Synthetic incoherent feedforward circuits show adaptation to the amount of their genetic template

Molecular Systems Biology

Volumn 7, Issue , 2011, Pages

  Bleris, Leonidas ^a   Xie, Zhen ^b   Glass, David ^c   Adadey, Asa ^d   Sontag, Eduardo ^e   Benenson, Yaakov ^f  

^a The University of Texas at Dallas   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c PRINCETON UNIVERSITY   (United States)

^d UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^e RUTGERS UNIVERSITY   (United States)

^f ETH ZURICH   (Switzerland)

Author keywords

feedforward motifs; gene dosage and noise; mammalian cells; microRNAs; negative autoregulation

Indexed keywords

ARTICLE; DNA TEMPLATE; GENE DOSAGE; GENE EXPRESSION; GENETIC TRANSCRIPTION; MOLECULAR BIOLOGY; PRIORITY JOURNAL; STOICHIOMETRY; BIOLOGICAL MODEL; CELL STRAIN HEK293; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC DATABASE; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; METHODOLOGY; PLASMID; RNA INTERFERENCE; SYNTHETIC BIOLOGY;

MAMMALIA;

MICRORNA; TRANSCRIPTION FACTOR;

DATABASES, GENETIC; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HEK293 CELLS; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; PLASMIDS; RNA INTERFERENCE; SYNTHETIC BIOLOGY; TEMPLATES, GENETIC; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 80051486871     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2011.49     Document Type: Article

References (43)

