Use of two-component signal transduction systems in the construction of synthetic genetic networks

Current Opinion in Microbiology

Volumn 13, Issue 2, 2010, Pages 240-245

  Ninfa, Alexander J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE;

CELL FUNCTION; CHEMOTAXIS; GENE CONTROL; GENETIC ENGINEERING; NONHUMAN; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GENETIC ENGINEERING; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI;

PROKARYOTA;

EID: 77949918369     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2010.01.003     Document Type: Review

References (58)

1. Kaern M., Blake W.J., and Collins J.J. The engineering of gene regulatory networks. Annu Rev Biomed Eng 5 (2003) 179-206. An early review nicely stating the goals and methods of synthetic biology.
2. Endy D. Foundations for engineering biology. Nature 438 (2005) 449-453
3. Andrianantoandro E., Basu S., Karig D.K., and Weiss R. Synthetic biology: new engineering rules for an emerging discipline. Mol Syst Biol 2 (2006) 0028
4. Levskaya A., Chevalier A.A., Tabor J.L., Simpson Z.B., Lavery L.A., Levy M., Davidson E.A., Scouras A., Ellington A.D., Marcotte E.M., and Voigt C.A. Engineering Escherichia coli to see light. Nature 438 (2005) 441-442. A dramatic example of grafting of sensory capabilities.
5. Elowitz M.B., and Leibler S. A synthetic oscillator network of transcriptional regulators. Nature 403 (2000) 335. This work was one of the initial efforts in the field of synthetic biology.
6. Atkinson M.R., Savageau M.A., Meyers J.T., and Ninfa A.J. Development of genetic circuitry exhibiting toggle switch or oscillatory behavior in Escherichia coli. Cell 113 (2003) 597-607. Early devices in the field of synthetic biology that function as toggle switches and clocks in large cell populations.
7. Fung E., Wong W.W., Suen J.K., Bulter T., Lee S.G., and Liao J.C. A synthetic gene-metabolic oscillator. Nature 435 (2005) 118-122
8. •] that appears to work much better.
9. Gardner T.S., Cantor C.R., and Collins J.J. Construction of a genetic toggle switch in Escherichia coli. Nature 403 (2000) 339-342. This work was one of the first examples of a synthetic genetic device that functioned very well and could later be used as a module in larger synthetic genetic networks.
10. Tropynina T.S., Golubev O.V., Stupak E.E., and Tchuraev R.N. Construction of an artifi{ligature}cial digenic network with epigenetic properties. Mol Biol 36 (2002) 472-475
11. Basu S., Gerchman Y., Collins C.H., Arnold F.H., and Weiss R. A synthetic multicellular system for programmed pattern formation. Nature 434 (2005) 1130-1134
12. Basu S., Mehreja R., Thiberge S., Chen M.-T., and Weiss R. Spatiotemporal control of gene expression with pulse-generating networks. Proc Natl Acad Sci U S A 101 (2004) 6355-6360
13. Kobayashi H., Kærn 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 U S A 101 (2004) 8414-8419. A very clear demonstration of the basic goals and methods of synthetic biology.
14. Tabor J.J., Salis H.M., Simpson Z.B., Chevalier A.A., Levskaya A., Marcotte E.M., Voigt C.A., and Ellington A.D. A synthetic genetic edge detection program. Cell 137 (2009) 1272-1281
15. You L., Cox R.S., Weiss R., and Arnold F.H. Programmed population control by cell-cell communication and regulated killing. Nature 428 (2004) 868-871
16. Ro D.K., Paradise E.M., Ouellet M., Fisher K.J., Newman K.L., Ndungu J.M., Ho K.A., Eachus R.A., Ham T.S., Kirby J., et al. Production of the antimalarial drug precursor artemieinic acid in engineered yeast. Nature 440 (2006) 940-943. This inspirational work shows the potential social benefits that the synthetic biology approach may provide.
