The 3D Topography of Mitotic Chromosomes

Mol Cell. 2020 Sep 17;79(6):902-916.e6. doi: 10.1016/j.molcel.2020.07.002. Epub 2020 Aug 7.

Abstract

A long-standing conundrum is how mitotic chromosomes can compact, as required for clean separation to daughter cells, while maintaining close parallel alignment of sister chromatids. Pursuit of this question, by high resolution 3D fluorescence imaging of living and fixed mammalian cells, has led to three discoveries. First, we show that the structural axes of separated sister chromatids are linked by evenly spaced "mini-axis" bridges. Second, when chromosomes first emerge as discrete units, at prophase, they are organized as co-oriented sister linear loop arrays emanating from a conjoined axis. We show that this same basic organization persists throughout mitosis, without helical coiling. Third, from prophase onward, chromosomes are deformed into sequential arrays of half-helical segments of alternating handedness (perversions), accompanied by correlated kinks. These arrays fluctuate dynamically over <15 s timescales. Together these discoveries redefine the foundation for thinking about the evolution of mitotic chromosomes as they prepare for anaphase segregation.

Keywords: chromatin loops; chromosome axes; chromosome coiling; chromosome compaction; helical perversions; mitotic chromosomes; sister chromatids; spatial patterning.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Anaphase / genetics
  • Animals
  • Cell Cycle Proteins / genetics*
  • Cell Cycle Proteins / isolation & purification
  • Chromatids / genetics
  • Chromosomal Proteins, Non-Histone
  • Chromosomes / genetics*
  • DNA Topoisomerases, Type II / genetics
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / isolation & purification
  • Imaging, Three-Dimensional
  • Mammals
  • Metaphase / genetics
  • Mitosis / genetics*
  • Prophase / genetics

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Adenosine Triphosphatases
  • DNA Topoisomerases, Type II