1932

Abstract

Many essential processes in biology share a common fundamental step—establishing physical contact between distant segments of DNA. How fast this step is accomplished sets the “speed limit” for the larger-scale processes it enables, whether the process is antibody production by the immune system or tissue differentiation in a developing embryo. This naturally leads us to ask, How long does it take for DNA segments that are strung out over millions of base pairs along the chromatin fiber to find each other in the crowded cell? This question, fundamental to biology, can be recognized as the physics problem of the first-passage time, or the waiting time for the first encounter. Here, we review a number of approaches to revealing the physical principles by which cells solve, with astonishing efficiency, the first-passage problem for remote genomic interactions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-062215-010925
2016-07-05
2024-10-16
Loading full text...

Full text loading...

/deliver/fulltext/biophys/45/1/annurev-biophys-062215-010925.html?itemId=/content/journals/10.1146/annurev-biophys-062215-010925&mimeType=html&fmt=ahah

Literature Cited

  1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. 1.  2007. Molecular Biology of the Cell New York: Garland Sci, 5th. [Google Scholar]
  2. Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A. 2.  et al. 2014. Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol. Cell 55:383–96 [Google Scholar]
  3. ben-Avraham D, Havlin S. 3.  2000. Diffusion and Reactions in Fractals and Disordered Systems Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  4. Bénichou O, Voituriez R. 4.  2008. Narrow-escape time problem: time needed for a particle to exit a confining domain through a small window. Phys. Rev. Lett. 100:168105 [Google Scholar]
  5. Bialek W.5.  2012. Biophysics: Searching for Principles Princeton, NJ: Princeton Univ. Press [Google Scholar]
  6. Bickmore WA, van Steensel B. 6.  2013. Genome architecture: domain organization of interphase chromosomes. Cell 152:1270–84 [Google Scholar]
  7. Blackwood EM, Kadonaga JT. 7.  1998. Going the distance: a current view of enhancer action. Science 281:60–63 [Google Scholar]
  8. Bohn M, Heermann DW. 8.  2010. Diffusion-driven looping provides a consistent framework for chromatin organization. PLOS ONE 5:8e12218 [Google Scholar]
  9. Bronstein I, Israel Y, Kepten E, Mai S, Shav-Tal Y. 9.  et al. 2009. Transient anomalous diffusion of telomeres in the nucleus of mammalian cells. Phys. Rev. Lett. 103:018102 [Google Scholar]
  10. Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O. 10.  et al. 2006. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441:770–73 [Google Scholar]
  11. Condamin S, Bénichou O, Tejedor V, Voituriez R, Klafter J. 11.  2007. First-passage times in complex scale-invariant media. Nature 450:77–80 [Google Scholar]
  12. Cremer T, Cremer C. 12.  2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2:292–301 [Google Scholar]
  13. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. 13.  1999. Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145:1119–31 [Google Scholar]
  14. de Gennes PG. 14.  1971. Reptation of a polymer chain in the presence of fixed obstacles. J. Chem. Phys. 55:572–79 [Google Scholar]
  15. Dekker J, Rippe K, Dekker M, Kleckner N. 15.  2002. Capturing chromosome conformation. Science 295:1206–11 [Google Scholar]
  16. Deng W, Barkai E. 16.  2009. Ergodic properties of fractional Brownian-Langevin motion. Phys. Rev. E 79:011112 [Google Scholar]
  17. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y. 17.  et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80 [Google Scholar]
  18. Doi M, Edwards SF. 18.  1986. The Theory of Polymer Dynamics New York: Oxford Univ. Press [Google Scholar]
  19. Ferko MC, Patterson BW, Butler PJ. 19.  2006. High-resolution solid modeling of biological samples imaged with 3D fluorescence microscopy. Microsc. Res. Tech. 69:648–55 [Google Scholar]
  20. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, Kleckner N. 20.  2013. Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell 153:882–95 [Google Scholar]
  21. Grunstein M.21.  1997. Histone acetylation in chromatin structure and transcription. Nature 389:349–52 [Google Scholar]
  22. He Y, Burov S, Metzler R, Barkai E. 22.  2008. Random time-scale invariant diffusion and transport coefficients. Phys. Rev. Lett. 101:058101 [Google Scholar]
  23. Jeon JH, Metzler R. 23.  2010. Fractional Brownian motion and motion governed by the fractional Langevin equation in confined geometries. Phys. Rev. E 81:021103 [Google Scholar]
  24. Jeon JH, Metzler R. 24.  2012. Inequivalence of time and ensemble averages in ergodic systems: exponential versus power-law relaxation in confinement. Phys. Rev. E 85:021147 [Google Scholar]
