Topoisomerase II mediates meiotic crossover interference.

Citation:

Zhang L, Wang S, Yin S, Hong S, Kim KP, Kleckner N. Topoisomerase II mediates meiotic crossover interference. Nature. 2014;511 (7511) :551-6.

Date Published:

2014 Jul 31

Abstract:

Spatial patterning is a ubiquitous feature of biological systems. Meiotic crossovers provide an interesting example, defined by the classic phenomenon of crossover interference. Here we identify a molecular pathway for interference by analysing crossover patterns in budding yeast. Topoisomerase II plays a central role, thus identifying a new function for this critical molecule. SUMOylation (of topoisomerase II and axis component Red1) and ubiquitin-mediated removal of SUMOylated proteins are also required. The findings support the hypothesis that crossover interference involves accumulation, relief and redistribution of mechanical stress along the protein/DNA meshwork of meiotic chromosome axes, with topoisomerase II required to adjust spatial relationships among DNA segments.

Key Publications by Subject Area

Chromosomes as Mechanical Objects

• Kleckner, N., Zickler, D., Jones, G.H., Henle, J., Dekker, J. and Hutchinson, J. 2004. A mechanical basis for chromosome function. Proc. Natl. Acad. Sci. USA, 101, 12592-12597.

• Fisher, J.K. and Kleckner, N. 2014. Magnetic Force Micropiston: an integrated force microfluidic device for the application of compressive forces in a confined environment. Rev. Sci. Instrum. 85 023704 (2014)

Mammalian chromosome dynamics

• Liang, Z., Zickler, D., Prentiss, M., Chang, F.S., Witz, G., Maeshima, K. and Kleckner, N. 2015. Chromosomes progress to metaphase in multiple discrete steps via global compaction/expansion cycles. Cell 161: 1124-1137.

E.coli chromosome dynamics

• Fisher, J.K., Bourniquel, A., Witz, G., Weiner, B., Prentiss, M. and Kleckner, N. 2013. Four-dimensional imaging of E. coli organization and dynamics in living cells. Cell 153, 882-895.

• Kleckner, N., Fisher, J.K., Stouf, M., White, M.A., Bates, D. and Witz, G. 2014. The bacterial nucleoid: nature, dynamics and sister segregation. Curr. Opin. Microbiol. 22: 127-137.

Meiotic Crossover Interference

• Zhang, L., Wang, S., Yin, S., Hong, S. Kim, K.P. and Kleckner, N. 2014. Topoisomerase II mediates meiotic crossover interference. Nature 511: 551-556.

• Zhang, L, Espagne, E., De Muyt, A., Zickler, D. and Kleckner, N. 2014. Interference-mediated synaptonemal complex formation with embedded crossover-designation. Proc. Natl. Acad. Sci. U.S.A. 111(47):E5059-68. doi: 10.1073/pnas.1416411111.

• Wang, S., Zickler, D., Kleckner, N. and Zhang, L. 2015. Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process. Cell Cycle, 14(3): 305-314.

Homologous Chromosome Pairing

• Zickler, D. and Kleckner, N. 2015. Recombination, pairing and synapsis of homologs in meiosis. In Kowalczykowski, S., Hunter, N. and Heyer, W.-D., DNA Replication (Cold Spring Harbor: Cold Spring Harbor Press) Cold Spring Harb Perspect Biol 2015;7:a016626 doi: 10.1101/CSHPERSPECT.a016626.

• Gladyshev E. and Kleckner, N. 2014. Direct recognition of homology between double helices of DNA in Neurospora crassa. Nat. Commun. 5: 3509 doi: 10.1038/ncomms4509.

• Mirkin, E.V., Chang, F. S. and Kleckner, N. 2013. Dynamic trans interactions in yeast chromosomes. PLoS One 8(9): e75895. doi:10.1371/journal.pone.0075895

• Danilowicz, C., Lee, C.H., Kim K., Hatch, K., Coljee, V.W., Kleckner, N. and Prentiss, M. 2009. Single molecule detection of direct, homologous DNA/DNA pairing. Proc. Natl. Acad. Sci. USA, 106, 19,824-19,829.

• Weiner, B.M. and Kleckner, N. 1994. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977-991.

• Burgess, S.M., Kleckner, N. and Weiner, B.M. 1999. Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev. 13, 1627-1641.

• Kleckner, N. and Weiner, B.M. 1993. Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic and premeiotic cells. Cold Spring Harbor Symp. Quant. Biol. 58: 553-565.

Meiotic Sordaria Chromosomes

• De Muyt A, Zhang, L., Piolot, T., Kleckner, N., Espagne,, E. and Zickler D. 2014. E3 ligase Hei10: a multi-faceted structure-based signaling molecule with roles within and beyond meiosis. Genes Dev 28: 1111-1123.

• Storlazzi, A., Gargano, S., Ruprich-Robert, G., Falque, M., David, M., Kleckner, N. and Zickler, D. 2010. Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141 94-106.

Nancy Kleckner

Herchel Smith Professor of Molecular Biology

Topoisomerase II mediates meiotic crossover interference.

Citation:

Date Published:

Abstract:

Key Publications by Subject Area