Construction of a genetic multiplexer to toggle between chemosensory pathways in Escherichia coli

Journal of Molecular Biology

Volumn 406, Issue 2, 2011, Pages 215-227

  Moon, Tae Seok ^a   Clarke, Elizabeth J ^a   Groban, Eli S ^a   Tamsir, Alvin ^a   Clark, Ryan M ^b   Eames, Matthew ^a   Kortemme, Tanja ^a   Voigt, Christopher A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b City Arts and Technology High School   (United States)

Author keywords

GFP; green fluorescent protein; National Science Foundation; NSF; RBS; red fluorescent protein; RFP; ribosome binding site

Indexed keywords

ARABINOSE; ASPARTIC ACID; GREEN FLUORESCENT PROTEIN; HISTIDINE; LEUCINE; METHIONINE; METHYLTRANSFERASE; PHOSPHATASE; RED FLUORESCENT PROTEIN; SERINE; THREONINE;

ARTICLE; BACTERIAL STRAIN; CHEMORECEPTOR; CHEMORECEPTOR REFLEX; CHEMOTAXIS; CONTROLLED STUDY; ESCHERICHIA COLI; FLOW CYTOMETRY; GENE INSERTION; GENE SWITCHING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SOMATOSENSORY SYSTEM;

ESCHERICHIA COLI; HARNESS;

EID: 79251595456     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.12.019     Document Type: Article

References (72)

