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Chromosoma

, Volume 117, Issue 2, pp 103–110 | Cite as

Beyond the code: the mechanical properties of DNA as they relate to mitosis

  • Kerry S. BloomEmail author
Mini-Review

Introduction

As students of mitosis, we seek to identify the DNA and protein components required for chromosome segregation and to design experiments in order to test our latest theory on how these components fit together. The identification of what is approaching a complete parts list has provided major advances in the past few years. The problem on the horizon is to understand how the parts fit together to segregate the complete genetic complement to daughter cells with the accuracy required to form complex organisms. Historically, science is guided by our observations, thus much of our intuition stems from how we interact with our environment. We make analogies based on our experiences and use these to help us begin to think about processes inside a cell. The problem lies in that life inside a cell is nothing like our life.

There are several physical concepts to consider as we delve into the life of a cell. One is the sense of scale. As we think small (i.e., micrometers), consider...

Keywords

Sister Chromatid Chromosome Segregation Persistence Length Sister Centromere Kinetochore Microtubule 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

I would like to thank Dr. Elaine Yeh, Dr. Jay Fisher, Rachael Bloom, Julian Haase, and Ben Harrison for discussion and critical comments on the manuscript and Julian Haase for artwork.

References

  1. Baum M, Ngan VK, Clarke L (1994) The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol Biol Cell 5:747–761PubMedGoogle Scholar
  2. Baumann C, Korner R, Hofmann K, Nigg EA (2007) PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128:101–114PubMedCrossRefGoogle Scholar
  3. Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259PubMedCrossRefGoogle Scholar
  4. Bloom K, Amaya E, Yeh E (1984) Centromeric DNA structure in yeast. In: Borsey GG, Cleveland DW, Murphy DB (eds) Molecular biology of the cytoskeleton. Cold Spring Harbor Laboratory, New York, pp 175–184Google Scholar
  5. Bloom K, Sharma S, Dokholyan NV (2006) The path of DNA in the kinetochore. Curr Biol 16:R276–R278PubMedCrossRefGoogle Scholar
  6. Brower-Toland BD, Smith CL, Yeh RC, Lis JT, Peterson CL, Wang MD (2002) Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc Natl Acad Sci USA 99:1960–1965PubMedCrossRefGoogle Scholar
  7. Camahort R, Li B, Florens L, Swanson SK, Washburn MP, Gerton JL (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol Cell 26:853–865PubMedCrossRefGoogle Scholar
  8. Cui Y, Bustamante C (2000) Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc Natl Acad Sci USA 97:127–132PubMedCrossRefGoogle Scholar
  9. Dickinson RB, Caro L, Purich DL (2004) Force generation by cytoskeletal filament end-tracking proteins. Biophys J 87:2838–2854PubMedCrossRefGoogle Scholar
  10. Ding R, McDonald KL, McIntosh JR (1993) Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J Cell Biol 120:141–151PubMedCrossRefGoogle Scholar
  11. Fitzgerald-Hayes M, Clarke L, Carbon J (1982) Nucleotide sequence comparisons and functional analysis of yeast centromere DNAs. Cell 29:235–244PubMedCrossRefGoogle Scholar
  12. Gittes F, Mickey B, Nettleton J, Howard J (1993) Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol 120:923–934PubMedCrossRefGoogle Scholar
  13. Gore J, Bryant Z, Nollmann M, Le MU, Cozzarelli NR, Bustamante C (2006) DNA overwinds when stretched. Nature 442:836–839PubMedCrossRefGoogle Scholar
  14. Grishchuk EL, Molodtsov MI, Ataullakhanov FI, McIntosh JR (2005) Force production by disassembling microtubules. Nature 438:384–388PubMedCrossRefGoogle Scholar
  15. Hays TS, Salmon ED (1990) Poleward force at the kinetochore in metaphase depends on the number of kinetochore microtubules. J Cell Biol 110:391–404PubMedCrossRefGoogle Scholar
  16. He D, Brinkley BR (1996) Structure and dynamic organization of centromeres/prekinetochores in the nucleus of mammalian cells. J Cell Sci 109(Pt 11):2693–2704PubMedGoogle Scholar
  17. Howard J (2001) Mechanics of motor proteins and the cytoskeleton. Sinauer, SunderlandGoogle Scholar