1. Acar M, Pando BF, Arnold FH, Elowitz MB, van Oudenaarden A (2010) A general mechanism for network-dosage compensation in gene circuits. Science 329: 1656-1660
2. Balazsi G, Barabasi AL, Oltvai ZN (2005) Topological units of environmental signal processing in the transcriptional regulatory network of Escherichia coli. Proc Natl Acad Sci USA 102: 7841-7846 (Pubitemid 40781025)
3. Basu S, Mehreja R, Thiberge S, Chen MT, Weiss R (2004) Spatio-temporal control of gene expression with pulse-generating networks. Proc Natl Acad Sci USA 101: 6355-6360 (Pubitemid 38585978)
4. Becskei A, Serrano L (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590-593 (Pubitemid 30367734)
5. Blake WJ, Kaern M, Cantor CR, Collins JJ (2003) Noise in eukaryotic gene expression. Nature 422: 633-637 (Pubitemid 36460419)
6. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JR, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956 (Pubitemid 41345211)
7. Cantone I, Marucci L, Iorio F, Ricci MA, Belcastro V, Bansal M, Santini S, di Bernardo M, di Bernardo D, Cosma MP (2009) A yeast synthetic network for in vivo assessment of reverse-engineering and modeling approaches. Cell 137: 172-181
8. Cohen RN, van der Aa M, Macaraeg N, Lee AP, Szoka FC (2009) Quantification of plasmid DNA copies in the nucleus after lipoplex and polyplex transfection. J Control Release 135: 166-174
9. Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186 (Pubitemid 36193353)
10. Entus R, Aufderheide B, Sauro H (2007) Design and implementation of three incoherent feed-forward motif based biological concentration sensors. Syst Synth Biol 1: 119-128 (Pubitemid 351448386)
11. Goentoro L, Shoval O, Kirschner MW, Alon U (2009) The incoherent feedforward loop can provide fold-change detection in gene regulation. Mol Cell 36: 894-899
12. Holtz WJ, Keasling JD (2010) Engineering static and dynamic control of synthetic pathways. Cell 140: 19-23
13. Isaacs FJ, Hasty J, Cantor CR, Collins JJ (2003) Prediction and measurement of an autoregulatory genetic module. Proc Natl Acad Sci USA 100: 7714-7719 (Pubitemid 36760035)
14. Kaplan S, Bren A, Dekel E, Alon U (2008) The incoherent feed-forward loop can generate non-monotonic input functions for genes. Mol Syst Biol 4: 203
15. Keyomarsi K, Pardee AB (1993) Redundant cyclin overexpression and gene amplification in breast-cancer cells. Proc Natl Acad Sci USA 90: 1112-1116 (Pubitemid 23053961)
16. Kittisopikul M, Suel GM (2010) Biological role of noise encoded in a genetic network motif. Proc Natl Acad Sci USA 107: 13300-13305
17. Lee T, Rinaldi N, Robert F, Odom D, Bar-Joseph Z, Gerber G, Hannett N, Harbison C, Thompson C, Simon I, Zeitlinger J, Jennings E, Murray H, Gordon B, Ren B, Wyrick J, Tagne J-B, Volkert T, Fraenkel E, Gifford D et al (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804 (Pubitemid 35231527)
18. Leisner M, Bleris L, Lohmueller J, Xie Z, Benenson Y (2010) Rationally designed logic integration of regulatory signals in mammalian cells. Nat Nanotechnol 5: 666-670
19. Lu TK, Khalil AS, Collins JJ (2009) Next-generation synthetic gene networks. Nat Biotechnol 27: 1139-1150
20. Lucchesi JC, Kelly WG, Parming B (2005) Chromatin remodeling in dosage compensation. Ann Rev Genet 39: 615-651 (Pubitemid 43011128)
21. Ma WZ, Trusina A, El-Samad H, Lim WA, Tang C (2009) Defining network topologies that can achieve biochemical adaptation. Cell 138: 760-773
22. Ma'ayan A, Jenkins SL, Neves S, Hasseldine A, Grace E, Dubin-Thalere B, Eungdamrong NJ, Weng GZ, Ram PT, Rice JJ, Kershenbaum A, Stolovitzky GA, Blitzer RD, Iyengar R (2005) Formation of regulatory patterns during signal propagation in a mammalian cellular network. Science 309: 1078-1083 (Pubitemid 41134466)
23. Mangan S, Alon U (2003) Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA 100: 11980-11985 (Pubitemid 37271501)
24. Mangan S, Itzkovitz S, Zaslaver A, Alon U (2006) The incoherent feedforward loop accelerates the response-time of the gal system of Escherichia coli. J Mol Biol 356: 1073-1081 (Pubitemid 43199913)
25. McCullagh E, Farlow J, Fuller C, Girard J, Lipinski-Kruszka J, Lu D, Noriega T, Rollins G, Spitzer R, Todhunter M, El-Samad H (2009) Not all quiet on the noise front. Nat Chem Biol 5: 699-704
26. 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 (Pubitemid 35231534)
27. Nakamoto M, Jin P, O'Donnell WT, Warren ST (2005) Physiological identification of human transcripts translationally regulated by a specific microRNA. Hum Mol Genet 14: 3813-3821 (Pubitemid 43020083)
28. Ozbudak EM, Thattai M, Kurtser I, Grossman AD, van Oudenaarden A (2002) Regulation of noise in the expression of a single gene. Nat Genet 31: 69-73
29. Paulsson J (2004) Summingup the noise in gene networks. Nature 427: 415-418
30. Pollard H, Remy JS, Loussouarn G, Demolombe S, Behr JP, Escande D (1998) Polyethylenimine but not cationic lipids promotes trans-gene delivery to the nucleus in mammalian cells. J Biol Chem 273: 7507-7511 (Pubitemid 28152775)
31. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S (2006) Stochastic mRNA synthesis in mammalian cells. PLoS Biol 4: 1707-1719 (Pubitemid 44610091)
32. Raser JM, O'Shea EK (2005) Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013 (Pubitemid 41362308)
33. Rinaudo K, Bleris L, Maddamsetti R, Subramanian S, Weiss R, Benenson Y (2007) A universal RNAi-based logic evaluator that operates in mammalian cells. Nat Biotechnol 25: 795-801 (Pubitemid 47052185)
34. Russell RB, Aloy P (2008) Targeting and tinkering with interaction networks. Nat Chem Biol 4: 666-673
35. Schwake G, Youssef S, Kuhr JT, Gude S, David MP, Mendoza E, Frey E, Radler JO (2010) Predictive modeling of non-viral gene transfer. Biotechnol Bioeng 105: 805-813
36. 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
37. 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 107: 15995-16000
38. Sontag ED (2010) Remarks on feedforward circuits, adaptation, and pulse memory. IET Syst Biol 4: 39-51
39. Stenberg P, Lundberg LE, Johansson AM, Ryden P, Svensson MJ, Larsson J (2009) Buffering of segmental and chromosomal aneuploidies in Drosophila melanogaster. PLoS Genet 5: 10
40. Tsang J, Zhu J, van Oudenaarden A (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26: 753-767 (Pubitemid 46856248)
41. Tseng WC, Haselton FR, Giorgio TD (1997) Transfection by cationic liposomes using simultaneous single cell measurements of plasmid delivery and transgene expression. J Biol Chem 272: 25641-25647 (Pubitemid 27438879)
42. Tyson JJ, Chen KC, Novak B (2003) Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr Opin Cell Biol 15: 221-231 (Pubitemid 36332198)
43. Veitia RA, Bottani S, Birchler JA (2008) Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects. Trends Genet 24: 390-397