1. Golden J.W., Robinson S.J., and Haselkorn R. Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena Nature 314 1985 419 423
2. van der Woude M.W., and Baumler A.J. Phase and antigenic variation in bacteria Clin. Microbiol. Rev. 17 2004 581 611
3. Cerdeno-Tarraga A.M., Patrick S., Crossman L.C., Blakely G., Abratt V., and Lennard N. Extensive DNA inversions in the B. fragilis genome control variable gene expression Science 307 2005 1463 1465
4. Sternberg N., and Hamilton D. Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites J. Mol. Biol. 150 1981 467 486
5. Friedland A.E., Lu T.K., Wang X., Shi D., Church G., and Collins J.J. Synthetic gene networks that count Science 324 2009 1199 1202
6. Baumgardner J., Acker K., Adefuye O., Crowley S.T., Deloache W., and Dickson J.O. Solving a Hamiltonian Path Problem with a bacterial computer J. Biol. Eng. 3 2009 11
7. Klemm P. Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli EMBO J. 5 1986 1389 1393
8. Gally D.L., Bogan J.A., Eisenstein B.I., and Blomfield I.C. Environmental regulation of the fim switch controlling type 1 fimbrial phase variation in Escherichia coli K-12: effects of temperature and media J. Bacteriol. 175 1993 6186 6193
9. McClain M.S., Blomfield I.C., and Eisenstein B.I. Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli J. Bacteriol. 173 1991 5308 5314
10. Ham T.S., Lee S.K., Keasling J.D., and Arkin A.P. A tightly regulated inducible expression system utilizing the fim inversion recombination switch Biotechnol. Bioeng. 94 2006 1 4
11. Ham T.S., Lee S.K., Keasling J.D., and Arkin A.P. Design and construction of a double inversion recombination switch for heritable sequential genetic memory PLoS One 3 2008 e2815
12. Becskei A., Seraphin B., and Serrano L. Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion EMBO J. 20 2001 2528 2535
13. Gardner T.S., Cantor C.R., and Collins J.J. Construction of a genetic toggle switch in Escherichia coli Nature 403 2000 339 342
14. Kobayashi H., Kaern M., Araki M., Chung K., Gardner T.S., Cantor C.R., and Collins J.J. Programmable cells: interfacing natural and engineered gene networks Proc. Natl Acad. Sci. USA 101 2004 8414 8419
15. Anderson J.C., Clarke E.J., Arkin A.P., and Voigt C.A. Environmentally controlled invasion of cancer cells by engineered bacteria J. Mol. Biol. 355 2006 619 627
16. Anderson J.C., Voigt C.A., and Arkin A.P. Environmental signal integration by a modular AND gate Mol. Syst. Biol. 3 2007 133
17. You L., Cox R.S. III, Weiss R., and Arnold F.H. Programmed population control by cell-cell communication and regulated killing Nature 428 2004 868 871
18. Sinha J., Reyes S.J., and Gallivan J.P. Reprogramming bacteria to seek and destroy an herbicide Nat. Chem. Biol. 6 2010 464 470
19. Topp S., and Gallivan J.P. Guiding bacteria with small molecules and RNA J. Am. Chem. Soc. 129 2007 6807 6811
20. Weiss L.E., Badalamenti J.P., Weaver L.J., Tascone A.R., Weiss P.S., Richard T.L., and Cirino P.C. Engineering motility as a phenotypic response to LuxI/R-dependent quorum sensing in Escherichia coli Biotechnol. Bioeng. 100 2008 1251 1255
21. Pawson T., and Scott J.D. Signaling through scaffold, anchoring, and adaptor proteins Science 278 1997 2075 2080
22. Zeke A., Lukács M., Lim W.A., and Reményi A. Scaffolds: interaction platforms for cellular signalling circuits Trends Cell Biol. 19 2009 364 374
23. Dickens M., Rogers J.S., Cavanagh J., Raitano A., Xia Z., and Halpern J.R. A cytoplasmic inhibitor of the JNK signal transduction pathway Science 277 1997 693 696
24. Garrington T.P., and Johnson G.L. Organization and regulation of mitogen-activated protein kinase signaling pathways Curr. Opin. Cell Biol. 11 1999 211 218
25. Xu S., and Cobb M.H. MEKK1 binds directly to the c-Jun N-terminal kinases/stress-activated protein kinases J. Biol. Chem. 272 1997 32056 32060
26. Park S.H., Zarrinpar A., and Lim W.A. Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms Science 299 2003 1061 1064
27. Baker M.D., Wolanin P.M., and Stock J.B. Signal transduction in bacterial chemotaxis BioEssays 28 2006 9 22
28. Gestwicki J.E., and Kiessling L.L. Inter-receptor communication through arrays of bacterial chemoreceptors Nature 415 2002 81 84
29. Gosink K.K., Buron-Barral M.C., and Parkinson J.S. Signaling interactions between the aerotaxis transducer Aer and heterologous chemoreceptors in Escherichia coli J. Bacteriol. 188 2006 3487 3493
30. Bourret R.B., and Stock A.M. Molecular information processing: lessons from bacterial chemotaxis J. Biol. Chem. 277 2002 9625 9628
31. Liu J.D., and Parkinson J.S. Genetic evidence for interaction between the CheW and Tsr proteins during chemoreceptor signaling by Escherichia coli J. Bacteriol. 173 1991 4941 4951
32. Maddock J.R., and Shapiro L. Polar location of the chemoreceptor complex in the Escherichia coli cell Science 259 1993 1717 1723
33. Greenfield D., McEvoy A.L., Shroff H., Crooks G.E., Wingreen N.S., Betzig E., and Liphardt J. Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy PLoS Biol. 7 2009 e1000137
34. Keymer J.E., Endres R.G., Skoge M., Meir Y., and Wingreen N.S. Chemosensing in Escherichia coli: two regimes of two-state receptors Proc. Natl Acad. Sci. USA 103 2006 1786 1791
35. Endres R.G., and Wingreen N.S. Precise adaptation in bacterial chemotaxis through "assistance neighborhoods" Proc. Natl Acad. Sci. USA 103 2006 13040 13044
36. Sourjik V., and Berg H.C. Functional interactions between receptors in bacterial chemotaxis Nature 428 2004 437 441
37. Liu J.D., and Parkinson J.S. Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis Proc. Natl Acad. Sci. USA 86 1989 8703 8707
