Google Scholar 

Potts, P. R., Porteus, M. H. & Yu, H. Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J. 25, 3377–3388 (2006).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Ampatzidou, E., Irmisch, A., O’Connell, M. J. & Murray, J. M. Smc5/6 is required for repair at collapsed replication forks. Mol. Cell. Biol. 26, 9387–9401 (2006).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Betts Lindroos, H. et al. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways. Mol. Cell 22, 755–767 (2006).

PubMed  Article  CAS  Google Scholar 

Menolfi, D., Delamarre, A., Lengronne, A., Pasero, P. & Branzei, D. Essential roles of the Smc5/6 complex in replication through natural pausing sites and endogenous DNA damage tolerance. Mol. Cell 60, 835–846 (2015).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Li, X. & Heyer, W.-D. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 18, 99–113 (2008).

CAS  PubMed  Article  Google Scholar 

Bermúdez-López, M. et al. The Smc5/6 complex is required for dissolution of DNA-mediated sister chromatid linkages. Nucleic Acids Res. 38, 6502–6512 (2010).

PubMed  PubMed Central  Article  CAS  Google Scholar 

Kegel, A. & Sjögren, C. The Smc5/6 complex: more than repair? Cold Spring Harb. Symp. Quant. Biol. 75, 179–187 (2010).

CAS  PubMed  Article  Google Scholar 

Jeppsson, K. et al. The chromosomal association of the Smc5/6 complex depends on cohesion and predicts the level of sister chromatid entanglement. PLoS Genet. 10, e1004680 (2014).

PubMed  PubMed Central  Article  CAS  Google Scholar 

Kegel, A. et al. Chromosome length influences replication-induced topological stress. Nature 471, 392–396 (2011).

CAS  PubMed  Article  Google Scholar 

Decorsière, A. et al. Hepatitis B virus X protein identifies the Smc5/6 complex as a host restriction factor. Nature 531, 386–389 (2016).

PubMed  Article  CAS  Google Scholar 

Murphy, C. M. et al. Hepatitis B virus X protein promotes degradation of SMC5/6 to enhance HBV replication. Cell Rep. 16, 2846–2854 (2016).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Li, T., Robert, E. I., van Breugel, P. C., Strubin, M. & Zheng, N. A promiscuous α-helical motif anchors viral hijackers and substrate receptors to the CUL4–DDB1 ubiquitin ligase machinery. Nat. Struct. Mol. Biol. 17, 105–112 (2010).

PubMed  Article  CAS  Google Scholar 

Abdul, F. et al. Smc5/6 antagonism by HBx is an evolutionarily conserved function of hepatitis B virus infection in mammals. J. Virol. 92, e00769-18 (2018).

CAS  PubMed  PubMed Central  Article  Google Scholar 

van Breugel, P. C. et al. Hepatitis B virus X protein stimulates gene expression selectively from extrachromosomal DNA templates. Hepatology 56, 2116–2124 (2012).

PubMed  Article  CAS  Google Scholar 

Dupont, L. et al. The SMC5/6 complex compacts and silences unintegrated HIV-1 DNA and is antagonized by Vpr. Cell Host Microbe 29, 792–805.e6 (2021).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Gibson, R. T. & Androphy, E. J. The SMC5/6 complex represses the replicative program of high-risk human papillomavirus type 31. Pathogens 9, 786 (2020).

CAS  PubMed Central  Article  Google Scholar 

Nagy, G. et al. Motif oriented high-resolution analysis of ChIP-seq data reveals the topological order of CTCF and cohesin proteins on DNA. BMC Genomics 17, 637 (2016).

PubMed  PubMed Central  Article  CAS  Google Scholar 

Sutani, T. et al. Condensin targets and reduces unwound DNA structures associated with transcription in mitotic chromosome condensation. Nat. Commun. 6, 7815 (2015).

PubMed  Article  Google Scholar 

Taylor, E. M., Copsey, A. C., Hudson, J. J. R., Vidot, S. & Lehmann, A. R. Identification of the proteins, including MAGEG1, that make up the human SMC5-6 protein complex. Mol. Cell. Biol. 28, 1197–1206 (2008).

CAS  PubMed  Article  Google Scholar 

Harvey, S. H., Krien, M. J. & O’Connell, M. J. Structural maintenance of chromosomes (SMC) proteins, a family of conserved ATPases. Genome Biol. 3, reviews3003.1 (2002).

Article  Google Scholar 

Arumugam, P. et al. ATP hydrolysis is required for cohesin’s association with chromosomes. Curr. Biol. 13, 1941–1953 (2003).

CAS  PubMed  Article  Google Scholar 

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).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Guerineau, M. et al. Analysis of the Nse3/MAGE-binding domain of the Nse4/EID family proteins. PLoS ONE 7, e35813 (2012).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Hudson, J. J. R. et al. Interactions between the Nse3 and Nse4 components of the SMC5-6 complex identify evolutionarily conserved interactions between MAGE and EID families. PLoS ONE 6, e17270 (2011).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Vondrova, L. et al. A role of the Nse4 kleisin and Nse1/Nse3 KITE subunits in the ATPase cycle of SMC5/6. Sci. Rep. 10, 9694 (2020).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Venegas, A. B., Natsume, T., Kanemaki, M. & Hickson, I. D. Inducible degradation of the human SMC5/6 complex reveals an essential role only during interphase. Cell Rep. 31, 107533 (2020).

CAS  PubMed  Article  Google Scholar 

Jo, A., Li, S., Shin, J. W., Zhao, X. & Cho, Y. Structure basis for shaping the Nse4 protein by the Nse1 and Nse3 dimer within the Smc5/6 complex. J. Mol. Biol. 433, 166910 (2021).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Zabrady, K. et al. Chromatin association of the SMC5/6 complex is dependent on binding of its NSE3 subunit to DNA. Nucleic Acids Res. 44, 1064–1079 (2016).