In through the out door: A loop-binding-first model for topological cohesin loading.
SMC complex
chromosome cohesion
cohesin
Journal
BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851
Informations de publication
Date de publication:
19 Aug 2024
19 Aug 2024
Historique:
revised:
04
08
2024
received:
26
05
2024
accepted:
09
08
2024
medline:
19
8
2024
pubmed:
19
8
2024
entrez:
19
8
2024
Statut:
aheadofprint
Résumé
Cohesin is a ring-shaped complex that is loaded on DNA in two different conformations. In one conformation, it forms loops to organize the interphase genome; in the other, it topologically encircles sibling chromosomes to facilitate homologous recombination and to establish the cohesion that is required for orderly segregation during mitosis. How, and even if, these two loading conformation are related is unclear. Here, I propose that loop binding is a required first step for topological binding. This loop-binding-first model integrates the known information about the two loading mechanisms, explains genetic requirements for the two and explains how topological loading evolved from loop binding.
Identifiants
pubmed: 39159466
doi: 10.1002/bies.202400120
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2400120Subventions
Organisme : NIGMS NIH HHS
ID : R35GM148359
Pays : United States
Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Hoencamp, C., & Rowland, B. D. (2023). Genome control by SMC complexes. Nature Reviews Molecular Cell Biology, 24, 633–650.
Pradhan, B., Kanno, T., Igarashi, M. U., Loke, M. S., Baaske, M. D., Wong, J. S. K., Jeppsson, K., Björkegren, C., & Kim, E. (2023). The Smc5/6 complex is a DNA loop‐extruding motor. Nature, 616, 843–848.
Davidson, I. F., Bauer, B., Goetz, D., Tang, W., Wutz, G., & Peters, J. M. (2019). DNA loop extrusion by human cohesin. Science, 366, 1338–1345.
Ganji, M., Shaltiel, I. A., Bisht, S., Kim, E., Kalichava, A., Haering, C. H., & Dekker, C. (2018). Real‐time imaging of DNA loop extrusion by condensin. Science, 360, 102–105.
Haering, C. H., Farcas, A. M., Arumugam, P., Metson, J., & Nasmyth, K. (2008). The cohesin ring concatenates sister DNA molecules. Nature, 454, 297–301.
Taschner, M., & Gruber, S. (2023). DNA segment capture by Smc5/6 holocomplexes. Nature Structural & Molecular Biology, 30, 619–628.
Bürmann, F., Funke, L. F. H., Chin, J. W., & Löwe, J. (2021). Cryo‐EM structure of MukBEF reveals DNA loop entrapment at chromosomal unloading sites. Molecular Cell, 81, 4891–4906.e8.
Kim, E., Barth, R., & Dekker, C. (2023). Looping the genome with SMC complexes. Annual Review of Biochemistry, 92, 15–41.
Wang, X., Brandão, H. B., Le, T. B., Laub, M. T., & Rudner, D. Z. (2017). Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science, 355, 524–527.
Srinivasan, M., Fumasoni, M., Petela, N. J., Murray, A., & Nasmyth, K. A. (2020). Cohesion is established during DNA replication utilising chromosome associated cohesin rings as well as those loaded de novo onto nascent DNAs. eLife, 9, e56611.
Sjögren, C., & Nasmyth, K. (2001). Sister chromatid cohesion is required for postreplicative double‐strand break repair in Saccharomyces cerevisiae. Current Biology, 11, 991–995.
Kitajima, T. S., Sakuno, T., Ishiguro, K., Iemura, S., Natsume, T., Kawashima, S. A., & Watanabe, Y. (2006). Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature, 441, 46–52.
Murayama, Y., & Uhlmann, F. (2015). DNA entry into and exit out of the cohesin ring by an interlocking gate mechanism. Cell, 163, 1628–1640.
Higashi, T. L., Eickhoff, P., Sousa, J. S., Locke, J., Nans, A., Flynn, H. R., Snijders, A. P., Papageorgiou, G., O'Reilly, N., Chen, Z. A., Costa, A., & Uhlmann, F. (2020). A structure‐based mechanism for DNA entry into the cohesin ring. Molecular Cell, 79, 917–933.e9.