  25. Jhunjhunwala S, van Zelm MC, Peak MM, Cutchin S, Riblet R. 25.  et al. 2008. The 3D structure of the immunoglobulin heavy-chain locus: implications for long-range genomic interactions. Cell 133:265–79 [Google Scholar]
  26. Kou SC, Xie XS. 26.  2004. Generalized Langevin equation with fractional Gaussian noise: subdiffusion within a single protein molecule. Phys. Rev. Lett. 93:180603 [Google Scholar]
  27. Krivega I, Dean A. 27.  2012. Enhancer and promoter interactions—long distance calls. Curr. Opin. Genet. Dev. 22:79–85 [Google Scholar]
  28. Lamond AI, Earnshaw WC. 28.  1998. Structure and function in the nucleus. Science 280:547–53 [Google Scholar]
  29. Langevin P.29.  1908. Sur la théorie du mouvement brownien [On the theory of Brownian motion]. C. R. Acad. Sci. (Paris) 146:530–33 [Google Scholar]
  30. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T. 30.  et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93 [Google Scholar]
  31. Lin YC, Benner C, Mansson R, Heinz S, Miyazaki K. 31.  et al. 2012. Global changes in the nuclear positioning of genes and intra- and interdomain genomic interactions that orchestrate B cell fate. Nat. Immunol. 13:1196–204 [Google Scholar]
  32. Lucas JS, Zhang Y, Dudko OK, Murre C. 32.  2014. 3D trajectories adopted by coding and regulatory DNA elements: first-passage times for genomic interactions. Cell 158:339–52 [Google Scholar]
  33. Lutz E.33.  2001. Fractional Langevin equation. Phys. Rev. E 64:051106 [Google Scholar]
  34. Metzler R, Klafter J. 34.  2000. The random walk's guide to anomalous diffusion: a fractional dynamics approach. Phys. Rep. 339:11–77 [Google Scholar]
  35. Montroll EW, Weiss GH. 35.  1965. Random walks on lattices. II. J. Math. Phys. 6:167–81 [Google Scholar]
  36. Niki H, Yamaichi Y, Hiraga S. 36.  2000. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 14:212–23 [Google Scholar]
  37. Nitzan A.37.  2006. Chemical Dynamics in Condensed Phases: Relaxation, Transfer, and Reactions in Condensed Molecular Systems New York: Oxford Univ. Press [Google Scholar]
  38. Pastor RW, Zwanzig R, Szabo A. 38.  1996. Diffusion limited first contact of the ends of a polymer: comparison of theory with simulation. J. Chem. Phys. 105:3878–82 [Google Scholar]
  39. Phillips R, Kondev J, Theriot J, Garcia HG. 39.  2012. Physical Biology of the Cell London/New York: Garland Sci, 2nd ed.. [Google Scholar]
  40. Qian H.40.  2003. Fractional Brownian motion and fractional Gaussian noise. Processes with Long-Range Correlations: Theory and Applications Rangarajan G, Ding M. 22–33 New York: Springer [Google Scholar]
  41. Redner S.41.  2001. A Guide to First-Passage Processes Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  42. Rouse PE.42.  1953. A theory of the linear viscoelastic properties of dilute solutions of coiling polymers. J. Chem. Phys. 21:1272–80 [Google Scholar]
  43. Saxton MJ.43.  1994. Anomalous diffusion due to obstacles: a Monte Carlo study. Biophys. J. 66:394–401 [Google Scholar]
  44. Saxton MJ.44.  1996. Anomalous diffusion due to binding: a Monte Carlo study. Biophys. J. 70:1250–62 [Google Scholar]
  45. Spector DL.45.  2003. The dynamics of chromosome organization and gene regulation. Annu. Rev. Biochem. 72:573–608 [Google Scholar]
  46. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P. 46.  et al. 2006. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev. 20:2349–54 [Google Scholar]
  47. Thanbichler M, Wang SC, Shapiro L. 47.  2005. The bacterial nucleoid: a highly organized and dynamic structure. J. Cell. Biochem. 96:506–21 [Google Scholar]
  48. Tonegawa S.48.  1983. Somatic generation of antibody diversity. Nature 302:575–81 [Google Scholar]
  49. Vazquez J, Belmont AS, Sedat JW. 49.  2001. Multiple regimes of constrained chromosome motion are regulated in the interphase Drosophila nucleus. Curr. Biol. 11:1227–39 [Google Scholar]
  50. Weber SC, Spakowitz AJ, Theriot JA. 50.  2010. Bacterial chromosomal loci move subdiffusively through a viscoelastic cytoplasm. Phys. Rev. Lett. 104:238102 [Google Scholar]
  51. Weber SC, Thompson MA, Moerner WE, Spakowitz AJ, Theriot JA. 51.  2012. Analytical tools to distinguish the effects of localization error, confinement, and medium elasticity on the velocity autocorrelation function. Biophys. J. 102:2443–50 [Google Scholar]
  52. Woodcock CL, Ghosh RP. 52.  2010. Chromatin higher-order structure and dynamics. Cold Spring Harb. Perspect. Biol. 2:a000596 [Google Scholar]
  53. Zimm BH.53.  1956. Dynamics of polymer molecules in dilute solution: viscoelasticity, flow birefringence and dielectric loss. J. Chem. Phys. 24:269–78 [Google Scholar]
  54. Zink D, Cremer T, Saffrich R, Fischer R, Trendelenburg MF. 54.  et al. 1998. Structure and dynamics of human interphase chromosome territories in vivo. Hum. Genet. 102:241–51 [Google Scholar]
/content/journals/10.1146/annurev-biophys-062215-010925
Loading
/content/journals/10.1146/annurev-biophys-062215-010925
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error