38. Schulmeister S., Ruttorf M., Thiem S., Kentner D., Lebiedz D., and Sourjik V. Protein exchange dynamics at chemoreceptor clusters in Escherichia coli Proc. Natl Acad. Sci. USA 105 2008 6403 6408
39. Kwon O., Georgellis D., and Lin E.C. Rotational on-off switching of a hybrid membrane sensor kinase Tar-ArcB in Escherichia coli J. Biol. Chem. 278 2003 13192 13195
40. Michalodimitrakis K.M., Sourjik V., and Serrano L. Plasticity in amino acid sensing of the chimeric receptor Taz Mol. Microbiol. 58 2005 257 266
41. Utsumi R., Brissette R.E., Rampersaud A., Forst S.A., Oosawa K., and Inouye M. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate Science 245 1989 1246 1249
42. Ward S.M., Delgado A., Gunsalus R.P., and Manson M.D. A NarX-Tar chimera mediates repellent chemotaxis to nitrate and nitrite Mol. Microbiol. 44 2002 709 719
43. Derr P., Boder E., and Goulian M. Changing the specificity of a bacterial chemoreceptor J. Mol. Biol. 355 2006 923 932
44. Villalobos A., Ness J.E., Gustafsson C., Minshull J., and Govindarajan S. Gene Designer: a synthetic biology tool for constructing artificial DNA segments BMC Bioinformatics 7 2006 285
45. Cardozo M.J., Massazza D.A., Parkinson J.S., and Studdert C.A. Disruption of chemoreceptor signaling arrays by high level of chew, the receptor-kinase coupling protein Mol. Microbiol. 75 2010 1171 1181
46. Weiss R. Cellular Computation and Communications Using Engineered Genetic Regulatory Networks 2001 Massachusetts Institute of Technology Cambridge, MA
47. Boukhvalova M.S., Dahlquist F.W., and Stewart R.C. CheW binding interactions with CheA and Tar. Importance for chemotaxis signaling in Escherichia coli J. Biol. Chem. 277 2002 22251 22259
48. Levit M.N., Grebe T.W., and Stock J.B. Organization of the receptor-kinase signaling array that regulates Escherichia coli chemotaxis J. Biol. Chem. 277 2002 36748 36754
49. Goldberg S.D., Derr P., DeGrado W.F., and Goulian M. Engineered single- and multi-cell chemotaxis pathways in E. coli Mol. Syst. Biol. 5 2009 283
50. Adler J., and Templeton B. The effect of environmental conditions on the motility of Escherichia coli J. Gen. Microbiol. 46 1967 175 184
51. Lai H.C., Shu J.C., Ang S., Lai M.J., Fruta B., and Lin S. Effect of glucose concentration on swimming motility in enterobacteria Biochem. Biophys. Res. Commun. 231 1997 692 695
52. Hamer R., Chen P.Y., Armitage J.P., Reinert G., and Deane C.M. Deciphering chemotaxis pathways using cross species comparisons BMC Syst. Biol. 4 2010 3
53. Tran H.T., Krushkal J., Antommattei F.M., Lovley D.R., and Weis R.M. Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function BMC Genomics 9 2008 471
54. Martin A.C., Wadhams G.H., and Armitage J.P. The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides Mol. Microbiol. 40 2001 1261 1272
55. Mandell D.J., and Kortemme T. Computer-aided design of functional protein interactions Nat. Chem. Biol. 5 2009 797 807
56. Kortemme T., Joachimiak L.A., Bullock A.N., Schuler A.D., Stoddard B.L., and Baker D. Computational redesign of protein-protein interaction specificity Nat. Struct. Mol. Biol. 11 2004 371 379
57. Bolon D.N., Grant R.A., Baker T.A., and Sauer R.T. Specificity versus stability in computational protein design Proc. Natl Acad. Sci. USA 102 2005 12724 12729
58. Skerker J.M., Perchuk B.S., Siryaporn A., Lubin E.A., Ashenberg O., Goulian M., and Laub M.T. Rewiring the specificity of two-component signal transduction systems Cell 133 2008 1043 1054
59. Alves R., and Savageau M.A. Comparative analysis of prototype two-component systems with either bifunctional or monofunctional sensors: differences in molecular structure and physiological function Mol. Microbiol. 48 2003 25 51
60. Groban E.S., Clarke E.J., Salis H.M., Miller S.M., and Voigt C.A. Kinetic buffering of cross talk between bacterial two-component sensors J. Mol. Biol. 390 2009 380 393
61. Siryaporn A., and Goulian M. Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli Mol. Microbiol. 70 2008 494 506
62. Voigt K., Izsvak Z., and Ivics Z. Targeted gene insertion for molecular medicine J. Mol. Med. 86 2008 1205 1219
63. Buchholz F., Angrand P.O., and Stewart A.F. Improved properties of FLP recombinase evolved by cycling mutagenesis Nat. Biotechnol. 16 1998 657 662
64. Buchholz F., and Stewart A.F. Alteration of Cre recombinase site specificity by substrate-linked protein evolution Nat. Biotechnol. 19 2001 1047 1052
65. Santoro S.W., and Schultz P.G. Directed evolution of the site specificity of Cre recombinase Proc. Natl Acad. Sci. USA 99 2002 4185 4190
66. Sarkar I., Hauber I., Hauber J., and Buchholz F. HIV-1 proviral DNA excision using an evolved recombinase Science 316 2007 1912 1915
67. Oberdoerffer P., Otipoby K.L., Maruyama M., and Rajewsky K. Unidirectional Cre-mediated genetic inversion in mice using the mutant loxP pair lox66/lox71 Nucleic Acids Res. 31 2003 e140
68. Steen E.J., Kang Y., Bokinsky G., Hu Z., Schirmer A., and McClure A. Microbial production of fatty-acid-derived fuels and chemicals from plant biomass Nature 463 2010 559 562
69. Datsenko K.A., and Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl Acad. Sci. USA 97 2000 6640 6645
70. Gibson D.G., Young L., Chuang R.Y., Venter J.C., Hutchison C.A. III, and Smith H.O. Enzymatic assembly of DNA molecules up to several hundred kilobases Nat. Methods 6 2009 343 345
71. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., and Tsien R.Y. A monomeric red fluorescent protein Proc. Natl Acad. Sci. USA 99 2002 7877 7882
72. Temme K., Salis H., Tullman-Ercek D., Levskaya A., Hong S.H., and Voigt C.A. Induction and relaxation dynamics of the regulatory network controlling the type III secretion system encoded within Salmonella pathogenicity island 1 J. Mol. Biol. 377 2008 47 61