The cost of sensitive response and accurate adaptation in networks with an incoherent type-1 feed-forward loop

Journal of the Royal Society Interface

Volumn 10, Issue 87, 2013, Pages

  Lan, Ganhui ^a   Tu, Yuhai ^b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b IBM T J WATSON RESEARCH CENTER   (United States)

Author keywords

Adaptation accuracy; Energy dissipation; Incoherent type 1 feed forward loop; Non equilibrium system; Sensitivity

Indexed keywords

ENERGY DISSIPATION;

ADAPTATION ACCURACY; BIOCHEMICAL CIRCUITS; CELLULAR ADAPTATION; ENERGY DISSIPATION RATE; FEEDFORWARD LOOPS; NONEQUILIBRIUM SYSTEM; SENSITIVITY; SHORT-TIME RESPONSE;

COSTS;

ARTICLE; ENERGY COST; EUKARYOTIC CELL; INCOHERENT TYPE 1 FEED FORWARD LOOP; NEGATIVE FEEDBACK; PHOSPHORYLATION AND DEPHOSPHORYLATION; REGULATORY MECHANISM; ADAPTATION; ADAPTATION ACCURACY; BIOLOGICAL MODEL; CHEMISTRY; ENERGY DISSIPATION; FEEDBACK SYSTEM; INCOHERENT TYPE-1 FEED-FORWARD LOOP; KINETICS; NON-EQUILIBRIUM SYSTEM; SENSITIVITY;

EUKARYOTA;

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAS PROTEIN;

ADAPTATION ACCURACY; ENERGY DISSIPATION; INCOHERENT TYPE-1 FEED-FORWARD LOOP; NON-EQUILIBRIUM SYSTEM; SENSITIVITY;

ADAPTATION, BIOLOGICAL; FEEDBACK, PHYSIOLOGICAL; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; KINETICS; MODELS, BIOLOGICAL; RAS PROTEINS;

EID: 84883226338     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2013.0489     Document Type: Article

References (31)