Tanaka, K., Hao, Z., Kai, M., & Okayama, H. (2001). Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. The EMBO Journal, 20, 5779–5790.
Hartman, T., Stead, K., Koshland, D., & Guacci, V. (2000). Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. Journal of Cell Biology, 151, 613–626.
Kikuchi, S., Borek, D. M., Otwinowski, Z., Tomchick, D. R., & Yu, H. (2016). Crystal structure of the cohesin loader Scc2 and insight into cohesinopathy. Proceedings of the National Academy of Sciences of the United States of America, 113, 12444–12449.
Petela, N. J., Gligoris, T. G., Metson, J., Lee, B. G., Voulgaris, M., Hu, B., Kikuchi, S., Chapard, C., Chen, W., Rajendra, E., Srinivisan, M., Yu, H., Löwe, J., & Nasmyth, K. A. (2018). Scc2 is a potent activator of cohesin's ATPase that promotes loading by binding Scc1 without Pds5. Molecular Cell, 70, 1134–1148.e7.
Murayama, Y., & Uhlmann, F. (2014). Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature, 505, 367–371.
Ciosk, R., Shirayama, M., Shevchenko, A., Tanaka, T., Toth, A., Shevchenko, A., & Nasmyth, K. (2000). Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Molecular Cell, 5, 243–254.
Srinivasan, M., Scheinost, J. C., Petela, N. J., Gligoris, T. G., Wissler, M., Ogushi, S., Collier, J. E., Voulgaris, M., Kurze, A., Chan, K. L., Hu, B., Costanzo, V., & Nasmyth, K. A. (2018). The cohesin ring uses its hinge to organize DNA using non‐topological as well as topological mechanisms. Cell, 173, 1508–1519.e18.
Gruber, S., Arumugam, P., Katou, Y., Kuglitsch, D., Helmhart, W., Shirahige, K., & Nasmyth, K. (2006). Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell, 127, 523–537.
Collier, J. E., & Nasmyth, K. A. (2022). DNA passes through cohesin's hinge as well as its Smc3‐kleisin interface. eLife, 11, e80310.
Wutz, G., Várnai, C., Nagasaka, K., Cisneros, D. A., Stocsits, R. R., Tang, W., Schoenfelder, S., Jessberger, G., Muhar, M., Hossain, M. J., Walther, N., Koch, B., Kueblbeck, M., Ellenberg, J., Zuber, J., Fraser, P., & Peters, J. M. (2017). Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. The EMBO Journal, 36, 3573–3599.
Beckouët, F., Hu, B., Roig, M. B., Sutani, T., Komata, M., Uluocak, P., Katis, V. L., Shirahige, K., & Nasmyth, K. (2010). An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Molecular Cell, 39, 689–699.
Kueng, S., Hegemann, B., Peters, B. H., Lipp, J. J., Schleiffer, A., Mechtler, K., & Peters, J. M. (2006). Wapl controls the dynamic association of cohesin with chromatin. Cell, 127, 955–967.
Kinoshita, K., Tsubota, Y., Tane, S., Aizawa, Y., Sakata, R., Takeuchi, K., Shintomi, K., Nishiyama, T., & Hirano, T. (2022). A loop extrusion‐independent mechanism contributes to condensin I‐mediated chromosome shaping. Journal of Cell Biology, 221, e202109016.
Tang, M., Pobegalov, G., Tanizawa, H., Chen, Z. A., Rappsilber, J., Molodtsov, M., Noma, K. I., & Uhlmann, F. (2023). Establishment of dsDNA‐dsDNA interactions by the condensin complex. Molecular Cell, 83, 3787–3800.e9.
Nagasaka, K., Davidson, I. F., Stocsits, R. R., Tang, W., Wutz, G., Batty, P., Panarotto, M., Litos, G., Schleiffer, A., Gerlich, D. W., & Peters, J. M. (2023). Cohesin mediates DNA loop extrusion and sister chromatid cohesion by distinct mechanisms. Molecular Cell, 83, 3049–3063.e6.