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R Soc Open Sci. 2015 Nov 25;2(11):150486. doi: 10.1098/rsos.150486. eCollection 2015 Nov.

Only accessible information is useful: insights from gradient-mediated patterning.

Royal Society open science

Mikhail Tikhonov, Shawn C Little, Thomas Gregor

Affiliations

  1. Joseph Henry Laboratories of Physics , Princeton University , Princeton, NJ 08544, USA ; Harvard Center of Mathematical Sciences and Applications , Harvard University , Cambridge, MA 02138, USA ; Harvard John A. Paulson School of Engineering and Applied Sciences, Harvard University , Cambridge, MA 02138, USA ; Kavli Institute for Bionano Science and Technology, Harvard University , Cambridge, MA 02138, USA.
  2. Joseph Henry Laboratories of Physics , Princeton University , Princeton, NJ 08544, USA ; Lewis-Sigler Institute for Integrative Genomics, Princeton University , Princeton, NJ 08544, USA.

PMID: 26716005 PMCID: PMC4680620 DOI: 10.1098/rsos.150486

Abstract

Information theory is gaining popularity as a tool to characterize performance of biological systems. However, information is commonly quantified without reference to whether or how a system could extract and use it; as a result, information-theoretic quantities are easily misinterpreted. Here, we take the example of pattern-forming developmental systems which are commonly structured as cascades of sequential gene expression steps. Such a multi-tiered structure appears to constitute sub-optimal use of the positional information provided by the input morphogen because noise is added at each tier. However, one must distinguish between the total information in a morphogen and information that can be usefully extracted and interpreted by downstream elements. We demonstrate that quantifying the information that is accessible to the system naturally explains the prevalence of multi-tiered network architectures as a consequence of the noise inherent to the control of gene expression. We support our argument with empirical observations from patterning along the major body axis of the fruit fly embryo. We use this example to highlight the limitations of the standard information-theoretic characterization of biological signalling, which are frequently de-emphasized, and illustrate how they can be resolved.

Keywords: Drosophila; developmental biology; genetic regulation; information theory

References

  1. Biochim Biophys Acta. 2011 Oct;1810(10):924-32 - PubMed
  2. Curr Opin Genet Dev. 1993 Aug;3(4):585-94 - PubMed
  3. Exp Cell Res. 2014 Feb 1;321(1):25-31 - PubMed
  4. Phys Rev Lett. 2009 Dec 18;103(25):258101 - PubMed
  5. Curr Opin Biotechnol. 2014 Aug;28:149-55 - PubMed
  6. Birth Defects Res C Embryo Today. 2006 Sep;78(3):224-42 - PubMed
  7. Development. 2013 Apr;140(8):1621-38 - PubMed
  8. Annu Rev Genet. 2013;47:483-508 - PubMed
  9. Cell. 2007 Jul 13;130(1):153-64 - PubMed
  10. Mol Syst Biol. 2013;9:639 - PubMed
  11. Curr Opin Genet Dev. 2012 Aug;22(4):331-8 - PubMed
  12. Dev Biol. 1996 May 1;175(2):314-24 - PubMed
  13. Cell. 2013 Aug 15;154(4):789-800 - PubMed
  14. Phys Rev Lett. 2009 May 29;102(21):218101 - PubMed
  15. Phys Rev E Stat Nonlin Soft Matter Phys. 2010 Apr;81(4 Pt 1):041905 - PubMed
  16. Trends Neurosci. 2004 Dec;27(12):727-34 - PubMed
  17. J Theor Biol. 1969 Oct;25(1):1-47 - PubMed
  18. Cold Spring Harb Perspect Biol. 2009 Sep;1(3):a001255 - PubMed
  19. Genome Biol. 2009;10 (7):R80 - PubMed
  20. Phys Biol. 2014 Apr;11(2):026004 - PubMed
  21. Science. 1970 Jun 26;168(3939):1545-50 - PubMed
  22. Curr Biol. 2014 Jun 2;24(11):1283-8 - PubMed
  23. Curr Opin Genet Dev. 2010 Aug;20(4):443-7 - PubMed
  24. Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Apr;85(4 Pt 1):041903 - PubMed
  25. PLoS One. 2008 Jul 23;3(7):e2774 - PubMed
  26. Curr Opin Biotechnol. 2014 Aug;28:156-64 - PubMed
  27. Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16301-8 - PubMed
  28. PLoS Comput Biol. 2013;9(3):e1002965 - PubMed
  29. Exp Cell Res. 2014 Feb 1;321(1):11-6 - PubMed
  30. Science. 1996 Nov 15;274(5290):1109-15 - PubMed
  31. PLoS Comput Biol. 2014 Jan;10(1):e1003408 - PubMed
  32. Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Sep;80(3 Pt 1):031920 - PubMed
  33. PLoS Biol. 2008 Feb;6(2):e27 - PubMed
  34. Genetics. 2015 Jan;199(1):39-59 - PubMed
  35. Science. 2013 Feb 22;339(6122):923-7 - PubMed
  36. Science. 2014 Dec 12;346(6215):1370-3 - PubMed
  37. Annu Rev Biophys Biomol Struct. 2007;36:413-34 - PubMed
  38. Science. 2012 Apr 13;336(6078):183-7 - PubMed
  39. Curr Opin Genet Dev. 2012 Apr;22(2):79-85 - PubMed
  40. Development. 1991 Feb;111(2):601-9 - PubMed
  41. Science. 2011 Oct 21;334(6054):354-8 - PubMed
  42. Curr Opin Genet Dev. 2012 Dec;22(6):542-6 - PubMed
  43. Curr Opin Genet Dev. 2011 Dec;21(6):726-31 - PubMed
  44. Curr Opin Genet Dev. 2012 Dec;22(6):553-61 - PubMed
  45. Cell. 1988 Jul 1;54(1):83-93 - PubMed
  46. Science. 2013 Dec 6;342(6163):1188-93 - PubMed
  47. Annu Rev Cell Dev Biol. 2011;27:377-407 - PubMed
  48. Proc Natl Acad Sci U S A. 2014 Mar 11;111(10):3683-8 - PubMed

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