1. Alon U. 2007 Network motifs: theory and experimental approaches. Nat. Rev. Genet. 8, 450-461. (doi:10.1038/nrg2102)
2. Alon U. 2007 An introduction to systems biology: design principles of biological circuits, vol. 10. New York, NY: CRC Press.
3. Eichenberger P et al. 2004 The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2, e328. (doi:10.1371/journal.pbio.0020328)
4. Lee TI et al. 2002 Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298, 799-804. (doi:10.1126/science.1075090)
5. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U. 2002 Network motifs: simple building blocks of complex networks. Science 298, 824-827. (doi:10.1126/science.298.5594.824)
6. Odom DT et al. 2004 Control of pancreas and liver gene expression by HNF transcription factors. Science 303, 1378-1381. (doi:10.1126/science.1089769)
7. Boyer LA et al. 2005 Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956. (doi:10.1016/j.cell.2005.08.020)
8. Swiers G, Patient R, Loose M. 2006 Genetic regulatory networks programming hematopoietic stem cells and erythroid lineage specification. Dev. Biol. 294, 525-540. (doi:10.1016/j.ydbio.2006.02.051)
9. Basu S, Mehreja R, Thiberge S, Chen MT, Weiss R. 2004 Spatiotemporal control of gene expression with pulse-generating networks. Proc. Natl Acad. Sci. USA 101, 6355-6360. (doi:10.1073/pnas.0307571101)
10. Mangan S, Alon U. 2003 Structure and function of the feed-forward loop network motif. Proc. Natl Acad. Sci. USA 100, 11 980-11 985. (doi:10.1073/pnas.2133841100)
11. Mangan S, Itzkovitz S, Zaslaver A, Alon U. 2006 The incoherent feed-forward loop accelerates the responsetime of the gal system of Escherichia coli. J. Mol. Biol. 356, 1073-1081. (doi:10.1016/j.jmb.2005.12.003)
12. Goentoro L, Shoval O, Kirschner MW, Alon U. 2009 The incoherent feedforward loop can provide foldchange detection in gene regulation. Mol. Cell 36, 894-899. (doi:10.1016/j.molcel.2009.11.018)
13. Goentoro L, Kirschner MW. 2009 Evidence that foldchange, and not absolute level, of b-catenin dictates Wnt signaling. Mol. Cell 36, 872-884. (doi:10.1016/j.molcel.2009.11.017)
14. Shoval O, Goentoro L, Hart Y, Mayo A, Sontag E, Alon U. 2010 Fold-change detection and scalar symmetry of sensory input fields. Proc. Natl Acad. Sci. USA 107, 15 995-16 000. (doi:10.1073/pnas. 1002352107)
15. Behar M, Hao N, Dohlman HG, Elston TC. 2007 Mathematical and computational analysis of adaptation via feedback inhibition in signal transduction pathways. Biophys. J. 93, 806-821. (doi:10.1529/biophysj.107. 107516)
16. Ma W, Trusina A, El-Samad H, Lim WA, Tang C. 2009 Defining network topologies that can achieve biochemical adaptation. Cell 138, 760-773. (doi:10.1016/j.cell.2009.06.013)
17. Shen-Orr SS, Milo R, Mangan S, Alon U. 2002 Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31, 64-68. (doi:10.1038/ng881)
18. Parent CA, Devreotes PN. 1999 A cell's sense of direction. Science 284, 765-770. (doi:10.1126/science.284.5415.765)
19. Levchenko A, Iglesias PA. 2002 Models of eukaryotic gradient sensing: application to chemotaxis of amoebae and neutrophils. Biophys. J. 82, 50-62. (doi:10.1016/S0006-3495(02)75373-3)
20. Takeda K, Shao D, Adler M, Charest PG, Loomis WF, Levine H, Groisman A, Rappel WJ, Firtel RA. 2012 Incoherent feedforward control governs adaptation of activated Ras in a eukaryotic chemotaxis pathway. Sci. Signal. 5, p. ra2. (doi:10.1126/scisignal. 2002413)
21. Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J. 2000 Molecular cell biology. New York, NY: W. H. Freeman.
22. Vigil D, Cherfils J, Rossman KL, Der CJ. 2010 Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat. Rev. Cancer 10, 842-857. (doi:10.1038/nrc2960)
23. Lan G, Sartori P, Neumann S, Sourjik V, Tu Y. 2012 The energy-speed-accuracy tradeoff in sensory adaptation. Nat. Phys. 8, 422-428. (doi:10.1038/nphys2276)
24. Michaelis L, Menten ML. 1913 Die Kinetik der Invertinwirkung. Biochem. Z 49, 333-369.
25. Van Kampen NG. 1981 Stochastic processes in physics and chemistry. Amsterdam, The Netherlands: North-Holland Physics Publishing.
26. Qian H. 2007 Phosphorylation energy hypothesis: open chemical systems and their biological functions. Annu. Rev. Phys. Chem. 58, 113-142. (doi:10.1146/annurev. physchem.58.032806.104550)
27. Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D, Tawfik DS, Milo R. 2011 The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50, 4402-4410. (doi:10.1021/bi2002289)
28. Ueda M, Shibata T. 2007 Stochastic signal processing and transduction in chemotactic response of eukaryotic cells. Biophys. J. 93, 11-20. (doi:10.1529/biophysj.106.100263)
29. Voet D, Voet JG, Pratt CW. 1999 Fundamentals of biochemistry. New York, NY: Wiley.
30. Hopfield JJ. 1974 Kinetics proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl Acad. Sci. USA 71, 4135-4139. (doi:10.1073/pnas.71.10.4135)
31. Qian H. 2006 Reducing intrinsic biochemical noise in cells and its thermodynamic limit. J. Mol. Biol. 362, 387-392. (doi:10.1016/j.jmb.2006.07.068)