17. Ninfa A.J., and Magasanik B. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A 83 (1986) 5909-5913. This work provides the first demonstration of the signaling mechanisms used by two-component systems.
18. Jiang P., Atkinson M.R., Srisawat C., Sun Q., and Ninfa A.J. Functional dissection of the dimerization and enzymatic activities of Escherichia coli nitrogen regulator II and their regulation by the PII protein. Biochemistry 39 (2000) 13433-13449
19. Yoshida T., Cai S., and Inouye M. Interaction of EnvZ, a sensory histidine kinase, with phosphorylated OmpR, the cognate response regulator. Mol Microbiol 46 (2002) 1283-1294
20. Igo M.M., Ninfa A.J., Stock J.B., and Silhavy T.J. Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev 3 (1989) 1725-1734
21. Hsing W., Russo F.D., Bernd K.K., and Silhavy T.J. Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J Bacteriol 180 (1998) 4538-4546
22. Lois A.F., Weinstein M., Ditta G.S., and Helinski D.R. Autophosphorylation and phosphatase activities of the oxygen-sensing protein FixL of Rhizobium meliloti are coordinately regulated by oxygen. J Biol Chem 268 (1993) 4370-4375
23. Carmany D.O., Hollingsworth K., and McCleary W.R. Genetic and biochemical studies of phosphatase activity of PhoR. J Bacteriol 185 (2003) 1112-1115
24. Perego M. Kinase-phosphatase competition regulates Bacillus subtilis development. Trends Microbiol 6 (1998) 366-370
25. Perego M. A new family of aspartyl phosphate phosphatases targeting the sporulation transcription factor Spo0A of Bacillus subtilis. Mol Microbiol 42 (2001) 133-143
26. Hoch J.A., and Varughese K.I. Keeping signals straight in phosphorelay signal transduction. J Bacteriol 183 (2001) 4941-4949
27. Skerker J.M., Perchuk B.S., Siyaporn 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
28. Laub M.T., and Goulian M. Specificity in two component signal transduction pathways. Annu Rev Genet 41 (2007) 121-145
29. Ninfa A.J., Ninfa E.G., Lupas A.N., Stock A., Magasanik B., and Stock J. Crosstalk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proc Natl Acad Sci U S A 85 (1988) 5492-5496
30. Wanner B.L. Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria?. J Bacteriol 174 (1992) 2053-2058
31. Gilles-Gonzalez M.A., Gonzalez G., and Perutz M. Kinase activity of the oxygen sensor FixL depends on the spin state of its heme iron. Biochemistry 34 (1995) 232-236. An early biochemical demonstration of a sensory mechanism.
32. Garnerone A.M., Cabanes D., Foussard M., Boistard P., and Batut J. Inhibition of the FixL sensor kinase by the FixT protein in Sinorhizobium meliloti. J Biol Chem 274 (1999) 32500-32506
33. Crosson S., McGrath P.T., Stephens C., McAdams H.H., and Shapiro L. Conserved modular design of an oxygen sensory/signaling network with species-specific output. Proc Natl Acad Sci U S A 102 (2005) 8018-8023
34. Shimoda N., Toyoda-Yammamoto A., Nagamine J., Usami S., Katayama M., Sakagami Y., and Machida Y. Control of expression of Agrobacterium vir genes by synergistic actions of phenolic signal molecules and monosaccharides. Proc Natl Acad Sci U S A 87 (1990) 6684-6688
35. Wang L., Grau R., Perego M., and Hoch J.A. A novel histidine kinase inhibitor regulating development in Bacillus subtilis. Genes Dev 11 (1997) 2569-2579
36. Mascher T., Helmann J.D., and Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70 (2006) 910-938
37. Bray D., Levin M.D., and Morton-Firth C.F. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393 (1998) 85-88
38. 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. This work demonstrated the possibility of grafting sensory capabilities onto two-component regulatory systems.
39. Appleman A.J., Chen L.-L., and Stewart V. Probing conservation of HAMP linker structure and signal transduction mechanism through the analysis of hybrid sensor kinases. J Bacteriol 185 (2003) 4872-4882