  18. Jannink G, Duplantier B, Sikorav JL (1996) Forces on chromosomal DNA during anaphase. Biophys J 71:451–465PubMedCrossRefGoogle Scholar
  19. Joglekar AP, Bouck DC, Molk JN, Bloom KS, Salmon ED (2006) Molecular architecture of a kinetochore-microtubule attachment site. Nat Cell Biol 8:581–585PubMedCrossRefGoogle Scholar
  20. Jun S, Mulder B (2006) Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA 103:12388–12393PubMedCrossRefGoogle Scholar
  21. Marshall WF, Marko JF, Agard DA, Sedat JW (2001) Chromosome elasticity and mitotic polar ejection force measured in living Drosophila embryos by four-dimensional microscopy-based motion analysis. Curr Biol 11:569–578PubMedCrossRefGoogle Scholar
  22. McAinsh AD, Tytell JD, Sorger PK (2003) Structure, function, and regulation of budding yeast kinetochores. Annu Rev Cell Dev Biol 19:519–539PubMedCrossRefGoogle Scholar
  23. Meluh PB, Yang P, Glowczewski L, Koshland D, Smith MM (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94:607–613PubMedCrossRefGoogle Scholar
  24. Mizuguchi G, Xiao H, Wisniewski J, Smith MM, Wu C (2007) Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129:1153–1164PubMedCrossRefGoogle Scholar
  25. Nicklas RB (1963) A quantitative study of chromosomal elasticity and its influence on chromosome movement. Chromosoma 14:276–295PubMedCrossRefGoogle Scholar
  26. Nicklas RB (1965) Chromosome velocity during mitosis as a function of chromosome size and position. J Cell Biol 25(Suppl):119–135PubMedCrossRefGoogle Scholar
  27. Nicklas RB (1983) Measurements of the force produced by the mitotic spindle in anaphase. J Cell Biol 97:542–548PubMedCrossRefGoogle Scholar
  28. Nicklas RB (1984) A quantitative comparison of cellular motile systems. Cell Motil 4:1–5PubMedCrossRefGoogle Scholar
  29. Nicklas RB (1988) The forces that move chromosomes in mitosis. Annu Rev Biophys Biophys Chem 17:431–449PubMedCrossRefGoogle Scholar
  30. O’Toole ET, Winey M, McIntosh JR (1999) High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell 10:2017–2031PubMedGoogle Scholar
  31. Pearson CG, Maddox PS, Salmon ED, Bloom K (2001) Budding yeast chromosome structure and dynamics during mitosis. J Cell Biol 152:1255–1266PubMedCrossRefGoogle Scholar
  32. Pietrasanta LI, Thrower D, Hsieh W, Rao S, Stemmann O, Lechner J, Carbon J, Hansma H (1999) Probing the Saccharomyces cerevisiae centromeric DNA (CEN DNA)-binding factor 3 (CBF3) kinetochore complex by using atomic force microscopy. Proc Natl Acad Sci USA 96:3757–3762PubMedCrossRefGoogle Scholar
  33. Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC (1995) The centromere: hub of chromosomal activities. Science 270:1591–1594PubMedCrossRefGoogle Scholar
  34. Purcell, EM (1977) Life at low Reynolds number. Am J Phys 45:3–11CrossRefGoogle Scholar
  35. Reynolds O (1883) An experimental investigation of the circumstances which determine whether the motion of water shall be direct or sinuous, and the law of resistance in parallel channels. Philos Trans R Soc Lond 174:935–982CrossRefGoogle Scholar
  36. Sharp JA, Franco AA, Osley MA, Kaufman PD (2002) Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev 16:85–100PubMedCrossRefGoogle Scholar
  37. Stoler S, Rogers K, Weitze S, Morey L, Fitzgerald-Hayes M, Baker RE (2007) Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc Natl Acad Sci USA 104:10571–10576PubMedCrossRefGoogle Scholar
  38. Waters JC, Skibbens RV, Salmon ED (1996) Oscillating mitotic newt lung cell kinetochores are, on average, under tension and rarely push. J Cell Sci 109(Pt 12):2823–2831PubMedGoogle Scholar
  39. Willard HF (1990) Centromeres of mammalian chromosomes. Trends Genet 6:410–416PubMedCrossRefGoogle Scholar
  40. Yan J, Maresca TJ, Skoko D, Adams CD, Xiao B, Christensen MO, Heald R, Marko JF (2006) Micromanipulation studies of chromatin fibers in Xenopus egg extracts reveal ATP-dependent chromatin assembly dynamics. Mol Biol Cell 18:464–474PubMedCrossRefGoogle Scholar
  41. Zinkowski RP, Meyne J, Brinkley BR (1991) The centromere–kinetochore complex: a repeat subunit model. J Cell Biol 113:1091–1110PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of BiologyUniversity of North Carolina at Chapel HillChapel HillUSA

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