Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope.

Citation:

Koszul R, Kim KP, Prentiss M, Kleckner N, Kameoka S. Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell. 2008;133 (7) :1188-201.

Date Published:

2008 Jun 27

Abstract:

Chromosome movement is prominent during meiosis. Here, using a combination of in vitro and in vivo approaches, we elucidate the basis for dynamic mid-prophase telomere-led chromosome motion in budding yeast. Diverse findings reveal a process in which, at the pachytene stage, individual telomere/nuclear envelope (NE) ensembles attach passively to, and then move in concert with, nucleus-hugging actin cables that are continuous with the global cytoskeletal actin network. Other chromosomes move in concert with lead chromosome(s). The same process, in modulated form, explains the zygotene "bouquet" configuration in which, immediately preceding pachytene, chromosome ends colocalize dynamically in a restricted region of the NE. Mechanical properties of the system and biological roles of mid-prophase movement for meiosis, including recombination, are discussed.

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

Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope.

Citation:

Date Published:

Abstract:

Key Publications by Subject Area