40. 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
41. Xu Q., Black W.P., Ward S.M., and Yang Z. Nitrate-dependent activation of Dif signaling pathway of Myxococcus xanthus mediated by a NarX-DifA interspecies chimera. J Bacteriol 187 (2005) 6410-6418
42. Xu Q., Black W.P., Mauriello E.M.F., Zusman D.R., and Yang Z. Chemotaxis mediated by NarX-FrzCD chimeras and nonadapting repellent responses in Myxococcus xanthus. Mol Microbiol 66 (2007) 1370-1381
43. Kwon O., Georgellis D., and Lin E.C.C. Rotational on-off switching of a hybrid membrane sensor kinase Tar-ArcB in Escherichia coli. J Biol Chem 278 (2003) 13192-13196
44. Cheung J., Bingman C.A., Reyngold M., Hendrickson W.A., and Waldburger C.D. Crystal structure of a functional dimer of the PhoQ sensor domain. J Biol Chem 283 (2008) 13762-13770
45. Cheung J., and Hendrickson W.A. Crystal structures of C4-dicarboxylate ligand complexes with sensor domains of histidine kinases DcuS and DctB. J Biol Chem 283 (2008) 30256-30265
46. Zhou Y.F., Nan B., Nan J., Ma Q., Panjikar S., Liang Y.H., Wang Y., and Su X.D. C4-dicarboxylates sensing mechanism revealed by the crystal structures of DctB sensor domain. J Mol Biol 383 (2008) 49-61
47. Reinelt S., Hofmann E., Gerharz T., Bott M., and Madden D.R. The structure of the periplasmic ligand-binding domain of the sensor kinase CitA reveals the first extracellular PAS domain. J Biol Chem 278 (2003) 39189-39196
48. ••], this work illustrates additional approaches for engineering new sensory capabilities.
49. Verhamme D.T., Arents J.C., Postma P.W., Crielaard W., and Hellingwerf K.J. Glucose-6-phosphate-dependent phosphoryl flow through the Uhp two-component regulatory system. Microbiology 147 (2001) 3345-3352
50. Moglich A., Ayers R.A., and Moffat K. Design and signaling mechanism of light-regulated histidine kinases. J Mol Biol 385 (2009) 1433-1444. Demonstration of grafting sensory function of a PAS domain (of the type containing a flavin and known as a LOV domain). Given the huge number of PAS domains in nature, many sensory capabilities may be grafted in this fashion.
51. 2 sensor domain of FixL and histidine kinase domain from a thermophile. Biochem Biophys Acta 1646 (2003) 136-144
52. Cunningham K.A., and Burkholder W.F. The histidine kinase inhibitor Sda binds near the site of autophosphorylation and may sterically hinder autophosphorylation and phosphotransfer to Spo0F. Mol Microbiol 71 (2009) 659-677
53. Pioszak A.A., and Ninfa A.J. The Escherichia coli PII signal transduction protein regulates the activities of the two-component systems transmitter protein NRII by direct interaction with the kinase domain of the transmitter module. Biochemistry 39 (2000) 13450-13461
54. Song Y., Peisach D., Pioszak A.A., Xu Z., and Ninfa A.J. Crystal structure of the C-terminal domain of the two-component system transmitter protein nitrogen regulator II (NRII; NtrB), regulator of nitrogen assimilation in Escherichia coli. Biochemistry 43 (2004) 6670-6678
55. Pioszak A.A., and Ninfa A.J. Mechanism of the PII-activated phosphatase activity of Escherichia coli NRII (NtrB): how the different domains of NRII collaborate to act as a phosphatase. Biochemistry 42 (2003) 8885-8899
56. Ninfa A.J., and Jiang P. PII signal transduction proteins: sensors of alpha-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8 (2005) 168-173
57. Sprinzak D., and Elowitz M.B. Reconstruction of genetic circuits. Nature 438 (2005) 443-448. This work offers a glimpse of possible future uses of synthetic biology approaches to study natural genetic networks.
58. 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. This work demonstrated the possibility of grafting sensory capabilities onto two-component regulatory systems.